make a study guide for the exam on infant development. the first file is the study questions by the instructor, use some short sentences to answer those questions, the other files are the readings address to some questions, you only need to read the abstract for most of the questions, for some questions not in the readings, you could find it online.

Psychology 104 (N. Akhtar) Study Guide for Exam I

This exam covers material from lectures 1/6 through 1/29, and the following articles: Morelli et al. (1992),
Keller et al. (2009), Cirelli et al. (2014), Waters et al. (2014), Hepper (2015), Sandman et al. (2012),
Brubaker et al. (2019), Howarth et al. (2019), Byers-Heinlein et al. (2010), Suberi et al. (2017), Redshaw
et al. (2019), Gao et al. (2018), Betancourt et al. (2016), Graham et al. (2013), Xiao et al. (2017), Karasik et
al. (2015), Cole et al. (2012)

Introduction: Nature of Development, Social Ecology of Infancy
1. Explain what is meant by the following contrasts: nature vs. nurture, continuity vs. discontinuity,

vulnerability vs. resilience. Why is the nature/nurture contrast a false dichotomy?
2. What 3 characteristics distinguish developmental changes from other types of change?
3. How do prospective studies of risk factors overcome some of the weaknesses of retrospective studies of risk

factors?
4. Discuss the resilience of some of the children in the Werner (1989) study. What kinds of things served as

protective factors?
5. Describe the notion of “good enough parenting.”
6. List and describe three ways in which a child’s genes can influence his/her experiences.
7. Describe a cross-cultural difference in parents’ behavior and how it relates to differences in parents’ beliefs

about who is primarily responsible for infants’ and toddlers’ learning. What other factor (other than beliefs)
may also play a role in these behavioral differences?

8. Morelli et al. (1992) studied variations in sleeping arrangements in two communities. How do the parents
explain their decisions on where their children should sleep? In which society did more children tend to use
transition objects and bedtime rituals to help them fall asleep?

9. Keller et al. (2009) describe two styles of parenting infants. What are they called and what are their main
characteristics?

10. What is epigenetics? How do the agouti mice demonstrate that prenatal experience can affect gene
expression? In general, what environmental factors are known to influence gene expression?

11. List several factors that may play a role in the relationship between siblings.
12. Describe with an example what it means to say that siblings experience different “micro-environments”

within the family.

Methods of Research
1. Explain, with an example, why one cannot infer a causal relationship when 2 variables are correlated.
2. Explain the logic of the habituation technique with an example. What can we conclude when infants
dishabituate?
3. Describe the different research designs for measuring developmental change (cross-sectional and

longitudinal) and list their advantages and disadvantages.
4. What two types of studies do developmental behavioral geneticists conduct?
5. Describe some of the special challenges involved in doing research with infants.
6. What is the difference between experimental and observational methods of research? What is the main

advantage of experimental studies?
7. What was Cirelli et al.’s (2014) main finding? How did they show that contingency and not mirroring was

responsible for this finding?
8. What are the two behaviors young infants have the most control over? Give some examples of how these

behaviors have been used in empirical research on infants’ capabilities.
9. What is “converging evidence”?
10. What makes scientific research on babies different from the knowledge people gain from their own

interactions with babies?
11. How did Waters et al. (2014) show that maternal stress can be “contagious” to their infants?

Prenatal Development and Birth
1. List the 3 stages of prenatal development and the major developmental change that occurs in each stage.
2. Discuss the problems in interpreting correlations between prenatal risk factors (e.g., maternal stress) and
developmental problems in the baby.
3. What is the “fetal origins hypothesis”? List 4 kinds of developments linked to prenatal experiences.
4. What are teratogens? Does the timing of exposure to teratogens matter?
5. Describe DeCasper and Spence’s (1986) landmark study demonstrating that newborns can

“remember”/recognize auditory events they were exposed to in utero. How did DeCasper et al. (1994)
extend these findings? What was their main dependent measure?

6. What is the predictive-adaptive response model? Did Sandman et al.’s (2012) findings support this model?
7. What are the three main stages of labor?
8. What is the most common birth position for laboring mothers in most of the world’s societies?
9. What was the main finding of Howarth et al.’s (2019) study of first-time fathers?
10. What were the main findings of Brubaker et al. (2019)? Was this an observational or an experimental study?

Neonatal Development
1. What is the Apgar score? What does it tell us about the health of a newborn?
2. List and describe 4 reflexes that have clear survival value and 4 reflexes that are not necessary for survival.
3. Describe Meltzoff and Moore’s studies of neonatal imitation – why were their results so surprising?
4. What was Redshaw et al.’s (2019) main finding? Was this a longitudinal or cross-sectional study?
5. What are some ways to soothe a crying infant?
6. What is “feeding imprinting”? What were Suberi et al.’s (2017) main findings?
7. According to Gao et al. (2018), what 2 things help preterm newborns deal with pain? Was one more

effective than the other? Was the combination of these 2 things more effective than either alone?
8. What was new about the Byers-Heinlein et al. (2010) study? What were their two main findings?

Neuropsychological Development
1. What are some of the effects of “deprivation” and “enrichment” studies with animals? What do they

illustrate about the nature of normal brain development?
2. Know the meanings of these terms: neurons, dendrites, synapses, glial cells, myelinization, plasticity.
3. List and describe the 4 stages of neural development.
4. Describe the Kennard principle about the early plasticity of the brain and discuss how it has been qualified

by studies with rats.
5. Distinguish between the effects of radiation and alcohol on the developing fetal brain.
6. Describe how functional (behavioral) changes and structural changes in the brain are reciprocal.
7. What factors associated with low SES are believed to affect brain development? What were Betancourt et

al.’s (2016) main findings?
8. How did Graham et al. (2013) demonstrate the relation between interparental conflict and infants’

processing of tone of voice? What do these findings tell us about sleeping infants?

Perceptual and Motor Development
1. What do young babies like to look at?
2. What is meant by cross-modal perception? Describe 2 studies illustrating cross-modal perception in infants.
3. What is the perceptual narrowing hypothesis? Give examples from both auditory and visual domains.
4. What were Xiao et al.’s (2017) main findings?
5. How do Karasik et al.’s (2015) findings provide evidence for both cultural differences as well as individual

differences in independent sitting ability?
6. Distinguish between gross motor development and fine motor development. Which comes first?
7. Can motor development can be influenced by experience? Provide examples.
8. Distinguish between the ulnar grasp and the pincer grasp.
9. What were Cole et al.’s (2012) main findings when they compared walking with and without diapers?

SHORT PAPER

Interpersonal synchrony increases prosocial behavior in infants

Laura K. Cirelli,1 Kathleen M. Einarson1 and Laurel J. Trainor1,2,3

1. Department of Psychology, Neuroscience & Behaviour, McMaster University, Canada
2. McMaster Institute for Music and the Mind, McMaster University, Canada
3. Rotman Research Institute, Baycrest Hospital, Toronto, Canada

Abstract

Adults who move together to a shared musical beat synchronously as opposed to asynchronously are subsequently more
likely to display prosocial behaviors toward each other. The development of musical behaviors during infancy has been
described previously, but the social implications of such behaviors in infancy have been little studied. In Experiment 1, each
of 48 14-month-old infants was held by an assistant and gently bounced to music while facing the experimenter, who
bounced either in-synchrony or out-of-synchrony with the way the infant was bounced. The infants were then placed in a
situation in which they had the opportunity to help the experimenter by handing objects to her that she had ‘accidently’
dropped. We found that 14-month-old infants were more likely to engage in altruistic behavior and help the experimenter
after having been bounced to music in synchrony with her, compared to infants who were bounced to music asynchronously
with her. The results of Experiment 2, using anti-phase bouncing, suggest that this is due to the contingency of the
synchronous movements as opposed to movement symmetry. These findings support the hypothesis that interpersonal motor
synchrony might be one key component of musical engagement that encourages social bonds among group members, and
suggest that this motor synchrony to music may promote the very early development of altruistic behavior.
A video abstract of this article can be viewed at http://www.youtube.com/watch?v=IaqWehfDm7c&feature=youtu.be

Research highlights

• Moving to music in synchrony with an adult
increases 14-month-old infants’ helpfulness

• Prosocial effects of interpersonal movement develop
early

• Congruent movement synchrony has the same pro-
social effect as mirrored synchrony

Introduction

Music is present at social events such as religious
ceremonies, military activities, and celebrations where
within-group social affiliation, emotional bonding, and
sharing common goals are desirable (Dissanayake, 2006).
The steady underlying beat that can be extracted from
music encourages entrained motor movements (Fujioka,

Trainor, Large & Ross, 2012; Large, 2000), and recent
studies suggest that adults who engage in a task that
encourages high levels of interpersonal motor synchrony
later display heightened affiliative behaviors toward one
another. For example, synchronized walking, singing,
and finger tapping lead to increased cooperative behav-
iors and higher ratings of likeability among those
involved (Anshel & Kippler, 1988; Hove & Risen, 2009;
Launay, Dean & Bailes, 2013; Valdesolo, Ouyang &
DeSteno, 2010; Wiltermuth & Heath, 2009). This effect
of interpersonal synchrony on prosocial behaviors that
influence social cohesion may result from perceptual and
attentional biases toward synchronous counterparts
(Macrae, Duffy, Miles & Lawrence, 2008; Woolhouse &
Tidhar, 2010), or from appraisals of self-similarity
among synchronous group members (Valdesolo &
DeSteno, 2011). One study suggests that music also
influences social behavior during childhood. Children
who participated in a musical game later played together

Address for correspondence: Laurel J. Trainor, Department of Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, ON L8S 4K1,
Canada; e-mail: LJT@mcmaster.ca

© 2014 John Wiley & Sons Ltd

Developmental Science 17:6 (2014), pp 1003–1011 DOI: 10.1111/desc.12193

in a more helpful and cooperative manner than children
who participated in a non-musical game (Kirschner &
Tomasello, 2010), although the specific role of interper-
sonal synchrony was not measured in this study. Here we
test whether interpersonal synchrony promotes prosocial
behavior in infancy.
Some aspects of sophisticated musical processing

develop early. Young infants prefer musically consonant
over dissonant sounds (Trainor, Tsang & Cheung, 2002),
they can remember and detect changes in melodies
(Plantinga & Trainor, 2009), rhythms (Chang & Trehub,
1977), and timbres (Trainor, Lee & Bosnyak, 2011), and
by 1 year of age, they show evidence of enculturation to
the timing structures and pitch classes used in the music
of their culture (Gerry, Unrau & Trainor, 2012; Hannon
& Trehub, 2005; Trainor & Trehub, 1992). Furthermore,
early musical processing is influenced by interactions
between auditory and motor systems. Infants bounced to
an ambiguous rhythm pattern on either every second or
every third beat subsequently preferred to listen to the
version of that pattern with accented beats matching the
pattern to which they had been bounced (Phillips-Silver
& Trainor, 2005). Infants who took part in active
participatory parent-and-infant music classes showed
enhanced musical processing, heightened brain responses
to sound, and increased use of prelinguistic gestures after
participation, in comparison to infants who were
assigned randomly to classes where music was experi-
enced passively in the background (Gerry et al., 2012;
Trainor, Marie, Gerry, Whiskin & Unrau, 2012). Most
relevantly, infants in the active participatory
music-making group also showed more positive social-
emotional development.
By their first birthday, infants are also becoming

active social agents, who understand that the behavior
of others can be goal-directed (see Sommerville &
Woodward, 2010, for a review). They are beginning to
engage in coordinated activities that require joint
attention with another individual (see Moore & Dun-
ham, 1995; Tomasello, Carpenter, Call, Behne & Moll,
2005, for reviews). For example, 12-month-old infants
will point to an object in order to inform another
person of its whereabouts (Liszkowski, Carpenter, Stri-
ano & Tomasello, 2006; Liszkowski, Carpenter &
Tomasello, 2008). Altruistic behavior is also emerging
at this age; 14-month-olds are motivated to help an
experimenter by returning objects that have been
dropped (Warneken & Tomasello, 2006, 2007). Young
infants quickly form preferences for social agents that
help others (Hamlin, Wynn & Bloom, 2007; Hamlin &
Wynn, 2012) and visual cues such as attractiveness,
gender, and self-similarity influence their social prefer-
ences (Kelly, Liu, Ge, Quinn, Slater, Lee, Liu & Pascalis,

2007; Kinzler, Dupoux & Spelke, 2007; Langlois &
Roggman, 1987; Quinn, Yahr, Kuhn, Slater & Pascalis,
2002). Twenty-one-month-olds even direct their instru-
mental helping behaviors toward adults who previously
attempted to provide a toy, regardless of whether the
adult succeeded (Dunfield & Kuhlmeier, 2010).
Although these children were somewhat older than the
infants in the present investigation, these findings
suggest that social interactions can later influence infant
instrumental helpfulness.
The goal of the present investigation was to determine

whether 14-month-old infants use interpersonal motor
synchrony in the context of musical engagement as a cue
to direct their own prosocial behaviors. If infants are
similar to adults, moving to music in synchrony with an
adult should encourage infants to feel similar to and/or
attentive toward this adult (Macrae et al., 2008; Valde-
solo & DeSteno, 2011). This should increase later
prosociality directed toward this adult. On the other
hand, bouncing asynchronously with an adult should
not increase prosociality. We therefore hypothesized that
infants would be more likely to display helping behaviors
toward an experimenter following an experience of
interpersonal synchrony as opposed to interpersonal
asynchrony.
We also investigated whether the predictability of the

musical movement was important. Typically, musical
engagement involves temporal alignment of movements
to evenly spaced, predictable beats. Like interpersonal
synchrony, being able to predict another person’s move-
ments could make person-perception easier, which could
then influence later social behavior. In all previous
research on the influence of interpersonal musical engage-
ment on social behavior, synchronyand predictability have
either been confounded (Kirschner & Tomasello, 2010), or
predictability has been held constant across synchronous
and asynchronous conditions (e.g., Hove & Risen, 2009;
Valdesolo et al., 2010; Wiltermuth & Heath, 2009). To
investigate the influence of movement predictability on
prosociality, we compared the helping rates of infants
bounced to music with evenly spaced (isochronous) and
therefore predictable beats to the helping rates of infants
bounced to music with unevenly spaced, unpredictable
beats.
To investigate these questions, the assistant held and

bounced each infant to music while facing the experi-
menter (see Figure 1 and Movie S1). The infant
watched the experimenter, who bounced either
in-synchrony or out-of-synchrony with the way the
infant was being bounced. To examine the role of
movement predictability, the assistant and experimenter
either bounced to an evenly spaced, predictable beat
while the infant listened to the original version of the

© 2014 John Wiley & Sons Ltd

1004 Laura K. Cirelli et al.

song, or they bounced to an unevenly spaced, unpre-
dictable beat while the infant listened to a version of the
song distorted in time such that beat-to-beat onsets
varied randomly. After this, we tested the infants’
willingness to help the experimenter with whom they
had previously bounced. Specifically, we measured
whether infants would hand back objects to the exper-
imenter that she had ‘accidentally’ dropped, following
the work of Warneken and Tomasello (2007), which
shows that 14-month-olds understand the experi-
menter’s intentions, and will sometimes display such
spontaneous instrumental helping behaviors.

Experiment

1

Participants

Infants were recruited from the Developmental Studies
Database at McMaster University. Forty-eight walking
infants from English-speaking homes (24 girls; M age =
14.2 months; SD = 0.2 months) completed the experi-
ment. An additional 14 infants were excluded because of
excessive fussiness (n = 10) or equipment failure (n = 4).
The McMaster Research Ethics Board (MREB)
approved all experimental procedures. Informed consent
was obtained from all parents.

Phase 1: Interpersonal Movement Phase

Stimuli

Infants heard a 145 s Musical Instrument Digital
Interface (MIDI) version of ‘Twist and Shout’ (by The
Beatles) played over loudspeakers. Infants in the ‘evenly
spaced (predictable) beats’ conditions heard the original
version of this track (beats per minute (BPM) = 129;
Audio S1). Infants in the ‘unevenly spaced (unpredict-
able) beats’ conditions heard the modified version of this
track, in which the inter-beat intervals changed after
each successive beat (Audio S2; SI has stimuli creation
details). In this case, because the time interval between
beats varied randomly, it was not possible to predict the
time of the next beat. The tracks were MIDI generated,
so there was no acoustic distortion associated with the
tempo changes.

While the infant listened to one of the two versions of
‘Twist and Shout’, the assistant and experimenter
listened to wood block beats on ‘bounce instruction
tracks’ via headphones. These beats were either synchro-
nous or asynchronous with the version of ‘Twist and
Shout’ to which the infant was bounced. Thus there were
four bounce conditions: synchronous bouncing/evenly
spaced beats; synchronous bouncing/unevenly spaced
beats; asynchronous bouncing/evenly spaced beats;
asynchronous bouncing/unevenly spaced beats. The
assistant and experimenter were instructed to bounce
by bending at the knees, so that the lowest point of their
bounce aligned temporally with the woodblock sounds.
See SI for details on beat track creation, and for analyses
that verified that the assistant and experimenter bounced
at the appropriate times.

Procedure

Upon arrival, the assistant interacted with the infant
while the experimenter explained the procedure to the

(a)

(b) (c)

Figure 1 Between-subject conditions during the
Interpersonal Movement Phase. (a) A visual representation of
how infants were bounced over time. Arrows represent the
downbeat, or the lowest point of the assistant’s and the
experimenter’s bounce. In the evenly spaced beats conditions
(shown in black), downbeats were isochronous and
predictable. In the unevenly spaced beats conditions (shown in
gray), the spacing between downbeats varied randomly among
11 preset inter-downbeat-intervals. The assistant and
experimenter either bounced (b) synchronously or (c)
asynchronously. In the evenly spaced beats + asynchrony
condition, the experimenter bounced 33% faster or slower
than the assistant holding the infant. In the unevenly spaced
beats + asynchrony condition, the assistant and experimenter
each bounced to a differentially randomized version of the 11
inter-downbeat time intervals.

© 2014 John Wiley & Sons Ltd

Synchrony increases infant helping 1005

parent(s). Parents completed three subtests (‘Smiling’,
‘Approach’, and ‘Activity’) of the Infant Behavior
Questionnaire (IBQ) (Rothbart, 1981) in order to
account for pre-existing individual differences in infants’
sociability and willingness to approach novel objects. The
experimenter then left the room while the assistant
exposed the infant to the objects that would later be used
in the helping tasks. The assistant identified each
item (paper ball, clothespin, marker) by name, and
offered the items to the infant. Once the infant touched
each of the three objects, the Interpersonal Movement
Phase began.
The Interpersonal Movement Phase took place in a

sound-attenuating chamber. The parent was asked to
place the infant facing outwards in the child carrier worn
by the assistant. The parent then sat behind this
experimenter for the duration of the Interpersonal
Movement Phase, out of the infant’s line of sight. The
parent listened to masking music via headphones.
The experimenter stood 4.5 feet in front of the

assistant and the infant, directly facing the pair. The
bounce procedure was initiated via a button press by the
experimenter. This simultaneously triggered the onset of
the melodic stimuli heard through speakers by the infant
and the ‘bounce instruction tracks’ heard through
headphones by the assistant and experimenter (see SI
for Apparatus details). The assistant and experimenter
bounced for 145 s according to the bounce instructions
while the infant listened to the melodic stimuli (see video
S1 for an example). The assistant and experimenter wore
Nintendo Wii remotes at their waists, so that their
vertical acceleration over time could be recorded and
compared among the four interpersonal movement
conditions to ensure appropriate and consistent bounce
quality across conditions (see SI for results).

Phase 2: Prosocial Test Phase

Procedure

The infant was placed on a foam mat on the floor of the
sound-attenuating chamber. The assistant left the room,
and the experimenter began the helping tasks. The order
of the three helping tasks was counterbalanced across
conditions and between genders.
The present study included three trials each of three

instrumental helping tasks based on those developed by
Warneken and Tomasello (2007): the paper ball task
(experimenter tries to pick up out-of-reach paper balls
with tongs and place them into a bucket), the marker task
(experimenter draws a picture with markers and ‘acci-
dently’ bumps the markers off the table), and the
clothespin task (experimenter clips dishcloths up on a

clothesline and ‘accidently’ drops the clothespins she is
using).
For all tasks and trials, the experimenter captured the

infant’s attention before dropping the target object.
Each of the three trials began when the experimenter
reached for the target object. For the first 10 s, the
experimenter focused her gaze on the desired object.
For the next 10 s, she alternated her gaze between the
object and the infant. For the final 10 s, she vocalized
repeatedly about the object (‘my paper ball!’, ‘my
marker!’, or ‘my clothespin!’). The trial ended either
when the infant gave the dropped object to the exper-
imenter or after 30 s. Parents were asked to remain
passive and to refrain from communicating with their
infant (see SI for task details; S2 for example videos).

Data coding

To calculate overall rate of helpfulness, these tasks were
videotaped and later coded by two raters blind to the
conditions. During each of the nine trials, video raters
assigned one point if the infant handed the desired object
to the experimenter within the 30-s trial window. If the
infant attempted unsuccessfully to hand back the object,
or handed it back once the 30-s trial window had elapsed,
the infant was assigned 0.5 points. The mean helping rate
across tasks was calculated, and used as each infant’s
overall rate of helpfulness. Inter-rater reliability for video
coding was high, r = 0.98. Raters also recorded elapsed
time before helping occurred, to calculate scores for
spontaneous helping (0–10 s into trial, while experi-
menter focuses only on the object) and two measures of
delayed helping (11–20 s into trial, while experimenter
alternates gaze between object and infant; 21–30 s into
trial, while experimenter names desired object).

Results

We analyzed the correlation between helping rates and
parent-rated IBQ scores on ‘smiling’, ‘approach’, and
‘activity’. When these measures correlated with the
dependent variable in question, they were included as
covariates in an ANCOVA analysis. Otherwise, a stan-
dard ANOVA is reported.

Overall helping

An ANOVA on overall helpfulness rate (Figure 2),
with independent variables synchrony (bouncing in-
synchrony; bouncing out-of-synchrony) and beat pre-
dictability (evenly spaced and predictable; unevenly
spaced and unpredictable), revealed a trend for infants
to be more helpful following interpersonal synchrony

© 2014 John Wiley & Sons Ltd

1006 Laura K. Cirelli et al.

(50.6%, SEM = 6.1%) compared to asynchrony (34.0%,
SEM = 6.6%), F(1,44) = 3.45, p = .07, gp

2 = 0.07. The main
effect of beat predictability, F(1,44) = 2.56, p = .12, and the
interaction between synchrony and beat predictability
were not significant, F(1,44) = 0.11, p = .75.

1

Spontaneous and delayed helping

A similar ANOVA on spontaneous helpfulness (within
0–10 s) revealed that infants were significantly more
likely to demonstrate spontaneous helping following
interpersonal synchrony (25.8%, SEM = 4.3%) compared
to interpersonal asynchrony (13.1%, SEM = 3.9%),
F(1,44) = 4.75, p < .05, gp

2 = 0.10. Neither the main effect
of beat predictability (F(1,44) = 1.31, p = .26) nor the
interaction between synchrony and beat predictability
(F(1,44) = 0.73, p = .40) was significant.

The two measures of delayed helping (10–20 s; 20–30 s
post-trial onset) did not differ statistically and so their
values were combined into one measure for delayed
helping (>11 s into the trial). Delayed helpfulness rates
(>10 s) correlated significantly with the IBQ scale of
‘approach’, r = �0.39, p < .01. Infants who were rated as less likely to shy from novelty were more likely to display delayed helpfulness. An ANCOVA controlling for the variability explained by ‘approach’ scores was conducted on delayed helpfulness. The main effects of interpersonal synchrony (F(1,44) = 0.35, p = .56), beat predictability (F(1,44) = 1.54, p = .22), and their interaction (F(1,44) = 0.17, p = .68) were not significant.

These results suggest that synchrony specifically
encourages spontaneous helping, but not delayed help-
ing. Spontaneous helping occurs quickly and before the
experimenter directs her attention toward the infant,
which may reflect an early form of altruism. Delayed
helping occurs after the experimenter involves the infant
through her gaze direction and vocalizations, and there-
fore may reflect compliance rather than altruism. The
correlational results further suggest that spontaneous

and delayed helping are dissociable, and that only
delayed helping is related to personality traits.

Post-hoc video rating results

To verify that the experimenter acted consistently across
conditions during both phases of the experiment, two
video discrimination tasks were performed (see SI for
details). In the first task, 16 na€ıve adults watched paired
videos of the experimenter’s face and torso during the
Interpersonal Movement Phase. A one-sample t-test
revealed that raters’ ability to distinguish whether the
experimenter was in a synchronous or an asynchro-
nous bouncing condition was not significant, t(15) = 1.11,
p = .28. A paired-samples t-test revealed that raters did
not rate the level of happiness displayed by the exper-
imenter differently in the synchronous versus asynchro-
nous conditions, t(15) = 0.90, p = .38. In addition, the
average happiness ratings for each video did not corre-
late significantly with the helpfulness scores of the
infants from that session, R = 0.10, p = .57.

In the second post-hoc video discrimination task, a
separate group of 16 na€ıve adults watched paired videos

Figure 2 The percentage of objects handed back to the
experimenter as a measure of helpfulness (�SEM of overall
helping) in Experiment 1 (collapsed across even and uneven
beat conditions) and Experiment 2. From this graph, all three
measures of helping (overall, spontaneous and delayed) can be
visualized. In Experiment 1, infants from the synchronous
compared to asynchronous conditions tended to display
greater rates of overall helpfulness, and displayed significantly
greater rates of spontaneous helpfulness (no effect on delayed
helpfulness). In Experiment 2, the rates of overall and
spontaneous helpfulness by the infants in the anti-phase
condition were comparable to infants from the synchronous
condition in Experiment 1: overall and spontaneous
helpfulness rates were greater than those of infants from the
asynchronous Experiment 1 condition.

1 Due to the non-normality of this sample (Shapiro-Wilk = 0.92, p
< .05) we repeated the analysis using trimmed means, a more robust measure of central tendency (Brown & Forsythe, 1974; Field, 2009). Infants with the highest and lowest overall helping score from each of the four groups were removed for this analysis. With this adjusted sample, overall helpfulness correlated significantly with parent-rated IBQ scores of ‘approach’ (infants likelihood to shy from novelty), r = �0.38, p < .05. Using an ANCOVA on the trimmed means, controlling for the effects of ‘approach’, the main effect of synchrony reached significance, F(1,35) = 5.38, p < .05, gp

2 = 0.13. There was still no
significant main effect of beat predictability, F(1,35) = 2.25,
p = .14, and no significant interaction between the two variables,
F(1,35) = 0.20, p = .66.

© 2014 John Wiley & Sons Ltd

Synchrony increases infant helping 1007

showing experimenter behavior during the Prosocial
Test Phase (see SI for details). One-sample t-tests
revealed that raters did not significantly distinguish
the experimenter’s interactions with infants from the
synchronous/evenly spaced beat condition from her
interactions with infants from the asynchronous/
unevenly spaced beat condition. This was true both
when the infant did or did not help the experimenter
(t(15) = 0.52, p = .61; t(15) = 1.07, p = .30). The results of
these two video rating tasks indicate that differences in
infants’ helping behaviors cannot be attributed to
noticeable experimenter bias during either phase of the
experiment.

Experiment

2

In Experiment 1, we defined synchrony as in-phase
interpersonal movement. However, anti-phase interper-
sonal movement is also a stable form of oscillatory
movement, even though such actions alternate rather
than mirror each other (Schmidt, Carello & Turvey,
1990; Haken, Kelso & Bunz, 1985). Specifically, if two
individuals are bouncing in an anti-phase relationship,
when one person is at the lowest part of their bounce the
other is at the highest, and vice versa. Both are still
moving in the same manner and at the same tempo, but
in an opposite phase relationship. If movement contin-
gency drives the prosocial effect of interpersonal motor
synchrony, then anti-phase and in-phase synchronous
movement should both lead to comparable social effects.
If, instead, the social effect of synchronous movement is
driven by movement symmetry, then anti-phase move-
ment should not lead to comparable prosocial effects. In
Experiment 2, we investigated this hypothesis with 14-
month-old infants.

Participants

Twenty walking infants from English-speaking homes
participated (10 girls; M age = 14.4 months; SD = 0.5
months). An additional three infants were excluded due
to excessive fussiness.

Procedure

The procedure was identical to the procedure for the
synchronous/evenly spaced condition of Experiment 1
with the following exception: although the assistant still
bounced the infant so that the low part of her bounce
aligned with the woodblock sounds on the downbeats,
the experimenter instead bounced so that the high part
of her bounce (with legs fully extended) aligned with the

woodblock sounds on the downbeats. This resulted in
alternating bounces; when the assistant and infant were
at the top of their bounce the experimenter was at the
bottom, and vice versa.

Results

There was a trend for a positive correlation between
helpfulness and IBQ-rated ‘smiling’, r = 0.41, p = .07,
and a significant correlation between helpfulness and
‘approach’, such that infants less likely to shy from
novelty were more likely to help, r = �0.50, p < .05.

Overall helping

The helping rates of the infants in the anti-phase
bouncing condition were compared to the helping rates
of infants in the ‘synchronous’ and the ‘asynchronous’
conditions from Experiment 1, using two a priori
planned comparisons. Two GLM ANCOVAs with
‘smiling’ and ‘approach’ as covariates revealed that,
while the overall helping rates of infants in the anti-phase
condition (M = 47.8%, SEM = 6.6%) were not signifi-
cantly different from the helping rates of the infants in
synchronous condition, F(1, 40) = 0.14, p = .71, infants in
the anti-phase condition were significantly more likely to
display helpfulness than infants in the asynchronous
condition, F(1, 40) = 4.50, p < .05, gp

2 = .10 (see Figure 2).
This indicates that, like synchronous bouncing, anti-
phase bouncing leads to a boost in the prosocial behavior
of 14-month-olds.

Spontaneous and delayed helping

We repeated the analyses above for spontaneous help-
fulness (0–10 s) and found that helping rates in the anti-
phase condition did not differ from helping rates in
synchronous condition of Experiment 1, F(1, 40) = 0.01,
p = .96, but did differ significantly from helping rates in
the asynchronous condition, F(1, 40) = 4.78, p < .05, gp

2

= .11. For delayed helping, as expected, there were no
significant differences across conditions (ps > .5). These
results suggest that anti-phase and in-phase synchrony
lead to similar increases in spontaneous helping.

Discussion

The results of Experiment 1 demonstrate that experi-
encing interpersonal synchrony with an unfamiliar adult
promotes spontaneous prosocial behavior in 14-month-
old infants. The size of the synchrony effect on sponta-
neous helping was moderate (gp

2 = 0.10), which is

© 2014 John Wiley & Sons Ltd

1008 Laura K. Cirelli et al.

impressive given that this behavioral measure could be
influenced by many factors aside from our manipulation
(Fritz, 2012), and given the relatively short duration of
the interpersonal movement (145 s). Interestingly, inter-
personal synchrony specifically encouraged spontaneous
helpfulness. Delayed helpfulness was not affected by the
synchrony manipulation, but was related to individual
differences in willingness to approach novelty and
dispositional positivity. The lack of an effect of beat
predictability on helpfulness is not surprising given the
hypothesis relating interpersonal synchrony to prosoci-
ality (Macrae et al., 2008; Valdesolo & DeSteno, 2011).
However, because in past studies beat predictability has
been consistently confounded with interpersonal syn-
chrony or held constant across conditions, it was
important and informative to dissociate these two
variables. Overall, these results support the hypothesis
that interpersonal motor synchrony influences how
prosocial behaviors are directed early in development.

In Experiment 2 we found that a synchronous but
anti-phase bouncing experience led to increases in
prosocial behavior comparable to in-phase bouncing.
Similarly, free-style adult dancers who make synchro-
nous but not identical movements subsequently recall
more information about each other than those dancing
at different tempos (Woolhouse & Tidhar, 2010).
Together, these studies support the hypothesis that it is
the contingency and oscillatory stability underlying in-
and anti-phase interpersonal movement that drives the
effect of interpersonal motor synchrony on prosociality,
and not specifically movement symmetry.

Interpersonal motor synchrony may allow involved
parties to mark each other as similar to one another
(Valdesolo & DeSteno, 2011), which in turn leads to an
increase in affiliative behaviors. In infancy, other cues for
self-similarity such as race and native language have been
shown to contribute to social preference (Kelly et al.,
2007; Kinzler et al., 2007). Interpersonal motor syn-
chrony may work similarly, but has also been hypothe-
sized to enhance person-perception by directing attention
to synchronously moving counterparts (Macrae et al.,
2008). One way to test this hypothesis in future studies
would be to measure how much eye contact the infants
make with synchronously versus asynchronously moving
partners. These results are also consistent with the social
cohesion model of musical behavior, which proposes that
group musical engagement facilitates cooperation among
group members. This heightened cooperation enhances
that group’s ability to survive both directly and indirectly
(Brown, 2000; Freeman, 2000; Roederer, 1984).

The social cohesion model does not specify whether
social facilitation is driven by a cue that is restricted to
musical behavior, or by a cue that is relevant to, but not

restricted to, musical behavior. In the present results,
increased helpfulness, a form of prosocial behavior that
can enhance group cohesion, was observed regardless of
whether interpersonal movements were evenly spaced
(and therefore typically musical and highly predictable)
or unevenly spaced (and therefore not typically musical
and not predictable). Our results are consistent with the
idea that social facilitation driven by interpersonal
synchrony is not restricted to musical contexts. In fact,
it is not clear that music is even necessary as long as
movements are synchronous. This is an important
question for future research. However, the evenly spaced
beats in music provide an especially effective context for
encouraging synchronous movement among people.
Outside of a laboratory setting, it would be difficult for
individuals to coordinate movements occurring at
random intervals. As such, musical behaviors are a
potentially salient source of interpersonally synchronized
movement in everyday life.

Interpersonal synchrony is a common experience in an
infant’s social world. Caregivers often engage in musical
behaviors such as singing, clapping, dancing, and
bouncing with their young children. Our results suggest
that such activities promote socially cohesive behaviors
between infants and caregivers. Moreover, since the
helping behaviors manipulated in this experiment repre-
sent an early form of altruism (Warneken & Tomasello,
2006), the results presented here suggest that 14-month-
old infants are already using social cues to direct their
interpersonal helping, and that interpersonal synchrony
is one such cue.

Acknowledgements

This research was funded by a grant from the Natural
Sciences and Engineering Research Council of Canada
to LJT (197033-2009) and to LKC, and by an Ontario
Graduate Scholarship to LKC. LKC was the primary
researcher and LJT the senior researcher, but all authors
contributed to the ideas, analyses, and writing of the
manuscript. LKC and KME tested the participants. We
thank Leah Latterner for coding videos, Stephanie Wan
for helping with post-hoc video coding data collection,
and Dave Thompson for technical assistance. We thank
Terri Lewis for comments on an earlier draft.

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Supporting Information

Additional Supporting Information may be found in the online
version of this article:
Interpersonal Movement Phase Stimuli.
Prosocial Helping Tasks.
Wii Remote Analyses.
Post-hoc video discrimination tasks.

© 2014 John Wiley & Sons Ltd

Synchrony increases infant helping 1011

International Journal of Behavioral Development
2009, 33 (5), 412–420

http://www.sagepublications.com

© 2009 The International Society for the
Study of Behavioural Development

DOI: 10.1177/0165025409338441

Distal and proximal parentin

g

Parenting is a cultural practice that enables children’s develop-
ment and the acquisition of competence in a particular socio-
cultural environment from birth onwards (Greenfield, Keller,
Fuligni, & Maynard, 2003; Keller, 2003; Keller, Yovsi et al.,
2004; LeVine, 1970; Liu et al., 2005). Two different parenting
styles during the first months of life have been described in the
literature (Keller, 2007): the proximal and the distal style. The
proximal parenting style is characterized by bodily proximity
and body stimulation. The distal parenting style is character-
ized by face-to-face contact and object stimulation, i.e.,
communication through the distant senses. Distal and
proximal styles can be regarded as two alternative parenting
strategies which are related to the sociodemographic profile of
particular contexts.

The proximal parenting style is predominant in traditional
subsistence societies (Keller, Lohaus et al., 2004), in which
socialization goals that embody relatedness, obedience, and
hierarchy are preferred (Kağıtc‚ıbas‚ı, 1996; Keller, Kärtner,
Borke, Yovsi, & Kleis, 2005; Keller, Lamm et al., 2006). It
could be shown that this style reinforces closeness and warmth
(Bandura, 1989; Hetherington & Frankie, 1967). Further-
more, longitudinal studies showed that the early experience of
proximal parenting is related to an early development of com –
pliance (Keller, Kärtner et al., 2005; Keller, Yovsi et al., 2004).

The distal parenting style emphasizes autonomy and sepa-
rateness which have been demonstrated as precursors of
independent agency. It is valued in Western industrial and
postindustrial middle-class families, in which competition,
individual achievements, self-enhancement, and equality
constitute the preferred socialization goals (Keller, 2007;
Keller, Borke, Yovsi, Lohaus, & Jensen, 2005; Keller, Hentschel
et al., 2004; Keller, Kärtner et al., 2005; Keller, Lamm et al.,
2006; Keller, Lohaus et al., 2004). In longitudinal studies we
have demonstrated that the early experience of distal parent-
ing leads to an early development of self-recognition (Keller,
Kärtner et al., 2005; Keller, Yovsi et al., 2004).

The assumption of distal and proximal parenting as alterna-
tive strategies is based on findings demonstrating that high
amounts of body contact are consistently associated with low
amounts of mutual visual engagement and vice versa across
cultures (Keller, Lohaus et al., 2004; Keller, Yovsi et al., 2004;
LeVine, 2004). Further confirmation of this argument is
offered by studies on other primates. Bard and colleagu

es

(2005) demonstrated that in chimpanzees mutual gaze was
inversely related to maternal cradling. When mother and infant
are in constant physical contact, there is little mutual gaze.
These researchers further argue that mutual engagement can
be primarily tactile, which is evolutionarily the most basic
pattern, found in most non-human primates and humans in
rural eco-cultural environments (Bard, 2002; Stack, 2001).
When physical contact is reduced, mutual engagement shifts
to the visual (Lavelli & Fogel, 2002).

In this article, we want to systematically demonstrate that
proximal and distal parenting styles represent different parent-
ing strategies related to different sociodemographic profiles

Distal and proximal parenting as alternative parenting strategies during
infants’ early months of life: A cross-cultural study

Heidi Kellera, Joern Borkea, Thomas Staufenbiela, Relindis D. Yovsia, Monika Abelsa, Zaira Papaligourab,
Henning Jensenc, Arnold Lohausd, Nandita Chaudharye, Wingshan Lof and Yanjie Sug

Cultures differ with respect to parenting strategies already during infancy. Distal parenting, i.e., face-
to-face context and object stimulation, is prevalent in urban educated middle-class families of
Western cultures; proximal parenting, i.e., body contact and body stimulation, is prevalent in rural,
low-educated farmer families. Parents from urban educated families in cultures with a more inter –
dependent history use both strategies. Besides these cultural preferences, little is known about the
relations between these styles as well as the behavioural systems constituting them. In this study there-
fore, the relations between the styles and the constituting behaviours were analysed in samples that
differ with respect to their preferences of distal and proximal parenting. The hypothesized differences
between the samples and the negative relationship between distal and proximal parenting, as well as
between the respective behavioural systems can clearly be demonstrated. Furthermore, the impact
of the sociodemographic variables with respect to the parenting strategies can be shown. Results were
discussed as supporting two alternative parenting strategies that serve different socialization goals.

Keywords: culture; infancy; mother–child interaction; parenting strategies; socialization goals

Correspondence should be sent to Heidi Keller, University of
Osnabrück, Culture & Development, Artilleriestr. 34, Osnabrueck
49076, Germany; e-mail: hkeller@uos.de

The first author was granted funds from the German Research
Council for this study.

aUniversity of Osnabrück, Germany. bAristotle University of Thessaloniki,
Greece. cUniversity of Costa Rica, Costa Rica. dUniversity of Bielefeld, Germany.
eLady Irvin College, India. fAsian Pacific American Legal Center, USA. gUniver-
sity of Peking, China.

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 412

that can be found systematically in very different cultural
surroundings. We hypothesize that distal parenting is shown by
highly educated urban middle-class mothers. These mothers
have their first baby in their late twenties and early thirties and
usually have few children, as higher levels of formal education
correlate with lower numbers of children (Alvarez, Brenes, &
Cabezas, 1990). Formal education emphasizes cognitive func-
tioning as segregated from conative and emotional aspects of
thought (Serpell & Hatano, 1996) and thus analytical inde-
pendence (Greenfield, 1994). Formal education also affects
mother–infant interactions, increasing face-to-face communi-
cation (Richman, Miller, & LeVine, 1992; Tapia Uribe, Levine,
& Levine, 1994). Distal parenting can therefore be regarded as
connected with formal education in urban middle-class families.

Proximal parenting, however, is assumedly regarded as
appropriate by rural mothers who have their first baby in their
late teens or early twenties. Their living environment is char-
acterized by little access to formal education. The family is the
educational unit where learning is mainly observational
(Greenfield, 2004), and can be characterized as “legitimate
peripheral participation” (Lave & Wenger, 1991; Rogoff,
2003). This type of education centres on social intelligence
(Mundy-Castle, 1974) based on a hierarchical apprenticeship
model (Keller, 2003).

Cultural prototypes

The two parenting strategies are assumed to be closely related
to the dimensions of interpersonal distance and the dimension
of agency in Kağıtc‚ıbas‚ı’s model (1996). Interpersonal
distance has the end points of separateness and relatedness and
agency has the end points of heteronomy and autonomy.
Although several combinations are possible Kağıtc‚ıbas‚ı (1996)
describes three prototypical models: independence (separate-
ness and autonomy), interdependence (relatedness and
heteronomy) and psychological interdependence (relatedness
and autonomy). She relates these models to different contex-
tual patterns: the model of independence characterizes Western
urban middle-class families, the model of interdependence
characterizes non-Western rural families and the autonomous-
related (psychological interdependence) model characterizes
urban educated middle-class families from non-Western
societies. For this study data were collected in communities
which can be considered as representing these three cultural
models.

The first group of samples, representing the cultural model
of independence, therefore consists of urban, educated middle-
class families from Western societies. We collected samples of
Euro-American families from Los Angeles, German families
from Marburg, and Greek families from Athens. Euro-
American, German, and Greek middle-class families have been
described as endorsing a distal parenting strategy with a high
amount of eye contact and object play (Keller, Demuth, &
Yovsi, 2008; Keller, Hentschel et al., 2004; Keller, Kärtner et
al., 2005; Keller & Lamm, 2005; Keller, Papaligoura et al.,
2003; Keller, Yovsi et al., 2004; LeVine, 2004).

The second group of samples, representing the cultural
model of interdependence, consists of rural farming families
with little formal education. We recruited samples from the
ethnic tribe of Cameroonian Nso and Indian Gujarati villagers.
Nso and Gujarati villagers have been described as practising
proximal parenting strategies characterized by high amounts of
body contact and body stimulation (Abels et al., 2005; Keller,

2003; Keller, Abels et al., 2005; Keller, Kärtner et al., 2005;
Keller, Lohaus, Völker, Elben, & Ball, 2003; Keller, Voelker, &
Yovsi, 2005; Keller, Yovsi et al., 2004; Keller, Yovsi, & Voelker,
2002; Nsamenang, 1992; Nsamenang & Lamb, 1994).

For our third group of samples, representing the cultural
model of autonomous-relatedness, we collected samples from
San José (Costa Rica), Beijing and Taiyuan (China), Delhi
(India), and urban educated Nso (Cameroon). These families
are expected to value autonomy as well as relatedness due to
their urban educated lifestyle in a society that still holds beliefs
especially for family life that is traditionally oriented towards
relatedness (Kağıtc‚ıbas‚ı, 1996). They should therefore practise
distal as well as proximal parenting styles. Theoretically, they
could be expected to express the same amount of autonomous
related behaviours as the parents with an independent cultural
model and the same amount of relatedness oriented behaviours
as the parents with an interdependent cultural model.
However, previous studies revealed an intermediate position
(Keller, 2007; Keller, Yovsi et al., 2004).

We tested the following hypotheses:

1 We expected the four parenting systems (body contact, body
stimulation, face-to-face context, object stimulation) as well
as the two parenting styles (proximal and distal) to express
systematic variations across the three cultural models. We
expected the contexts representing the independent cultural
model to score highest on face-to-face context and object
stimulation, expressing the distal style of parenting and the
samples representing the interdependent cultural model to
score highest on body contact and body stimulation, repre-
senting the proximal style of parenting. With respect to
samples representing the model of autonomous relatedness,
we expect them to score middle on all systems, expressing
the two styles on a medium level.

2 We assumed that the sociodemographic profile substantially
defines the parenting style. However, culture has a surplus
meaning that accounts for additional variance in the
prediction of parenting styles.

3 Since we assumed that the two styles as well as the consti-
tutive parenting systems are part of alternative parenting
strategies, we expected distal and proximal parenting as well
as their components to be negatively related.

Method

Participants

Participants in the present study were 214 families from nine
different cultural communities; 39 of the families lived in rural
areas and 175 in urban areas; 130 were primiparae, 79 multi-
parae, while for 5 families this information was missing. There
were no significant differences concerning the gender of the
infants (χ2(8) = 5.63, ns). The assessment took place when the
youngest child in the family was about three months old
(plus/minus one week). All children were physically healthy at
the time of assessment (Table 1).

The Western urban middle-class samples

The Euro-American, German, and Greek samples consisted of
urban middle-class families with mostly first-born infants. The
mean mothers’ age was 31.49 (SD = 3.80) and the mean age
of the fathers 34.98 (SD = 4.86) years. Mothers and fathers

INTERNATIONAL JOURNAL OF BEHAVIORAL DEVELOPMENT, 2009, 33 (5), 412–420 413

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 413

414 KELLER ET AL. / DISTAL AND PROXIMAL PARENTING AS ALTERNATIVE STRATEGIES

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412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 414

hold high levels of formal education (14.55 (2.66) years of
formal schooling). They lived as nuclear families in apartments
and houses. Usually, infants had rooms of their own already.
During the early months of infants’ lives, mothers were the
exclusive caretakers who spend most of the time in
“mother–infant isolation”. The Euro-American sample was
recruited in 2002, the German and the Greek samples in 1999.

The rural village samples

The Cameroonian Nso families lived in the North-Western
grassfields of Cameroon, the Indian Gujarati families live in the
Nandesari area. The samples consisted of rural farming
families who lived patrilocally mainly in extended households.
The mean age of the mothers was 24.71 (5.15) and the mean
age of the fathers 31.14 (5.99) years. The level of formal
education was low to minimal (6.19 (2.48) years of formal
schooling). Mothers were infants’ primary caretakers during
the early months of life, however, the mother–infant dyad was
embedded in a close knit network of kin and neighbours.
During the night, infants co-slept with their mothers. The
samples were assessed in the years 2000, 2001, and 2003.

The non-Western urban middle-class samples

The urban Costa Rican, Chinese, Indian, and Cameroonian
samples were characterized by relatively high educational levels
(13.46 (1.74) years of formal schooling; lowest among the
Costa Rican mothers). The mean age of mothers was 28.40
(4.34) and the mean age of the fathers 31.69 (4.55) years.
Families were three generational or nuclear with kin living
close by, so that the mother–infant dyad lived in constant
interactional networks.

The families in the different samples followed different
lifestyles as related to religion with the Costa Rican and the
Nso families being Catholic. The Nso families all belonged to
the ethnic group of the Nso with a traditional sociocultural
system they also follow. The Indian families followed Hinduism
and the Chinese families Confucianism. Assessments were
made in 2001 in Costa Rica, in 2002 in China and in 2003 in
Cameroon and India.

Procedure

The data collection was done by local researchers and research
assistants who were trained in interview techniques, video –
taping, and demographic assessment by supervisors from the
German coordination centre of the study. In all cases, the field
researchers were members of the cultural community under
study.

Information about the character of the study was provided
to all the participants at the first contact. The instruction
informed the family that we were interested in child develop-
ment across cultures. Because of our interest concerning inter-
action behaviour in everyday life and in the families’ natural
surroundings, the families were visited at home. The visits
started with a warm-up and familiarization phase which
consisted of an informal conversation with the families, deter-
mined to some extent by the cultural community. This was
followed by the interview assessing demographic information.
Thereafter, a non-standardized free-play situation with only
the mother and the baby was videotaped. The mothers were
therefore asked to play in the way they usually do without any

further instruction. All communication was done in the
mother’s native language.

Because our intention was to examine a setting in every
culture that allowed the assessment of similarities as well as
differences in parenting, we decided to focus on free-play
situations between mother and infant. Although the studied
cultural communities differ substantially in their definitions of
the adequate care of small babies, free-play situations can be
found in all cultural environments, although to different
degrees depending on the workloads of the mothers. Individ-
ual bouts of play have a duration of 5 to 10 minutes length,
defined by infants’ attention spans during that developmental
phase. Free-play situations required the infant to be awake and
fed but there were no further specifications with respect to
content or duration (Keller, Lohaus et al., 2004; Keller,
Voelker, & Yovsi, 2005; Keller, Yovsi, & Voelker, 2002).

In order to familiarize the families with the videotaping
procedure, we recorded care and other routine situations, prior
to the actual recording of the free-play mother–infant inter –
action. These practice situations were not included in the video
analysis. The length of the free-play episodes was about 10
minutes (M = 9.02, SD = 2.68). The videotapes in the Greek
(M = 7.16, SD = 2.45) and in the rural Cameroonian (M =
7.22, SD = 3.00) sample were significantly shorter than the
videotapes in the Costa Rican sample (M = 10.53, SD = 4.53).
These discrepancies emerged from different amounts of
drop-out crying and/or sleepy/sleeping behaviour (299 sleepy
and 98 crying intervals in the Greek sample, 59 sleepy and
163 crying intervals in the Cameroonian sample, 101 sleepy
and 111 crying intervals in the Costa Rican sample) and
because of differences in the total length of the tapes. If the
babies fell asleep, the videotaping was stopped and not
continued. Because of the ratio scores described below, these
differences were controlled for in the statistical analysis. All
participants received a small gift as an acknowledgement of
their participation.

Measures

The coding of parenting systems

Parenting strategies were assessed with the behavioural systems
conceptualized in the component model of parenting (CMP,
Keller, 2002; Keller, Lohaus et al., 2004), which allowed a
culture-sensitive description through the flexible combination
of the different systems; body contact, body stimulation, face-
to-face context, and object stimulation. These systems reflect
universal parenting systems which occur in any cultural
context. However, the amount of the individual systems as well
as their combinations vary across cultures (Keller, 2007).
Following the description above and based on previous analysis
(Keller, Kuensemueller et al., 2005), these four parenting
systems can be compiled into a distal (face-to-face context and
object stimulation) and a proximal (body contact and body
stimulation) parenting style.

The videotaped free-play interactions were analysed by
members of the German coordination centre of this study
through a computer-based video analysis system (Voelker et
al., 1999). First, the whole registered time of free-play inter –
action was divided into 10-second intervals. In a second
stage, intervals in which the child was not fussy/crying or
sleepy/asleep were identified and each of these intervals

INTERNATIONAL JOURNAL OF BEHAVIORAL DEVELOPMENT, 2009, 33 (5), 412–420 415

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 415

received a separate code for the four parenting systems: body
contact system, face-to-face context, object stimulation, and
body stimulation.

If, during the interactional episodes, the mother or child
could not be clearly seen on the video, these events were coded
as not visible (due to extensive training of the researchers
hardly any non-visible situations occurred, less than .04% of
the episodes). Therefore, measurements, as well as reliabilities,
were based on episodes during which the relevant behaviour
was not obscured in any way.

In the following, the exact coding of the four parenting
systems is presented.

Body contact system. Body contact was coded each time when
one or more of the following body contact positions occurred
for at least 5 seconds of one 10-second interval: both legs of
the child are in contact with the mother, both legs and parts
of the torso of the child are in contact with the mother, the
whole or almost the whole body of the child is in contact with
the mother. Then the percentage of “body contact” intervals
per dyad was calculated.

Body stimulation system. Body stimulation was coded each
time when one or more of the following stimulation behaviours
occurred within one 10-second interval: the whole body of the
child is moved, body parts of the child are moved, the child is
touched repeatedly and all situations during which the infants
body is stimulated with the mother’s face; e.g., kissing. Then
the percentage of body stimulation intervals per dyad was
calculated.

Face-to-face context. The face-to-face system was defined as
effort of the mother to position her body and head to her infant
in a way that allowed face-to-face exchange. Face-to-face
positions were coded with a time sampling method when the
mother created a situation for at least 5 seconds of the 10-
second interval that allowed face-to-face exchange. In any
other case “no face-to-face positions” was coded. In a next
step the percentage of face-to-face intervals per dyad was
calculated.

Object stimulation system. The object stimulation system was
defined as the effort of the mother to attract the attention of
the infant to an object. Some mothers used toys such as
puppets or rings and other mothers used household objects or
things from nature around them such as spoons or wooden
sticks. The kind of object depended on the respective cultural
context and the preferences of the mother. Object stimulation
was coded when an object was included in the interaction
within a 10-second interval. In the next stage the percentage
of object stimulation intervals per dyad was calculated.

Proximal parenting style. For the proximal parenting style, the
average of the categories body contact system and body
stimulation system was calculated.

Distal parenting style. For the distal parenting style, the
average of the categories face-to-face context and the object
stimulation system was calculated.

Inter-rater reliability. The reliabilities were calculated on the
basis of a sub-sample of 10 video sequences that were
randomly collected from the complete set of samples (4.67%).
Cohen’s Kappa was .86 for the body contact system, .90 for
the body stimulation, .85 for the face-to-face context, and .99
for the object stimulation.

Results

The mean percentages of the occurrence of the four parenting
systems – body contact, body stimulation, face-to-face context,
and object stimulation – are shown in Table 2 separately for the
nine cultural samples. Averaging over the parenting systems we
included proximal parenting (body contact and body stimula-
tion) and distal parenting (face-to-face context and object
stimulation) as additional variables.

416 KELLER ET AL. / DISTAL AND PROXIMAL PARENTING AS ALTERNATIVE STRATEGIES

Table 2
Means and standard deviations (in parentheses) for parenting systems by samples

Body Body Face-to-face Object Proximal Distal
contact stimulation context stimulation parenting style parenting style

Sample N M (SD) M (SD) M (SD) M (SD) M (SD) M (SD)

Euro-American sample 20 .43a (.31) .55aa (.22) .57a (.22) .45a (.35) .49a (.21) .51a (.23)
German sample 31 .26a (.29) .45aa (.22) .84a (.18) .41a (.29) .35a (.20) .62a (.15)
Greek sample 29 .20a (.28) .56aa (.24) .77a (.18) .39a (.35) .38a (.22) .58a (.20)
Costa Rican sample 19 .57a (.30) .63aa (.19) .59a (.29) .08a (.13) .60a (.18) .33a (.17)
Chinese sample 20 .32a (.33) .59aa (.17) .60a (.26) .44a (.29) .46a (.19) .52a (.15)
Urban Nso sample 21 .52a (.36) .59aa (.28) .56a (.31) .24a (.37) .56a (.29) .40a (.17)
Urban Indian sample 35 .38a (.33) .60aa (.23) .54a (.24) .29a (.31) .49a (.22) .42a (.19)
Rural Nso sample 23 .83a (.22) .66aa (.22) .63a (.27) .01a (.02) .74a (.12) .32a (.14)
Rural Indian sample 16 .57a (.32) .48aa (.18) .40a (.22) .02a (.06) .52a (.16) .21a (.10)
Independent 80 .28a (.30) .51aa (.23) .75a (.22) .41a (.32) .40a (.22) .58a (.19)
Autonomous-related 95 .44b (.34) .60ba (.22) .57b (.27) .27b (.31) .52b (.22) .42b (.18)
Interdependent 39 .72c (.29) .59ab (.23) .53b (.27) .01c (.04) .65c (.20) .27c (.13)

Note. abcMeans in the same column that do not share superscripts differ at p < .05.

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 416

Differences between the cultural orientations
(hypothesis 1)

To test hypothesis 1 concerning the mean differences in the
four parenting systems between the different cultural models
(independence, autonomous relatedness, interdependence),
we first calculated a MANOVA with the cultural model as
independent variable and the four parenting systems as
dependent variables. The results showed that there were signifi-
cant differences concerning the occurrence of the parenting
systems F(8,416) = 13.44, p < .01 (Wilks λ = .63, partial χ2 = .21). As follow-up analyses four ANOVAs with the cultural models as independent variables and the parenting system as dependent variable were calculated. All parenting systems reached the level of significance (body contact: F(2,211) = 24.94, p < .01, χ2 = .19; body stimulation: F(2,211) = 3.65, p < .05, χ2 = .03; face-to-face context: F(2,211) = 14.17, p < .01, χ2 = .12; object stimulation: F(2,211) = 25.34, p < .01, χ2 = .19).

In a next step, multiple comparisons (Tukey HSD tests) with
the cultural models as independent variables and the parent-
ing system as dependent variable were calculated as post-hoc
tests. As shown in Table 2, all three groups differed significantly
in the predicted direction concerning the amount of body
contact and object stimulation. The amount of body stimula-
tion differed significantly between the independent (less) and
the interdependent samples (more) and the face-to-face
context differed significantly between the independent (more)
and the autonomous-related samples (less).

With parenting styles as the dependent variable, we were also
able to find support for hypothesis 1: the factor cultural model
produced a significant effect in the MANOVA, F(4,420) =
21.17, p < .01 (Wilks λ = .69, partial χ2 = .17) and both ANOVAs: F(2,211) = 18.99, p < .01 (partial χ2 = .15) for the proximal style and F(2,211) = 41.37, p < .01 (partial χ2 = .28) for the distal style as dependent variable. From Table 2 it can be seen that the three group means again differed in the predicted direction, which was statistically confirmed by multiple comparisons (Tukey HSD tests).

To further explore the relationships between the three
cultural models we conducted a discriminant function analysis
in which we predicted the cultural model from the amount of
proximal and distal parenting style. The first discriminant
function allowed for a statistical significant discrimination of
the three groups, χ2(4, N = 214) = 77.31, p < .01 (Wilks λ = 0.69). The second function did not make a significant contri- bution and accounted for less than 0.2% of the between- groups variance. 53.3% of the subjects could be correctly classified into their respective groups. Only nine subjects of the independent group were wrongly assigned to the interdepend- ent group and no misclassification resulted in the opposite direction. Figure 1 plots the discriminant scores of the subjects as points in the plane, spanned by the two discriminant func- tions. As can be seen from the three centroids, the first discrim- inant function accounted for differentiation among the three groups. The groups were ordered as predicted with the autonomous-related cultural model being between the inter - dependent and independent one.

The results thus demonstrated that the autonomous-related
cultural model occupied a middle position concerning their
parenting style.

Influence of the sociodemographic and cultural profile
(hypothesis 2)

To assess the influences of the sociodemographic variables and
the cultural models on the two parenting styles predicted in
hypothesis 2, we performed two separate hierarchical multiple
regression analyses. In a first step, the sociodemographic vari-
ables age, gender, and birth order of children as well as age and
years of formal education of mother were entered, and in the
second step, cultural models. (Because the information about
formal education of fathers was missing in two samples and its
high correlation with the education of mother in the others, r =
.78, p < .01, we omitted this variable from the regression analyses.) The categorical cultural models variable was split into two dummy-coded variables. Table 3 shows a similar pattern for both parenting styles. The three cultural models accounted for a statistical significant additional 8% (proximal) and 9% (distal) of the variance in the parenting styles beyond the variance explained by the sociodemographic variables. The sociodemographic variables alone accounted for 17% (proximal) and 32% (distal) of the variance. The variances of the two predictor groups overlapped considerably, but the cultural models contributed specifically to the prediction of the parenting styles and could not be completely reduced to the included sociodemographic variables.

Relations between distal and proximal parenting and
their components (hypothesis 3)

To test the general relations between the parenting systems
Pearson Product Moment correlations were calculated among
the four parenting systems. Table 4 shows the correlations for
the total sample. There were negative correlations between
body contact and face-to-face exchange as well as object stim-
ulation. There were also negative correlations between object
stimulation and body stimulation. There was a positive corre-
lation between body contact and body stimulation. Finally, also

INTERNATIONAL JOURNAL OF BEHAVIORAL DEVELOPMENT, 2009, 33 (5), 412–420 417

Figure 1. Discriminant function plot with circled centroids of the
three sociocultural orientations.

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 417

in line with hypothesis 3, we found a significant negative corre-
lation between the two parenting styles (r = –.47**, p < .01).

Discussion

This study was aimed at analyzing the structure of the relations
between and the cross-cultural variation of the parenting
systems: body contact, body stimulation, face-to-face context,
and object stimulation, as well as the composite scores: body
contact and body stimulation, representing a proximal parent-
ing style, and face-to-face context and object stimulation,
representing a distal parenting style. In order to test this struc-
ture we analysed samples with different sociodemographic
profiles that are supposed to enact different amounts and
different combinations of these parenting systems. We can
confirm the a priori classification of our samples with one
exception. The Euro-American participants, who were

supposed to prefer the distal style of parenting, demonstrated
the autonomous-related style instead, as they show relatively
high amounts of body contact and body stimulation and a
relatively low amount of face-to-face context. However, this
finding can be regarded as a consequence of the emphasis on
object stimulation. In many instances, mothers and babies
jointly looked at the same object. This pattern of shared atten-
tion in interactional situation is described in the literature
mainly for children during the second half of the first year. It
thus can be concluded that the Euro-American mothers
interacted with their 3 months old babies as if they were in a
different, later, developmental phase. This joint attention
processes also imply that the mothers hold their babies in their
laps, which increases the amount of body contact.

Basically, we can confirm different cultural preferences for
the parenting systems as well as for the combinations into distal
and proximal styles. With the discriminant function analysis we
can demonstrate that there is a good fit between the theoreti-
cally based grouping and the parenting behaviours (Figure 1).
But of course not all mothers were classified correctly. This
may due to the fact that there is also variance within one
cultural context. In particular, independent orientated soci-
eties are also characterized by a variety of individual styles and
habits. Because of this, it is more likely that some families from
independent living in cultural contexts show interdependent
behaviour than the other way round. And of course there is also
variance within the autonomous-related samples (Keller,
2007). Both pathways (the independent and the interdepend-
ent) are present and important in these contexts but it is
possible that some families may focus more on the independ-
ent and some more on the interdependent pathway.

We can show that the sociodemographic profile substantially
defines the parenting styles. Nevertheless, culture has a surplus
meaning that accounts for additional significance in the predic-
tion of parenting styles. It is presumably that this surplus
meaning is due to other culture-defining variables not explic-
itly coded in this study. This could be, e.g., religion, which has
not yet been systematically studied with respect to early parent-
ing from a cross-cultural perspective. Also, e.g., Confucianism
is believed to strongly inform parenting goals and practices
(e.g., Chao, 1994). No systematic comparison has been made
between Chinese Confucian and non-Confucian parents with
similar sociodemographic profiles. Future studies need to
further disentangle the meaning of culture, especially with
respect to the impact of different cultural traditions.

On an individual level, we can confirm our expectation that
the parenting styles as well as the composing systems are
negatively related to each other. Also here it becomes evident
that face-to-face context and body contact are the dominant
systems within the two styles. Our study contributes to the
evidence that body contact and face-to-face contact are two
alternative parenting strategies, as has been suggested by Bard
and colleagues (2005). Body contact can be assumed to be an
evolutionary old parenting system (Hofer, 1987). Moreover the
somesthetic system, comprising kinaesthetic and cutaneous
processes, is the earliest sensory system that develops in the
human embryo (Montagu, 1986). Body contact and touch
convey emotions (Stack, 2001) and thus meanings, especially
in terms of love and care, empathy and the feeling of security.
Body contact transmits interactional warmth directly and can
be related to the development of closeness and acceptance of
norms and values (Keller, 2003; Keller, Yovsi et al., 2004;
MacDonald, 1992). Accordingly affectionate touching and

418 KELLER ET AL. / DISTAL AND PROXIMAL PARENTING AS ALTERNATIVE STRATEGIES

Table 3
Product moment correlations and results of blockwise multiple
regression for dependent variables proximal parenting style (top)
and distal parenting style (bottom)

_

β

Step Variable r Step 1 Step 2 R2 ΔR2

1 Age child –.13 –.01 .02
Birthorder child .33** .30** .25*
Gender child .02 .03 .00
Age mother –.20** –.18* –.08
Education mother –.31** –.12 .12 .17**

2 Culture 1 –.39** –.24**
Culture 2 .39** .25* .25** .08**

β
Step Variable r Step 1 Step 2 R2 ΔR2

1 Age child .14 –.02 –.04
Birth order child –.43** –.31** –.26**
Gender child .04 .03 .05
Age mother .23** .11 .00
Education mother .50** .33** .11 .32**

2 Culture 1 .52** .31**
Culture 2 –.50** –.19† .42** .09**

Notes. Birth order is coded 1 = first child and 2 = other; Gender is
coded 1 = male, 2 = female; Culture 1 is coded 1 = independent and
0 = other; Culture 2 is coded 1 = interdependent and 0 = other.

N = 167; **p < .01; *p < .01; †p < .10.

Table 4
Correlations of parenting systems

Body Object Face-to-face
stimulation stimulation context

Body contact .28** –.46** –.22**
Body stimulation — –.39** .13**
Object stimulation — .02**
Face-to-face context —

Note. N = 214; **p < .01.

412-420 JBD338441 Keller:210 x 280mm 30/07/2009 10:58 Page 418

closeness are observed predominantly as parts of parenting
strategies that are oriented towards an interdependent cultural
model (Franco, Fogel, Messinger, & Frazier, 1996; Keller,
Voelker, & Yovsi, 2005; Konner, 1976).

Face-to-face contact, on the other hand, can be regarded as
a rather new parenting system (Keller, 2003). Also with respect
to ontogenetic development, the visual system is the last to
develop in the human embryo (Gottlieb, 1976). The distal
contact through face-to-face communication can be regarded
as an alternative to parenting mainly through body contact
during the early months of life. Accordingly it has been repeat-
edly demonstrated that physical proximity is an important
factor in influencing the infant’s engagement during face-
to-face play with more distant positions favouring more eye
contact (e.g., Lavelli & Fogel, 1998; Stack, Arnold, Girouard,
& Welbourne, 1999). However, it is physically not impossible
to have body contact and a face-to-face context at the same
time.

Our results gain strength from the fact that we analysed
parenting strategies from participants with very different
cultural models that favour different systems to different
degrees. Therefore the negative correlation between the
systems as well as the composite scores can be interpreted in
terms of basic strategies. Our data confirm that the four parent-
ing systems meaningfully describe the interactional experi-
ences of small babies and express the cultural emphasis of
particular combinations or styles. They also offer a fair method
of conceptualizing parenting in culture, since the parenting
system constitutes universals, that are differently embodied
across cultures. It is also evident that no one strategy is better
than another.

Our study also has constraints. The analyses are based on
free-play interactional situations. Although we have demon-
strated in different studies that free-play situations occur across
diverse cultural contexts, their prominence, however, also
differs (Keller, 2007). Further studies should include the
analysis of everyday routine situations as well as care situations
in order to gain a fuller understanding of children’s everyday
experiences. Also the analysis of infants’ contribution to the
interactional flow would be important for understanding the
expression of cultural models in everyday interactional
situations.

Generally, proximal and distal parenting can be regarded as
parts of two alternative modes of self-development (Greenfield
et al., 2003; Keller & Greenfield, 2000; Keller, Kärtner et al.,
2005; Keller, Yovsi et al., 2004). So far, research on the origin
of self-development has mainly been based on the analysis of
face-to-face interactions (Kaye & Fogel, 1980; Keller, Yovsi et
al., 2004; Rochat, 2001) with the implicit and explicit assump-
tion that infants from birth on are perceived as independent
agents with mental states, desires, and preferences. The results
of our study underscore the importance of considering alter-
native modes of self development. We propose a proximal
pathway with an understanding of the self as a primarily rela-
tional co-agent. Future studies should help to explain different
developmental pathways with different developmental goals
leading to different conceptions of the self.

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Research Article

The human experience of emotion seems personal and
internally generated, but people’s feelings can originate
from the affective states of others around them. Whether
it is the enthusiasm of a team member that ignites excite-
ment or the acute anxiety of a partner that generates a
sense of unease, people are highly sensitive to the emo-
tional tenor of their social partners and may uncon-
sciously achieve affective convergence with them. Affect
is a neurophysiological state that may vary in valence
(positive or negative) as well as arousal (low or high;
Barrett, 2006). Affect contagion, then, is the transmission
of affect from one person to another and has been sug-
gested to function, in part, to facilitate social connection
and coordination (Butler, 2011; Hatfield, Cacioppo, &
Rapson, 1994). Consistent with the notion of affect conta-
gion are findings that the regions of the mirror-neuron
system that are activated when individuals observe action
are similar to the regions that are activated when indi-
viduals perform the same action (Iacoboni et al., 1999).
In addition, synchrony has been observed in converging

voice frequency of dyad members (Gregory & Webster,
1996) and in behavioral mimicry of face and posture
(Chartrand & Bargh, 1999; Neumann & Strack, 2000).

Relying on imaging of neural regions or the occur-
rence of discrete behaviors can pose practical and infer-
ential challenges to measuring affect contagion in the
context of dynamic, face-to-face dyadic interactions. In
contrast, on-line peripheral physiological responses offer
a response channel that reacts quickly to affective
changes and allows for temporal precision to examine
subtle changes over time in dyad members. Indeed, some
of the first psychophysiological studies examining dyadic
social interactions found affect contagion in the form
of synchronization between autonomic responses of
interaction partners (Kaplan, Burch, & Bloom, 1964).
More recently, affective scientists have demonstrated that

518352PSSXXX10.1177/0956797613518352Waters et al.Stress Contagion
research-article2014

Corresponding Author:
Wendy Berry Mendes, 401 Parnassus Ave., San Francisco, CA 94118
E-mail: wendy.mendes@ucsf.edu

Stress Contagion: Physiological Covariation
Between Mothers and Infants

Sara F. Waters1, Tessa V. West2, and Wendy Berry Mendes

1

1Department of Psychiatry, University of California, San Francisco, and 2Department of Psychology,
New York University

Abstract
Emotions are not simply concepts that live privately in the mind, but rather affective states that emanate from the
individual and may influence others. We explored affect contagion in the context of one of the closest dyadic units,
mother and infant. We initially separated mothers and infants; randomly assigned the mothers to experience a stressful
positive-evaluation task, a stressful negative-evaluation task, or a nonstressful control task; and then reunited the
mothers and infants. Three notable findings were obtained: First, infants’ physiological reactivity mirrored mothers’
reactivity engendered by the stress manipulation. Second, infants whose mothers experienced social evaluation
showed more avoidance toward strangers compared with infants whose mothers were in the control condition. Third,
the negative-evaluation condition, compared with the other conditions, generated greater physiological covariation
in the dyads, and this covariation increased over time. These findings suggest that mothers’ stressful experiences are
contagious to their infants and that members of close pairs, like mothers and infants, can reciprocally influence each
other’s dynamic physiological reactivity.

Keywords
electrophysiology, emotional development, infant development, social behavior, stress reactions

Received 9/12/13; Revision accepted 12/1/1

3

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Stress Contagion 93

5

observing or interacting with a stranger experiencing
acute stress can engender physiological changes in the
observer (Buchanan, Bagley, Stansfield, & Preston, 2012;
Butler et al., 2003; Soto & Levenson, 2008), and this abil-
ity to “catch” another person’s affect may be related to
social sensitivity and emotional accuracy (Guastello,
Pincus, & Gunderson, 2006; Hess & Blairy, 2001; Levenson
& Ruef, 1992).

Dyadic physiological synchrony is associated with
romantic couples’ affective experiences. When romantic
partners were instructed to sit face-to-face and “get in
sync,” the degree to which women’s physiology synchro-
nized with their partners’ was associated with their
responsiveness to their partners’ daily affect (Ferrer &
Helm, 2013). In a seminal study, physiological linkage in
married couples during a conflict conversation was a sig-
nificant predictor of self-reported marital dissatisfaction
in both partners (Levenson & Gottman, 1983). Further, it
has been suggested that couples form a coregulatory unit
in which each member provides the feelings of security
and support that help the other effectively regulate emo-
tional and neurophysiological arousal during stressful or
painful times (Sbarra & Hazan, 2008).

The significance of the romantic pair bond is rivaled
only by the significance of the bond between mother and
child. The connection that forms between mother and
child is an evolutionary adaptation that helps ensure the
infant’s nurturance by facilitating the mother’s emotional
investment in her child (Bowlby, 1982). In humans,
mother-driven behavioral affective attunement fosters chil-
dren’s developing cognitive and social-emotional skills
(Harrist & Waugh, 2002). Several recent studies have found
evidence for mother-child cortisol synchrony, especially in
the context of negative affect or high anxiety (Hibel,
Granger, Blair, & Cox, 2009; Papp, Pendry, & Adam, 2009;
Williams et al., 2013). These studies measured naturally
occurring variation in physiological synchrony. In the pres-
ent research, we used an experimental design to induce
different affective states in mothers and then examined
whether infants caught that affective state. We also exam-
ined the extent to which mothers’ and infants’ physiologi-
cal changes synchronized by measuring the covariation of
physiological responses within dyads.

Although behavioral mimicry may be a primary source
of affect contagion, within the mother-infant dyad, lower-
level actions such as referencing and monitoring are pre-
requisites for affect contagion. Social referencing refers to
how infants nearing the end of their 1st year modify their
behavior in accordance with their mothers’ emotional cues
(Walden & Ogan, 1988). When mothers exhibit negative
emotion, for instance, infants interact with their environ-
ments with greater wariness, even if their attention is not
deliberately drawn to their mothers’ emotion (de Rosnay,

Cooper, Tsigaras, & Murray, 2006). We exposed mothers to
negative or positive evaluation during a stressful task in
order to examine the contagion of high-arousal negative
affect in comparison with high-arousal positive affect.
Given that negative affect is typically more salient and
impactful than positive affect for both adults (Baumeister,
Bratislavsky, Finkenauer, & Vohs, 2001) and infants (Sorce,
Emde, Campos, & Klinnert, 1985), we expected to find that
infants catch mothers’ negative affect to a greater extent
than mothers’ positive affect.

Many of the studies examining physiological syn-
chrony have focused on physiological linkage, in which
one individual’s physiological responses influence
another person’s physiological responses in a time-lag
design, but a second type of physiological synchrony
may be more relevant to the current context. Physiological
covariation describes the amount of correlation between
two individuals’ physiology within a single time period.
Conceptually, covariation is believed to result from shared
experiences or environments, and positive covariation
(i.e., the slopes of responses show the same direction of
change) results from the extent to which the individuals’
affective experiences are similar. Given the primacy of
affective cues within the mother-infant dyad, we focused
on physiological covariation as our model for affect
contagion.

We expected mothers’ affective reactivity to vary with
condition such that mothers who experienced negative
evaluation would have greater physiological reactivity
(i.e., sympathetic activation) and more externalizing neg-
ative affect than mothers who experienced positive eval-
uation, whose physiological reactivity would be greater
than that of mothers who experienced the low-stress
control condition. We expected that infants, who had
been separated from their mothers during the manipula-
tion, would catch their mothers’ affective state upon
reunion and manifest a pattern of physiological reactivity
similar to that induced in the mothers, as well as behav-
ioral responses consistent with environmental wariness if
their mothers had been in one of the social evaluation
conditions. We also anticipated that affect contagion
would be manifested as greater dyadic physiological syn-
chrony in the form of physiological covariation over time.
Finally, we expected this covariation over time to be
strongest for dyads in which mothers had received nega-
tive evaluation.

Method

Participants

Sixty-nine mothers (mean age = 33.6 years, SD = 5.6) and
their 12- to 14-month-olds (45% female, 55% male) were

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936 Waters et al.

recruited from the San Francisco Bay Area and were
compensated $75. Mothers were excluded if they were
hypertensive, had a pacemaker, took cardiac medica-
tions, or were pregnant. (For additional information
about the participants, see the

Supplemental Material

available online.

)

Procedure

Figure 1 presents an overview of the procedure (addi-
tional details are available in the Supplemental Material).
Upon arrival, each mother provided consent for herself
and her infant. The infant was taken to a playroom, with
a caregiver who came to the experiment with the mother
and baby, while the mother moved to a different room.
Here, the experimenter attached sensors to measure car-
diovascular responses and instructed the mother to relax
alone for a 5-min period, during which her baseline car-
diovascular responses were obtained. Then, the infant
was brought to the mother, and the experimenter attached
sensors to measure the infant’s cardiovascular responses.
The experimenter instructed the mother to help her
infant relax for a 2-min period, during which the infant’s
baseline cardiovascular responses were obtained.
Afterward, the infant returned to the playroom while the
mother remained in the room.

The mother completed a questionnaire on her current
affect, and then the experimenter introduced the upcom-
ing interview task (modified Trier Social Stress Test;
Kirschbaum & Hellhammer, 1994) and obtained verbal
consent to continue. The mother was instructed to give a
5-min speech about her strengths and weaknesses to
a panel of two evaluators. This speech was followed by a
5-min question and answer (Q&A) session.

Mothers were randomly assigned to one of three con-
ditions: social evaluation with positive feedback, social
evaluation with negative feedback, or no evaluation
(control). Social evaluation was provided by two trained
evaluators (one male, one female), who exhibited non-
verbal feedback during the speech and Q&A session. In
the positive-evaluation condition, the evaluators became
progressively more positive by smiling, nodding, and

leaning forward while the participant spoke, whereas in
the negative-evaluation condition, the evaluators became
progressively more negative, frowning, shaking their
heads, crossing their arms, and leaning back. This manip-
ulation of social approval versus social rejection has been
used successfully to induce high-arousal positive and
negative affective states, respectively (Akinola & Mendes,
2008). In the control condition, mothers were instructed
to deliver the speech and verbally answer questions writ-
ten on cards while alone in the room. Thus, the control
condition was similar to the experimental conditions in
terms of the physical metabolic demands (i.e., speaking
aloud, thinking about the same questions) but did not
have the social evaluation component. Immediately fol-
lowing the Q&A session, the mother completed another
affect questionnaire.

Next, the infant rejoined the mother for a 2-min
reunion period followed by a 2-min resting period in
which the mother was instructed to help her infant relax.
Mother and infant then experienced two poststress inter-
views with different female interviewers; these interviews
were videotaped for later behavioral coding. In each of
these interviews, the interviewer entered the room, sat
across from the mother-infant dyad, engaged the mother
in a short innocuous conversation about her infant’s
development, and then offered the infant a toy for 1 min.
In the final phase of the experiment, the two female
interviewers entered the room, sat across from the dyad,
and offered the infant identical sets of toys (toy offer) for
3 min. Upon completion of the study, the sensors were
detached, the mother was debriefed, and payment was
given.

Measures

Affect measures.  We used the Positive and Negative
Affect Schedule (PANAS; Watson, Clark, & Tellegen,
1988) to assess mothers’ affect. Mothers rated the degree
to which they were currently experiencing 20 different
affect states, using a 5-point scale from 1 (not at all) to 5
(a great deal). We calculated positive- and negative-affect
scores for each time point (i.e., before and after the

Mother
Baseline

5 min

Infant
Baseline

2 min

Speech
5 min

Q&A
5 min

Reunion
2 min

Rest
2 min

Poststress
Interview 1

2 min

Poststress
Interview 2

2 min

Toy
Offer
3 min

Time

Fig. 1.  Overview of the procedure. Dashed outlines indicate that the mother was alone; for all other periods, the mother
and infant were together. Bold outlines indicate the periods from which the mother’s and infant’s physiological data were
taken for covariation analyses. Q&A = question-and-answer session.

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Stress Contagion 93

7

speech task; αs ranged from .85 to .93). Because high-
arousal, externalizing negative affect was the expected
affective state following negative social evaluation, we
further differentiated an externalizing subscale consisting
of three of the negative-affect items: “hostile,” “irritable,”
and “upset” (αposttask = .83).

As a manipulation check, following the evaluation, we
asked mothers assigned to the positive- and negative-
evaluation conditions to rate seven statements about their
perceptions of the evaluators’ feedback (e.g., “She
thought I performed well on the task”). The 7-point rat-
ing scale ranged from 1 (strongly disagree) to 7 (strongly
agree; Akinola & Mendes, 2008). Perceptions of the male
and female evaluators were highly correlated, so the
scores were averaged to form a single scale (α = .94).

Autonomic nervous system measures.  We measured
electrocardiography (Biopac MP150 Data Acquisition
System, Biopac Systems, Inc., www.biopac.com) and
impedance cardiography (HIC-2000 Impedance Cardio-
graph, Bio-Impedance Technology, Inc., http://www
.microtronics-nc.com/BIT/Home.html) to obtain moth-
ers’ sympathetic nervous system (SNS) reactivity, specifi-
cally, preejection period (PEP; the time from contraction
of the left ventricle to opening of the aortic valve). PEP is
a chronotropic measure, such that greater activation is
indicated by a greater decrease in PEP. For ease of inter-
pretation, we multiplied PEP by −1, so that increases in
SNS are represented as increases in force of ventricle
contractility (VC).

Pilot testing of impedance cardiography collection on
infants revealed that application of the adhesive bands
was not well tolerated and was quite stressful for them.
Unfortunately, it was not feasible to obtain PEP data from
the infants. Instead, electrocardiography was collected
from two spot sensors on the chest, and we calculated
heart rate (HR, in beats per minute) as the measure of
infants’ SNS activation.1

The mothers’ physiological measures were collected
continuously from the baseline through the toy offer; for
infants, physiological responses were obtained at base-
line with the mother and then continuously from the 2nd
minute of reunion through the toy offer. Thus, we had 10
min of dyadic physiological data following the manipula-
tion. We scored mothers’ PEP and infants’ HR data by first
visually inspecting the waveforms for artifacts and then
aggregating the data in 30-s segments using Mindware
software (Impedance Cardiography Analysis Software 2.6
and Heart Rate Variability Analysis Software 2.6, Mindware
Technologies, Ltd., http://www.mindwaretech.com/). As
is standard practice, reactivity scores were calculated by
subtracting baseline responses (the last 30 s of baseline)
from every 30-s segment after the baseline.

Measure of infant behavior.  Infants’ behavioral
avoidance during the 1st minute of each poststress inter-
view was coded on a 5-point scale from 0 (infant did not
hesitate to engage with interviewer) to 4 (infant continu-
ously actively avoided interviewer). Behavioral indicators
ranged from passive (e.g., gaze aversion) to active (e.g.,
twisting bodily away) avoidance of the interviewers (Mur-
ray et al., 2008). After achieving reliability with the master
coder on 20% of the sample (weighted κ = .78), a female
research assistant, naive to mothers’ condition assign-
ment, coded all videotapes. Ten percent of the tapes
were uncodable because of equipment malfunction or an
inadequate camera angle.

Data analysis

The primary outcome variables were changes in SNS acti-
vation (mothers’ VC reactivity and infants’ HR reactivity),
mothers’ affective self-reports, and infants’ behavioral
avoidance. We first explored physiological reactivity sep-
arately for the mothers and babies. To examine effects of
evaluation condition, we focused on the time interval of
greatest activation, selected a priori on the basis of prior
research (e.g., Mendes, Blascovich, Hunter, Lickel, & Jost,
2007). For mothers, this was the 1st minute of the Q&A
session (when the task was novel, but feedback had been
established), and for infants, this was the 1st minute of
each poststress interview (when the situation was novel
and before the interviewer attempted to engage directly
with the infant). In analyses of mothers’ SNS activation,
we controlled for body mass index ( Jennings et al., 1981).

We then examined whether physiological covariation
varied as a function of evaluation condition and whether
it strengthened or weakened over the course of the inter-
action between mother and infant. To measure covaria-
tion, we estimated the relationship between mothers’ VC
reactivity and infants’ HR reactivity, using a nomothetic
approach in which mothers’ VC reactivity was treated as
the criterion variable and infants’ HR reactivity as the pre-
dictor; covariation was estimated as a path coefficient.
(We note that this analysis does not imply causation, but
rather, captures the relationship between variables mea-
sured simultaneously; for a similar strategy to estimate
dyadic similarity, see West & Kenny, 2011).2 We modeled
a linear growth curve in which time was centered at the
study midpoint (see the Supplemental Material for ran-
dom effects of intercept and slope, as well as intercept-
slope covariance). This model allowed us to estimate the
overall strength of covariation (i.e., the effect of infants’
HR reactivity on mothers’ VC reactivity), the effect of con-
dition on covariation (i.e., the interactive effect of infants’
HR reactivity and condition on mothers’ VC reactivity),
whether covariation strengthened over time (i.e., the

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938 Waters et al.

interactive effect of infants’ HR reactivity and time on
mothers’ VC reactivity), and whether it did so differently
as a function of condition (i.e., the interactive effect of
infants’ HR reactivity, time, and condition on mothers’ VC
reactivity). (Note that the main effect of time was also
included in the model.)

Data were analyzed using the MIXED procedure in
SPSS to account for nonindependence across the 20 time
segments of data when mother and baby were together.
We note that this procedure uses the Satterthwaite (1946)
method to calculate degrees of freedom, which can be
fractional; it also allows for missing data.

Results3

We first examined whether mothers experienced the eval-
uation conditions as intended by analyzing mothers’ per-
ceptions of the evaluators’ feedback, as well as their
self-reported positive and negative affect. Mothers who
received negative evaluation perceived the evaluators as
less supportive (M = 3.31, SD = 0.98) than did those who
received positive evaluation (M = 5.10, SD = 1.05), t(40) =
5.68, p < .001. In addition, mothers experienced greater decreases in positive affect and greater increases in nega- tive affect in the negative-evaluation condition, compared with the positive-evaluation and control conditions (see the Supplemental Material). When we examined external- izing negative affect specifically, we found that it differed significantly by condition, F(2, 64) = 7.32, p = .001.

Externalizing negative affect increased significantly after
negative evaluation (M = 0.54, SD = 0.98), compared with
positive evaluation (M = −0.23, SD = 0.71) and the control
task (M = −0.09, SD = 0.23), t(64) = −3.56, p = .001, and
t(64) = −2.96, p = .004. The control and positive-evaluation
conditions were not significantly different from each other,
p = .51. In sum, negative evaluation engendered primarily
externalizing (i.e., anger) responses.

Maternal physiological reactivity

Analysis of covariance revealed a significant main effect
of condition on mothers’ VC reactivity, F(2, 62) = 9.53,
p < .001 (Fig. 2a). As expected, the positive-evaluation condition (ΔVC = 6.0, SD = 6.49) and negative-evaluation condition (ΔVC = 10.75, SD = 8.81) engendered signifi- cant increases in sympathetic activation relative to the control condition (ΔVC = 0.74, SD = 8.29), t(62) = 2.29, p = .03, and t(62) = 4.21, p < .001, respectively. Negative evaluation was associated with greater SNS activation than was positive evaluation, t(62) = 1.80, p = .08. (See the Supplemental Material for information on the covari- ate body mass index.)

We then examined the correlation between SNS
responses and externalizing negative affect, finding
that the magnitude of this relationship varied across
conditions—negative evaluation: r(22) = .41, p = .058;
positive evaluation: r(20) = .33, p = .16; control: r(23) =
.04, p = .85. These data suggest that we successfully

–

8

–

6

–4

–2

0

2
4
6
8

In
f

a

nt
s’

H
ea

rt
R

at
e

R
ea

ct
iv

ity
(

b

ea
ts

/m
in

)

Mothers’ Evaluation Condition

Positive-
Evaluation
Condition

Negative-
Evaluation
Condition

Control
Condition

b

–1

1
3
5
7

9

11

13

M
ot

he
rs

’ V
en

tr
ic

le
C

on
tr

ac
til

ity
R

ea
ct

iv
ity

(m
s)

Mothers’ Evaluation Condition
Positive-
Evaluation
Condition
Negative-
Evaluation
Condition
Control
Condition
a

Fig. 2.  Mothers’ and infants’ physiological reactivity during the poststress interviews: (a) mothers’ mean increase in ventricle contractility
and (b) infants’ mean heart rate reactivity as a function of mothers’ evaluation condition. Error bars represent ±1 SE.

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Stress Contagion 939

engendered greater SNS reactivity in the two evaluation
conditions, which nonetheless showed differentiation in
both affective quality and the magnitude of physiological
responses.

Infants’ physiological reactivity

We examined infants’ HR reactivity during the poststress
interviews as a function of mothers’ evaluation condition.
Infants’ HR reactivity during the two poststress interviews
was significantly correlated, r(54) = .68, p < .001, so responses were averaged. Analysis of variance revealed a significant main effect of condition, F(2, 58) = 5.35, p = .007 (Fig. 2b). Infants whose mothers received negative evaluation exhibited significantly higher HR reactivity during the interviews (ΔHR = 5.76, SD = 6.35) than did infants whose mothers were in the control condition (ΔHR = −3.95, SD = 10.72), t(58) = −3.24, p = .002. The HR reactivity of infants of mothers assigned to the posi- tive-evaluation condition (ΔHR = 1.95, SD = 10.94) fell in between the HR reactivity of infants of mothers in the negative-evaluation condition, t(58) = −1.26, p = .21, and control condition, t(58) = −1.97, p = .05. (Analyses exam- ining the influences of infants’ sex and alternate caregiv- ers’ identity on infants’ outcomes are in the Supplemental Material.)

Infants’ behavioral avoidance

As was the case for infants’ HR reactivity, behavioral-
avoidance scores from the two poststress interviews were
significantly correlated, r(58) = .53, p < .001, and thus averaged. A significant main effect of condition was observed, F(2, 54) = 6.89, p = .002. Mothers who had experienced social evaluation had infants who were more avoidant toward the interviewers (positive-evalua- tion condition: M = 1.55, SD = 1.28; negative-evaluation condition: M = 1.76, SD = 1.1) compared with mothers assigned to the control condition (M = 0.67, SD = 1.0), t(60) = −3.36, p = .001, and t(60) = −4.15, p < .001, respec- tively (Fig. 3). Behavioral avoidance differed descriptively but not significantly between infants of mothers in the positive-evaluation condition and infants of mothers in the negative-evaluation condition (p = .47). (Recall that a small percentage of behavioral-avoidance data were missing. Analyses of maternal and infants’ physiological reactivity in the subsample with intact behavioral data are in the Supplemental Material.)

Mother-infant physiological
covariation over time

Finally, we tested covariation from the reunion through
the toy offer. Recall that covariation was estimated as a

path coefficient. The overall relationship between infants’
HR reactivity and mothers’ VC reactivity was positive and
significantly different from zero, F(1, 908.64) = 17.21, p =
.003, which indicated that, overall, there was covariation.4
The interaction between infants’ HR reactivity and evalu-
ation condition was not significant, p = .54; however, the
interaction of infants’ HR reactivity, evaluation condition,
and time was significant, F(2, 282.00) = 3.78, p = .02;
change in covariation over time varied as a function of
evaluation condition (Fig. 4). Specifically, in the negative-
evaluation condition, the interaction between infants’
HR reactivity and time was positive and significant,
t(368.43) = 2.56, p = .01; the greater the mothers’ SNS
activation, the greater their infants’ HR responses, and
this effect strengthened over the course of the study. We
note that at the end of the study, covariation was positive
and significant in the negative-evaluation condition,
t(436.41) = 3.49, p = .001. In the positive-evaluation and
control conditions, the interaction between infants’ HR
reactivity and time was not significant (ps = .92 and .21,
respectively); covariation did not change significantly
over time in these conditions. We also note that overall
covariation was not significantly different from zero in
the control condition, p = .12, but was different from zero
in the positive-evaluation condition, p = .01.

We created two contrast codes to compare the over-
time change in covariation in the negative-evaluation
condition with the over-time change in covariation in the
control condition (Contrast 1) and in the positive-evalua-
tion condition (Contrast 2). The Contrast 1 × Infants’ HR

0.0

0.5

1.0

1.5

2.0

2.5

In
fa

nt
s’

B
eh

av
io

ra
l A

vo
id

an
ce

Mothers’ Evaluation Condition
Positive-
Evaluation
Condition
Negative-
Evaluation
Condition
Control
Condition

Fig. 3.  Infants’ mean behavioral avoidance of the interviewers as a
function of mothers’ evaluation condition. Error bars represent ±1 SE.

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940 Waters et al.

Reactivity × Time interaction was significant, t(278.63) =
−2.76, p = .01, which indicated that the slope for the
negative-evaluation condition differed significantly from
the slope for the control condition. The Contrast 2 ×
Infants’ HR Reactivity × Time interaction was marginally
significant, t(317.37) = −1.65, p = .10, which indicated
that the slope for the negative-evaluation condition
differed marginally from the slope for the positive-
evaluation condition. The slopes for the positive-evalua-
tion and control conditions were not significantly differ-
ent from each other, p = .35.

Discussion

Employing an experimental design to induce positive or
negative social evaluative stress in mothers while they
were separated from their infants, we found that a moth-
er’s stress is embodied by her infant upon reunion.
Moreover, the mother-infant dyads showed greater physi-
ological covariation after mothers experienced a negative
stressor than after they experienced a positive stressor or
low-stress task, and this covariation increased over time.
We feel confident that infants’ responses were not driven
by a combination of their mothers’ reactivity coupled
with environmental triggers because the infants were
never exposed directly to the mothers’ stressors. To our
knowledge, this is the only study in which autonomic
nervous system reactivity has been measured simultane-
ously in mothers and infants following different stress

manipulations and in which the resulting physiological
attunement has been analyzed.

Mother-infant attunement is likely highly adaptive and
presumably evolved for a variety of reasons, such as
detecting and communicating danger from imminent
threats from conspecifics and other nonhuman animals,
and other environmental hazards. In animals, relational
processes between mothers and infants have long-lasting
modulatory effects on social and health outcomes.
Foundational studies of rat pups and their mothers dem-
onstrated that pups who receive higher levels of licking
and grooming behavior from their mothers have lower
responses to subsequent stressors (Meaney, 2001), and
that olfactory and auditory stimuli emitted from rat and
mouse pups allow for maternal monitoring of location
(Nagasawa, Okabe, Mogi, & Kikusio, 2012). Thus, mother-
infant attunement is likely to serve both adaptational and
survival purposes. In humans, its function is not fully
understood. In the current study, we initially induced
stress in only one member of each dyad, which allowed
us to test whether such attunement serves to communi-
cate affective information from one member to the other.
We found that maternal stress transmission had the great-
est impact on infants’ physiology when mothers had
experienced a negative-evaluative stressor. This suggests
that infants may be predisposed to attend to their moth-
ers’ heightened-arousal states, such as reactions to nega-
tive, threatening, or angering events.

Our study has several limitations and suggests several
interesting avenues of further inquiry. We suspect that there
are a variety of channels through which affect is communi-
cated between mother and infant. Stressed mothers may
exhibit changes in facial expression, odor, posture, vocal
tone, prosody, and touch, all of which may contribute to
the effects we observed. Although a mother’s soothing
physical touch helps a distressed infant better regulate him-
or herself (Feldman, Singer, & Zagoory, 2010; Field, 1998),
the touch of an acutely stressed mother has not been well
examined. Infants in our study sat on their mothers’ lap
during the poststress exchanges, and it is possible that the
mothers’ touch was a proximal cause for changes in physi-
ological reactivity. Given the amount of time many young
infants spend in physical contact with their parents, under-
standing of early biobehavioral synchrony would be
strengthened by isolating the impact of physical touch
following a paradigm like the one we used here.

We designed the study so that we could compare
responses to a negative stressor with responses to a milder,
positive stressor. However, it is fair to note that the nega-
tive-evaluation condition was associated with larger mater-
nal SNS activation than the positive-evaluation condition,
so we are unable to completely rule out intensity of reac-
tivity (rather than negative affect) as the causal factor influ-
encing physiological covariation.

–

0.10

–

0.05

0.00

0.05
0.10

0.15

0.20

0.25

0.30

0.35

0.40

2 4 6 8 10 12 14 16 18 20

Positive-Evaluation Condition

Negative-Evaluation Condition

Control Condition

M
ot

he
r-

In
fa

nt
P

hy
si

ol
og

ic
al

C
ov

ar
ia

tio
n

Time (30-s intervals)

Fig. 4.  Covariation of infants’ heart rate (HR) reactivity and mothers’
ventricle contractility (VC) reactivity over time, from reunion through
toy play, in the three evaluation conditions. Covariation is indexed as
the effect of (standardized) infants’ HR reactivity on (standardized)
mothers’ VC reactivity.

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Stress Contagion 941

In sum, our findings demonstrate that infants catch their
mothers’ physiological stress reactivity entirely through
interactions with their mothers, without exposure to the
stressor itself. These effects have implications for under-
standing transgenerational health and well-being. By
showing that maternal stress immediately influences
infants’ stress reactivity, we have demonstrated how stress
“gets under the skin” of children whose parents are
exposed to psychological stressors and have extended
understanding of how the social world influences infants
indirectly through exchanges with their close caregivers.

Author Contributions

W. B. Mendes and S. F. Waters designed the experiment. S. F.
Waters conducted the experiment. S. F. Waters and W. B.
Mendes edited and completed diagnostics of the physiological
data. S. F. Waters and T. V. West conducted the analyses. All
authors contributed to writing the manuscript.

Acknowledgments

We thank Kate Hawley, Helena Karnilowicz, and members of
the Emotion, Health, and Psychophysiology Lab for their many
contributions to this study.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with
respect to their authorship or the publication of this article.

Funding

This research was supported by the Sarlo/Ekman endowment
awarded to W. B. Mendes.

Supplemental Material

Additional supporting information may be found at http://pss
.sagepub.com/content/by/supplemental-data

Notes

1. The heart is dually innervated by sympathetic and parasym-
pathetic branches of the autonomic nervous system, so HR is
not considered a pure measure of sympathetic activation, in
contrast to PEP. That stated, correlations between PEP and HR
in active tasks tend to be medium to large; for example, in this
study, mothers’ PEP and HR during the stress task were strongly
correlated, r(65) = .52, p < .001. 2. Treating mothers’ VC reactivity as the predictor and infants’ HR reactivity as the criterion yielded the same pattern of results. Although we emphasize that we captured a correlation between mothers’ VC reactivity and infants’ HR reactivity, so the choice of criterion and predictor was arbitrary, we treated mothers’ VC reactivity as the criterion because it allowed us to adjust for the effect of mother’s body mass index on mother’s VC reactivity. 3. All data and programming code associated with these results can be obtained online at http://mendes.socialpsychology.org/ publications.

4. We reran all analyses reported here replacing mothers’ VC
reactivity with their HR reactivity, and the results were essen-
tially the same (though the covariation between mothers and
infants was weaker).

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93, 287–295.

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Curt A. Sandman, Elysia Poggi Davis and Laura M. Glynn

Prescient Human Fetuses Thrive

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Remarkable surveillance and response systems have evolved
and are conserved in many species, ranging from desert-
dwelling Western Spadefoot toads to humans, so that they can
detect threats to survival during early development and adjust
their developmental trajectories (Boorse & Denver, 2002).
When tadpoles detect the evaporation of life-sustaining pools
of desert water, their metamorphosis accelerates to ensure
their survival (Denver, 1997, 1999). The human fetal-placental
complex has evolved similar mechanisms to sample informa-
tion from maternal circulation: If the prenatal environment is
perceived to be stressful or hostile, the fetal-placental complex
may promote accelerated developmental trajectories, such
as preterm birth, that ensure short-term survival (Dunkel
Schetter, 2009). Competing models provide different frame-
works for understanding the longer-term consequences associ-
ated with fetal adaption to maternal signals in utero. In this
article, we provide support for one model on the basis of our
findings that congruous prenatal and postnatal environments
confer an adaptive advantage in motor and mental develop-
ment during an infant’s 1st year of life, even when the environ-
ments are unfavorable.

The influential developmental-origins-of-disease model
(Barker, 1998), also known as the fetal-programming model
(Lucas, Fewtrell, & Cole, 1999), predicts that early exposures
to threat or adversity have lifelong negative consequences
for health (Gluckman & Hanson, 2004; Gluckman, Hanson,
& Spencer, 2005). Fetal exposure to adversity increases subse-
quent risk for numerous poor health outcomes, including

cardiovascular disease, non-insulin-dependent diabetes mellitus,
obesity, and vulnerability to stressful life events (Barker,
1998; Kjaer, Wegener, Rosenberg, Lund, & Hougaard, 2010;
McCormack et al., 2003; Roseboom et al., 2000). Although an
impressive body of literature supports this model, most studies
examining fetal programming in human subjects have been
retrospective and have used measures of birth phenotype (e.g.,
birth weight, length of gestation) as surrogate indicators of pre-
natal adversity and as predictors of subsequent health outcomes
(Bohner & Breslau, 2008; Lucas et al., 1999).

Rather than assuming that disease and pathology constitute
the only outcomes for fetal or early developmental exposure to
trauma, a second model proposes a provocative and perhaps
radical alternative. The predictive-adaptive-response (PAR)
model (Gluckman et al., 2005; Gluckman & Hanson, 2004),
also known as the weather-forecasting model (Bateson et al.,
2004), predicts that, under certain conditions, organisms that
are stressed in utero may have an adaptive advantage if
they are confronted with stress later in development but an
increased risk for disease if the conditions of their postnatal
environment are favorable (Bogin, Silva, & Rios, 2007). Stud-
ies that have examined the consequences of discordance
between prenatal and postnatal nutrient environments have

Corresponding Author:
Curt A. Sandman, University of California, Irvine, 333 City Dr. West, Suite
1200, Orange, CA 92686
E-mail: casandma@uci.edu

Prescient Human Fetuses Thrive

Curt A. Sandman1, Elysia Poggi Davis1,2, and Laura M. Glynn1,3
1Department of Psychiatry and Human Behavior, University of California, Irvine; 2Department of Pediatrics,
University of California, Irvine; and 3Crean School of Health and Life Sciences, Chapman University

Abstract

Fetal detection of adversity is a conserved trait that allows many species to adapt their early developmental trajectories to
ensure survival. According to the fetal-programming model, exposure to stressful or hostile conditions in utero is associated
with compromised development and a lifelong risk of adverse health outcomes. In a longitudinal study, we examined the
consequences of prenatal and postnatal exposure to adversity for infant development. We found increased motor and mental
development during the 1st year of life among infants whose mothers experienced congruent levels of depressive symptoms
during and after pregnancy, even when the levels of symptoms were relatively high and the prenatal and postnatal environments
were unfavorable. Congruence between prenatal and postnatal environments prepares the fetus for postnatal life and confers
an adaptive advantage for critical survival functions during early development.

Keywords

predictive adaptive response, fetal programming, depression, stress, HPA axis, infant development, stress reactions

Received 11/16/10; Revision accepted 7/20/11

Research Article

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94 Sandman et al.

provided persuasive support for the PAR model. For instance,
increasing the discrepancy between prenatal and postnatal
nutrition has been shown to increase the risk for altered car-
diovascular function and cardiac hypertrophy in sheep (Cleal
et al., 2007), and humans provided with sufficient nutrition
after near-starvation in utero have been shown to have an
increased risk of developing metabolic diseases (Gluckman
et al., 2005). Prior prospective investigations of the PAR
model as it relates to human development have been limited to
studies of nutritional adversity.

Adequate maternal care is as critical to infant development
as nutrition (Chisholm, 1998; Chugani et al., 2001). When the
quality of maternal care is compromised by postpartum
depression, infants suffer pervasive negative consequences for
health and development (Fihrer, McMahon, & Taylor, 2009;
Kurstjens & Wolke, 2001), even if their mothers’ depressive
symptoms are subclinical (Moehler et al., 2007). Our exten-
sion of the PAR model predicts that a fetus exposed to mater-
nal depressive symptoms in utero will have an adaptive
advantage if it is exposed to the adverse conditions associated
with maternal depressive symptoms in infancy. We assessed
the consequences of prenatal and early postnatal exposure to
maternal depressive symptoms for infants’ mental and psycho-
motor development.

Method
To obtain medical and psychosocial information and to assess
symptoms of maternal depression, we administered compre-
hensive interviews and questionnaires at regular intervals
throughout the pregnancies of a sample of 221 healthy preg-
nant women (Sandman & Davis, 2010). After delivery, moth-
ers and infants were evaluated at regular intervals for 12
months. For analysis, infants were separated into four groups.
Two groups included infants whose mothers had concordant
prenatal and early postnatal depressive symptoms: either high
prenatal and postnatal symptoms (concordant adversity) or
low prenatal and postnatal symptoms (concordant favorabil-
ity) The other two groups included infants whose mothers had
discrepant prenatal and postnatal depressive symptoms: either
high levels of prenatal symptoms and low levels of postnatal
symptoms (prenatal-only adversity) or low levels of prenatal
symptoms and high levels of postnatal symptoms (postnatal-
only adversity; Table 1).

All subjects in our sample of pregnant women were
recruited from a large university medical center. To participate
in the study, subjects had to be pregnant with only one fetus,
English speaking, over the age of 18 years, nonsmoking, free
of conditions that could complicate pregnancy outcomes (e.g.,
endocrine, hepatic, or renal disorders; use of corticosteroid
medications), and free of uterine or cervical abnormalities.
To obtain medical, biological, and psychosocial information,
we examined subjects during laboratory visits performed over
the course of pregnancy at systematic intervals: at 14 to 16
weeks’ gestation (M = 15.31 weeks, SD = 0.92), 24 to 26

weeks’ gestation (M = 25.55 weeks, SD = 0.93), 30 to 32
weeks’ gestation (M = 30.96 weeks, SD = 0.77), and 36 or
more weeks’ gestation (M = 36.7 weeks, SD = 0.83). A research
nurse reviewed maternal medical records to assess prenatal
medical history and birth outcomes. No subjects reported
using alcohol or other drugs during pregnancy. Fourteen sub-
jects reported taking antidepressant (SSRI) medications; 11 of
these subjects were in the concordant-adversity group. Postna-
tal assessments of mothers and their infants were conducted at
3 months, 6 months, and 12 months postpartum.

Psychosocial measures
Maternal depressive symptoms were assessed with a nine-item
version (Santor & Coyne, 1997) of the Center for Epidemio-
logical Studies Depression Scale (CES-D; Radloff, 1977). At
each prenatal time point, subjects indicated how often they
had experienced each listed symptom of depression (e.g., “I
feel depressed”) during the past week, using a 4-point scale
(from 0, rarely or none of the time, to 3, most or all of the
time). This instrument has good internal consistency (Kuder-
Richardson 20 = .87), and raw total scores from the nine-item
version correlate highly with scores from the original scale
(r = .97; Santor & Coyne, 1997). We also administered the
Perceived Stress Scale at each prenatal and postnatal labora-
tory visit (Cohen, Kamarck, & Mermelstein, 1983). This brief,
valid, and reliable scale measures general perceptions of stress
(i.e., the degree to which respondents perceive their lives to be
unpredictable, uncontrollable, or overwhelming) without ref-
erence to the sources of stress (Cohen, 1986; Cohen et al.,
1983). Reported estimates have demonstrated the significant
reliability and predictive and concurrent validity of the scale
(Cohen et al., 1983).

Infant development
Infant development was assessed with the Bayley Scales of
Infant Development, Second Edition (BSID; Bayley, 1993),
which yields two primary scores: the Mental Developmental
Index (MDI) and Psychomotor Developmental Index (PDI).
We obtained infants’ MDI and PDI scores at 3, 6, and 12
months of age. Following conventional methods of scoring of
the BSID, we created composite MDI and PDI scaled scores

Table 1. Assignment of Infants to Groups on the Basis of
Maternal Levels of Depression During the Prenatal and Postnatal
Assessments

Prenatal assessment

Postnatal assessment Not depressed Depressed

Not depressed n = 82 n = 32
Depressed n = 38 n = 69

Note: Groups with concordant prenatal and early postnatal maternal de-
pressive symptoms are shown in boldface.

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Maternal Depression and Infant Outcomes

95

by summing the total number of items achieved on each index
at each time point, converting raw scores to scaled scores by
reference to a chronological table, and correcting for age-
related effects. Examiners were trained by a clinician who had
more than 15 years of experience with the BSID and were
directly supervised by a clinical psychologist. An independent
observer reviewed 20% of the digitally recorded assessments
from each postnatal time point. Interrater reliability was sig-
nificant for all three time points (95% at 3 and 6 months and
93% at 12 months).

Cortisol assessment
In the afternoon during each laboratory visit, blood samples
(20 ml) were drawn from the women by antecubital venipunc-
ture into purple-top EDTA Vacutainers for plasma and red-top
Vacutainers for serum collection. EDTA Vacutainers were
chilled on ice immediately, and aprotinin (Sigma Chemical
Co., St. Louis, MO) was added at 500 KIU/ml. Blood samples
in red-top Vacutainers sat at room temperature until clotted.
Samples were then centrifuged at 2000 × g for 15 min. Plasma
and serum were decanted into polypropylene tubes and stored
at –70 ºC until assayed.

Plasma cortisol levels were determined with a competitive-
binding, solid-phase, enzyme-linked immunosorbent assay
(IBL America, Minneapolis, MN). Plasma samples (20 μl) and
enzyme conjugate (200 μl) were added to the antibody-coated
microtiter wells, thoroughly mixed, and incubated for 60 min at
room temperature. Each well was washed three times with wash
solution (400 μl per well) and struck to remove residual drop-
lets. Substrate solution (100 μl) was added to each well and
incubated for 15 min at room temperature. The absorbance units
were measured at 450 nm within 10 min after the stop solution
(100 μl) had been added. The assay has less than 9% cross-
reactivity with progesterone and less than 2% cross-reactivity
with five other naturally occurring steroids. The interassay and
intra-assay coefficients of variance are reported as less than 8%,
and the minimum detectable level of the assay was 0.25 μg/dL.

Data analysis
We employed a nonlinear, categorical analysis of maternal
depressive symptoms for several reasons. First, the prenatal
and postpartum measures of depression were significantly
skewed, and the postpartum measures exhibited a bimodal dis-
tribution. The median z score for the postpartum measures was
–0.38, indicating nonnormal distribution. Several transforma-
tions of the postpartum data, including a logarithmic transfor-
mation, did not result in normalization and did not eliminate
the bimodal distribution. Second, levels of depressive symp-
toms are typically higher during pregnancy than they are
postpartum. We therefore examined how subjects ranked in
the shifting, bimodal distributions by assessing subjects’
CES-D scores in relation to the median scores. Third, previous
research demonstrating the adaptive response we expected to

observe has suggested that such effects are not linear. For
instance, variables used to compare prenatal and postpartum
conditions typically have been categorical (Bogin et al., 2007;
Jasienska, Thune, & Ellison, 2006; Roth, Lubin, Funk, &
Sweatt, 2009; Silverira, Portella, Goldani, & Barbieri, 2007).

For these reasons, and because of the semicontinuity of the
distributions (Delucchi & Bostrom, 2004), we assigned infants
to groups on the basis of whether their average prenatal
CES-D score across pregnancy and their CES-D score at 3
months postpartum were above or below the median (Stowe,
Hostetter, & Newport, 2005; Table 1). In subsequent analyses,
we assessed depressive symptoms at each of the prenatal time
points to determine the influence of the timing of exposures to
adversity. The effects of prenatal and postnatal exposures to
depression on motor and mental development at each postna-
tal assessment were tested with two-way analyses of covari-
ance (ANCOVAs). Main and interaction effects for prenatal
and postnatal exposures were computed. Potential covariates
in these models included ethnicity, maternal age, maternal
level of income, maternal level of education, obstetric risk
associated with the pregnancy, length of gestation, infant’s
birth order, and infant’s sex. At each postnatal assessment, we
included variables that were statistically significant predictors
of MDI or PDI scores in the corresponding ANCOVA model
to adjust for their contribution to main and interaction effects.
In addition, at 6 and 12 months after birth, the concurrent
maternal depression score was included as a covariate.

Results
At 3 months of age, infants in the two concordant groups per-
formed better than infants in the two discrepant groups did on
measures of psychomotor development, F(1, 215) = 3.89, p < .05 (Fig. 1d), but we found no differences between the groups on measures of mental development, F(1, 215) = 2.46, p = .11 (Fig. 1a). By 6 months of age, infants in the concordant groups achieved superior performance on measures of both psychomo- tor development, F(1, 186) = 4.24, p < .04 (Fig. 1e) and mental development, F(1, 186) = 6.87, p < .01 (Fig. 1b), compared with infants in the two discrepant groups. By 12 months of age, infants in the two concordant groups continued to have higher mental development scores, F(1, 178) = 11.95, p < .001 (Fig. 1c), but not higher psychomotor scores (Fig. 1f), compared with infants in the two discrepant groups. We found no main effects to indicate that exposure to maternal depression alone influ- enced mental or psychomotor development at any age.

Because previous research has demonstrated that fetal vul-
nerability to adverse prenatal environments varies according
to the stage of fetal maturation (Davis & Sandman, 2010),
we examined the effects of concordance between prenatal
depressive symptoms at particular prenatal time points (14
to 16 weeks’ gestation, 24 to 26 weeks’ gestation, 30 to 32
weeks’ gestation, and 36 or more weeks’ gestation) and post-
partum maternal depressive symptoms on infants’ develop-
mental trajectories. Maternal prenatal depressive symptoms at

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96 Sandman et al.

110

105

100
95

90

85

M
D

I S
co

re

Group

3 Months (N = 221)

M
D
I S
co
re

12 Months (n = 186)

Concordant Favorability

Concordant Adversity

Postnatal-Only Adversity

Prenatal-Only Adversity

12 Months (n = 186)
p < .001

6 Months (n = 195)
p < .01

3 Months (N = 221)

p < .05

6 Months (n = 195)
p < .04

110
105
100
95
90
85
110
105
100
95
90
85
M
D
I S
co
re
110
105
100
95
90
85

P
D

I S
co
re
110
105
100
95
90
85
P
D
I S
co
re
110
105
100
95
90
85
P
D
I S
co
re
Group

Group Group

Group
Group

a d

b e

c f

Fig. 1. Mean scores on the Mental Developmental Index (MDI) and Psychomotor Developmental Index (PDI) of the Bayley Scales
of Infant Development (Bayley, 1993) for infants in the concordant-favorability, postnatal-only-adversity, prenatal-only-adversity,
and concordant-adversity groups. The three panels on the left present the mean MDI scores for (a) 3-month-old, (b) 6-month-old, and
(c) 12-month-old infants, and the three panels on the right present the mean PDI scores for (d) 3-month-old, (e) 6-month-old, and
(f) 12-month-old infants. The p values indicate significant differences between the concordant and the discrepant groups. Error bars
indicate standard errors of the mean.

approximately 25 weeks’ gestation had effects consistent with
the PAR model. Among infants who were exposed to congru-
ent symptoms of maternal depression at approximately 25
weeks’ gestation and postpartum, we observed superior mental
development at 3 months, F(1, 212) = 5.69, p < .02; 6 months, F(1, 184) = 4.35, p < .04; and 12 months, F(1, 176) = 4.93,

p < .03. We also observed superior psychomotor development in 6-month-old infants whose mothers reported congruent lev- els of depressive symptoms at approximately 25 weeks’ gesta- tion and postpartum, F(1, 184) = 5.35, p < .02. No other single prenatal time points were consistently associated with the effects of prenatal and postnatal congruence.

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Maternal Depression and Infant Outcomes 97

To investigate whether congruence between prenatal and
postnatal maternal depressive symptoms exerts unique influ-
ences on child development, we assessed whether the degree
and continuity of maternal perceptions of recent stress also
affected the infants’ development. Despite our findings for
maternal depression, we found no evidence that congruence
between maternal perceptions of stress during and after preg-
nancy influenced infants’ mental or motor development. In
addition, we investigated the possibility that stress hormones
from the hypothalamic-pituitary-adrenal (HPA) axis were asso-
ciated with prenatal maternal depression. The effects of maternal
cortisol were examined in a series of 2 (period: prenatal, post-
natal) × 2 (symptoms: depression, no depression) ANCOVAs,
one for each prenatal time point. Congruence between prenatal
and postnatal maternal depression was not associated with
maternal level of cortisol at any gestational age.

Discussion
This prospective study is the first to evaluate the effects of
congruence between prenatal and postnatal levels of maternal
depression on human infant development. We obtained sup-
port for the PAR model with our counterintuitive finding that
infants thrive, at least on dimensions of critical psychomotor
and mental development, when their prenatal and postnatal
environments are congruent, even if the conditions of those
environments are adverse (Kurstjens & Wolke, 2001; Moehler
et al., 2007). Moreover, postpartum euthymia in mothers did
not benefit the psychomotor and mental development of
infants who had been exposed to maternal depressive symp-
toms in utero; this finding is consistent with the predictions of
the PAR model. Specifically, infants’ mental and motor func-
tions were relatively impaired when their mothers exhibited
symptoms of depression during pregnancy but became euthy-
mic during the first 3 months after birth. These results are con-
sistent both with reports that exposure to incongruent prenatal
and postnatal nutritional conditions increases infants’ risk
of developing metabolic disease and with findings of
adaptive advantages among infants exposed to matching pre-
natal and postnatal nutritional environments (Cleal et al.,
2007; Gluckman & Hanson, 2004).

Our findings indicate that stability between the prenatal and
the postnatal environments prepares the fetus for postnatal life
and that this preparation confers an advantage in critical sur-
vival functions during early development. The progression from
superior psychomotor ability to superior mental ability during
the 1st year of life among infants in the two concordant groups
might indicate both a short-term adaptive response and the
selection of a special characteristic that may be critical for sur-
vival (Bateson et al., 2004). Advanced psychomotor skills are
advantageous early in development, when infants’ capacities for
language and reasoning are undeveloped. As infants approach 1
year of age, they begin to use rudimentary language and reason-
ing, and it is reasonable to assume that advanced mental abilities
increase infants’ opportunity for survival. It is possible that a

progression of special skill advantages continues throughout the
life span of infants such as those in our concordant groups and
that accelerated psychomotor and mental development is
replaced by advantages in other proficiencies.

The observed effects that were consistent with the PAR
model were largely attributable to congruence between mater-
nal depressive symptoms at midgestation (approximately 25
weeks) and postpartum. The human fetus may be especially
sensitive or vulnerable to adversity during this period, as has
been reported previously (Davis et al., 2005; DiPietro, Novak,
Costigan, Atella, & Reusing, 2006; Glynn, Wadhwa, Dunkel
Schetter, & Sandman, 2001; Sandman, Davis, Buss, & Glynn,
2011). Moreover, in a study of another large cohort of women,
we found that biological and psychological symptoms of
maternal depression at approximately 25 weeks’ gestation
were the strongest predictors of postpartum depression (Yim
et al., 2010; Yim, Glynn, Dunkel Schetter, Chicz-DeMet, &
Sandman, 2009). These findings indicate that the fetus is most
sensitive to maternal signals of adversity when those signals
are the most predictive of future outcomes.

Without question, congruently favorable conditions before
and after birth are beneficial for developing infants and
children (Ainsworth, Blehar, Waters, & Wall, 1978; Calkins,
Graziano, Berdan, Keane, & Degnan, 2008; Kochanska, Phi-
libert, & Barry, 2009). Our finding that congruently unfavor-
able circumstances can also convey adaptive advantages may
be at odds with the predominant view of development, which
assumes that early exposures to adversity are associated with
significant lifelong costs to survival, growth, and reproduc-
tion. Other models of development, however, propose that
early exposures to stress have beneficial consequences later in
life. For instance, the stress-inoculation model predicts that
exposure to mild stress during early development promotes
resilience in the face of stressful (i.e., congruent) circum-
stances later in life (Lyons & Parker, 2007). The theory of bio-
logical sensitivity to context (Ellis, Boyce, Belsky, Bakermans-
Kranenburg, & van Ijzendoorn, 2011) posits that early expo-
sure to stress increases the lability of responses to subsequent
adversity. This increased lability results in increased impair-
ment after exposure to stress later in life but also an enhanced
ability to benefit from supportive and protective features of the
environment.

The debate about the adaptive consequences of early expo-
sure to adversity, specifically in relation to the rate of matura-
tion, is yet unresolved. According to one view, the delayed
growth and reproduction following early exposure to adversity
may be adaptive, given that delayed growth and reproduction
will reduce nutritional requirements if resources are scarce
during early development (Bogin et al., 2007). There is some
evidence, however, that early exposure to psychosocial adver-
sity accelerates maturation, especially in the area of reproduc-
tive development. For example, exposures to psychosocial
adversity during early development and again later in life
are associated with accelerated sexual maturation in girls
(Coall & Chisholm, 2003, 2010; Nettle, Coall, & Dickins,

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98 Sandman et al.

2010). Researchers have argued that such early maturation
maximizes the probability of reproduction and allows females
to increase their number of offspring; in conditions of increased
health risk, this greater number of offspring will ensure that
more offspring survive.

Considering our findings in the context of this debate sug-
gests competing explanations for the similarity between the
concordant groups in our study. First, it is possible that the
concordant-adversity group exhibited the accelerated matura-
tion associated with early adversity but that the mental and
motor advantages observed among infants in the concordant-
favorability group reflected the benefits of relatively favorable
prenatal and postnatal environments. Second, the similarities
between the two concordant groups may have resulted from
the same factors. If so, either both groups or neither group
exhibited accelerated maturation. Subsequent follow-up stud-
ies of the subjects in these groups could determine whether
either group exhibited the life-history costs typically associ-
ated with accelerated maturation. However, the improved
motor and cognitive skills in the two concordant groups may
have resulted not from accelerated maturation but rather from
fetal prediction of and preparation for postnatal life. We
believe that our findings support the conclusion that it was the
congruence between prenatal and postnatal exposures to
maternal depression, and not the exposure to maternal depres-
sion itself, that determined infants’ outcomes.

The precise mechanism by which a pregnant woman com-
municates her psychological state to her fetus is unknown.
One possibility is that maternal stress and depression expose
the fetus to elevated levels of stress hormones. The relation
between psychosocial measures of adversity, including depres-
sion, and HPA activity during pregnancy was nonsignificant in
our study and has been found to be low or nonsignificant in a
number of other studies (Davis & Sandman, 2010; Harville,
Savitz, Dole, Herring, & Thorp, 2009; Kramer et al., 2009);
these findings suggest that stress hormones alone are not the
mechanism by which maternal signals of psychosocial adver-
sity are communicated to the fetus.

Fetal exposure to maternal depression has been shown to be
associated with increased methylation of the glucocorticoid
receptor gene in neonates and with increased HPA responses
to stress or adversity; this finding suggests that an epigenetic
mechanism may underlie both the maternal communication of
adversity to the fetus and the persistent influence of the expo-
sure (Oberlander et al., 2008). In addition, animal studies have
indicated that specific patterns of maternal care during early
development can alter the methylation of the nerve growth
factor-inducible protein A (NGFI-A) binding site in a region of
the Nr3c1 promoter responsible for the control of hippocam-
pal glucocorticoid receptor expression; such findings support
the possibility of this epigenetic effect and point to its direct
implications for areas of the nervous system involved with
mental development (Weaver et al., 2004). These findings, and
findings from other studies reporting a link between persisting
altered expression of the brain-derived neurotrophic factor in

the prefrontal cortex and exposure to early adversity (Roth
et al., 2009), suggest possible routes of maternal influence on
fetal and early infant neurological development that have pro-
found implications for infants’ adjustments to life challenges.

Acknowledgments

This project was conceived and designed by C. A. S., E. P. D., and
L. M. G. Biological and medical reviews were conducted by C. A. S.
and L. M. G. Maternal postnatal assessments were made by L. M. G.
Longitudinal analysis of infant behavior was carried out by E. P. D.
Statistical analyses was performed by L. M. G. and C. A. S. The
authors are grateful for the outstanding assistance of Cheryl Crippen,
Carol Holliday, Christina Canino, Christine Cordova, and Natalie
Hernandez. The authors wish to thank the families who participated
in this longitudinal project.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with
respect to their authorship or the publication of this article.

Funding

This research was supported by awards from the National Institutes
of Health (NS-41298, HD-51852, and HD-28413 to C. A. S.; HD-
40967 to L. M. G.).

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https://doi.org/10.1177/1359105316687628

Journal of Health Psychology
2019, Vol. 24(7) 929 –940
© The Author(s) 2017

Article

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DOI: 10.1177/1359105316687628
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Introduction

Birth of a child is a major event for fathers.
Research reveals that the Western World has
seen social and cultural shifts in the involvement
and presence of fathers. In a qualitative study of
what the transition to parenthood meant Barclay
and Lupton (1999) concluded that for first-time
fathers, becoming a father involved changes in
both self-identity and relationship with their
partner. In addition, Henwood and Procter (2003)
concluded that a father is expected to be caring,
nurturing, understanding, approachable and sup-
portive; able to work with his partner as part of a
childrearing team; as well as willing to take an
active role in the running of the household.
Barclay and Lupton (1999) found that men must
address complex and evolving emotions as they

establish an attachment relationship with their
child. This process began with the advent of their
partner’s pregnancy followed by the father’s
experience of childbirth. While men expressed
excitement and joy about the birth of a first child,
they also expressed fear about becoming a parent
as they felt underprepared and unsure of the
expectations their partners may have of their role

First-time fathers’ perception
of their childbirth experiences

Anne M Howarth,
Kate M Scott and Nicola R Swain

Abstract
Birth satisfaction impacts on a man’s adjustment to his new role as father. Fathers have been found to have
needs similar to those of mothers during pregnancy and childbirth. Research suggests that these needs
may not be being met for first-time fathers. In a quantitative survey, fathers’ birth satisfaction was similar
to mothers. This study then used a phenomenological form of thematic analysis to gain an insight into the
birth experiences of 155 first-time New Zealand fathers. Core themes included safety of mother and baby,
understanding support role, mother in control and managing pain and care and communication after birth. Fathers
commented on what impacted on their childbirth experiences and in so doing outlined their needs for a
positive experience. Fathers experienced a high level of satisfaction along with a need to be involved and
included.

Keywords
dissatisfaction, health psychology, infants, interpretative phenomenological analysis, males, postpartum,
pregnancy, satisfaction, well-being

University of Otago, New Zealand

Corresponding author:
Nicola R Swain, Department of Psychological Medicine,
Dunedin School of Medicine, University of Otago,
Dunedin 9054, New Zealand.
Email: nicola.swain@otago.ac.nz

687628HPQ0010.1177/1359105316687628Journal of Health PsychologyHowarth et al.
research-article2017

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930 Journal of Health Psychology 24(7)

(Deave et al., 2008; Hildingsson et al., 2014).
Hildingsson et al. (2014) surveyed 1047 expect-
ant fathers in Sweden using the Fear of Birth
Scale. They conclude that around 14 per cent of
men experienced fear, and this was associated
with a negative birth experience.

One study interviewed 10 first-time fathers
in Sweden and found issues included the
father’s excitement tinged with concerns for the
safety of the mother and birthing child, the shar-
ing of this experience – his involvement and
appreciation of midwife support to be involved,
the effect the mother’s ability to cope and his
delight in a safe and healthy outcome for mother
and baby (Premberg et al., 2011).

In another study, 20 new fathers in England
were interviewed, and analysis indicated that
fathers had issues similar to those of their part-
ners. These included the need for support mech-
anisms, more inclusion in antenatal activities
and the need for information, including the
changes they can expect in their relationships
with their partners. Men felt that they were
without the support mechanisms available to
their pregnant partners, often leaving them feel-
ing isolated, made worse when they were with-
out the role models and guidelines that would
have enhanced their journey into fatherhood
(Deave and Johnson, 2008).

Before the child is born, men are often
stressed because they are unsure of their child-
birth role but are driven to be present by their
perceptions of cultural expectations (Johnson,
2002). Chapman (2000) revealed that men
tended to find it very difficult to cope with the
changes they witnessed in their partners during
childbirth, as well as with the pain they endured.
Labour pain often left men feeling excluded and
anxious about what was happening (Deave and
Johnson, 2008). Fathers expressed their concern
about feeling they had lost their partners to the
pain of the labour they were experiencing
(Chapman, 2000). Feeling safe has been explored
from the perspective of mothers, and this might
also be expected to be applicable to fathers
(Howarth et al., 2010, 2013).

Deave and Johnson (2008) reported that
being involved in the antenatal provisions,

being well informed about what to expect dur-
ing labour and birth, feeling he has a role to
play during labour and birth and knowing what
it is and feeling he has his own support network
dedicated to his needs can enhance a father’s
perception of the birth of his child. In an earlier
study, Johnson (2002) reported similar findings,
meeting these needs can positively influence
perception of childbirth and consequently the
new father’s relationship with his child.

Using quantitative methodology, Greenhalgh
et al. (2000) found that how the father experi-
enced his partner’s labour and birth may be a
potential risk factor for the father’s later psycho-
social well-being. Fathers who had a positive
experience of childbirth were more likely to have
no symptoms of depression at 6 weeks postpar-
tum compared to those who had unmet expecta-
tions of their birthing experience. Boyce et al.
(2007) also found that those first-time fathers
who did not have sufficient knowledge and
understanding of pregnancy, labour and birth
were at risk of feeling psychological distress.

Another recent Swedish study interviewed
eight first-time fathers. Their analysis resulted
in one major theme ‘a transformative experi-
ence’ which had the sub-themes: preparing for
childbirth, feeling vulnerable in a new situation,
being confirmed as part of a unit and meeting
the child for the first time. They conclude that
the needs of the fathers should be given more
recognition during childbirth.

In a survey of 78 UK fathers, it was found that
how men experienced childbirth had a later
effect on their emotional well-being (Greenhalgh
et al., 2000). Added to this, men were commonly
not given the opportunity to talk about their con-
cerns, thus leaving these concerns unresolved
(Friedewald et al., 2005). Similarly, Boyce et al.
(2007) concluded that providing men with more
information regarding pregnancy, childbirth and
parenting would be a positive step in assisting
these men to overcome their anxieties. Feeling
better about their partner’s pregnancy and the
birth of their child could assist the father make
the transition from couple-hood to family with
child and thus encourage him to be a supportive
partner (Castle et al., 2008). This, in turn, could

Howarth et al. 931

assist the mother in her endeavours to develop a
sense of herself as an effective and loving mother.
Thus, the prospect of quality relationships is
enhanced, with the child more likely to develop a
secure attachment (Fowles and Horowitz, 2006;
Howarth et al., 2011a; Nelson, 2004).

As part of a larger study, 111 Swedish fathers
commented on the birth experience, and content
analysis was conducted (Johansson et al., 2012).
Five categories of response were revealed and
named: competence of health-care profession-
als, professionals approach and involvement in
care, experiences of childbirth, expectations
about childbirth and the organisation.

Johansson et al. (2015) conducted a meta-
synthesis of how fathers experience childbirth.
They found only eight studies that met criteria
for inclusion: there were four from Sweden,
two from England and one each from Malawi
and Nepal. This reveals the lack of representa-
tive international reports published of father
experiences.

This research seeks to provide more evi-
dence about the importance of the role of first-
time fathers and provide some reflection on
their experiences. A qualitative study seems
appropriate as there is still some uncertainty
about what is important to first-time fathers wit-
nessing the birth of their babies. Additionally,
most published evidence appears to be from
Sweden and the United Kingdom, so this article
contributes by investigating another health sys-
tem found in New Zealand.

Method

Data collection approach

This study was part of a larger research project
examining the impact of childbirth preparation.
Participants recruited were couples expecting
their first child. A survey questionnaire was
posted to fathers as part of this study.

Participants

A national sample of 155 first-time fathers aged
over 18 years commented on aspects of their

childbirth experiences. Couples were eligible to
participate in this study if they were cohabiting
and intended to parent the child together. All
participants were sufficiently literate. Various
advertising took place, and the participants
were required to contact the researcher if they
were interested. Once they had contacted the
researcher, they all received information and
signed consent to participate.

Materials

Participants were recruited using posters, flyers,
advertisements and social media. A post-birth ques-
tionnaire provided the material for this analysis.
Specifically, the Mackey Childbirth Satisfaction
Rating Scale New Zealand Adaptation (adapted
with permission for fathers) which is a 34-item
scale measuring childbirth satisfaction was used
(Goodman et al., 2004). Throughout the question-
naire, fathers were asked to write down their
thoughts. Additional qualitative data the fathers
included with their questionnaires were also
included.

Procedure

All participants completed the enrolment docu-
ments giving their informed consent for partici-
pation in the study. Participants chose to
complete either paper or online versions. Ethical
approval from the New Zealand Lower South
Regional Ethics Committee was gained for this
study (reference number: LRS/10/11/052).

Quantitative analysis

Mackey Childbirth Satisfaction Rating Scale New
Zealand Adaptation. Birth satisfaction was
measured using the Mackey Childbirth Satis-
faction Rating Scale (Goodman et al., 2004)
New Zealand Adaptation (also adapted for
fathers). The 34-item scale contains questions
related to the behaviours of self, partner, baby,
nurse (midwife) and physicians. A further six
questions relate to expectations, whether the
experience was positive/negative, and give the
opportunity of commenting on the positive and

932 Journal of Health Psychology 24(7)

negative aspects of the labour and birth experi-
ence. The higher the score, the greater the birth
satisfaction.

The Mackey Childbirth Satisfaction Rating
Scale (Goodman et al., 2004) was developed for
women giving birth in the American maternity
system. This required some minor adjustments
to adapt it to the New Zealand midwifery-
driven maternity system. Consideration was
given to differing terminology, for example, the
term nurse was altered to midwife. Adaptations
to the questionnaires for fathers required word-
ing changes which recognised his role as birth
coach. For example, Your overall labour expe-
rience became Your overall experience of your
partner’s labour for the father’s questionnaire.
Permission was requested and given by Mackey
to use this scale and make these adaptations.

A summary of responses on the Mackey
Birth Satisfaction Rating Scale was created
using Excel. Means of subscales were created.

Analytic procedure – phenomenological thematic
analysis. A form of phenomenological thematic
analysis informed by interpretative phenomeno-
logical analysis (IPA) was used to examine the
data (Reid et al., 2005; Smith, 1995, 1996; Smith
et al., 1999, 2009; Trochim, 2006). Thematic
analysis informed by IPA provided a structure
within which data could be collated and coded
(Braun and Clarke, 2006; Smith et al., 2009).
Once the data were entered onto a database,
there was an initial reading of comments. Pat-
terns within the data, using information coded
across the data corpus, were identified. Data
were then organised into meaningful patterns
and groups. Data from the transcript of com-
ments that supported each code were briefly
summarised. Themes emerged from the sum-
mary. Connections between the initial themes
were identified and organised into broader
themes. Core themes were identified along with
related sub-themes, and a pattern of hierarchy
became apparent. This process continued until
the primary analyst (A.M.H.) felt the themes
provided a good overview of the data corpus. A
second qualitative data analyst read the com-
ments and independently organised the data into

themes. These were discussed with the primary
researcher, and an agreement was formed. In the
following presentation of results using verbatim
quotes, participants are referred to by their study
numbers.

Results

Demographic characteristics

Ages ranged from 20 to 49 years with a median
of 30.0 years. A total of 66 per cent of fathers
were married with the others in de facto rela-
tionships. A total of 59 per cent owned their
own homes, while 41 per cent were in rental
accommodation. A total of 78 per cent had some
form of post-secondary qualification. A total of
87 per cent were in full-time employment,
5.2 per cent were students and the others were
stay-at-home or unemployed. Approximately
83 per cent of fathers were identified as of
European descent and 6 per cent of Maori
descent. Approximately 12 per cent of fathers
had immigrated to New Zealand in the last
5 years.

An analysis of the fathers’ responses on the
Mackey Childbirth Satisfaction Rating Scale
was conducted. Results for fathers are presented
with three comparison groups. First, mothers in
this study and then published data from another
study using the same scale. It can be seen that
the satisfaction ratings of fathers are similar to
those of mothers in this study, as well as inter-
nationally. However, satisfaction with physi-
cians appears lower in this sample than in
international samples (Table 1).

Fathers’ perceptions of their childbirth
experiences

Men reported becoming a father was a life-
changing experience (Table 2). Some fathers
reported satisfying experiences, while others
were so dissatisfied that they made comments
such as

Don’t think I will be present for any future
children’s birth. (005)

Howarth et al. 933

Theme 1: safety of mother and baby

For fathers, safety was a primary concern. To
facilitate safety, fathers wanted to ensure the
best possible care. This involved professional-
ism from maternity health caregivers and a safe
and controlled birth environment.

Safety as a priority. Fathers were aware that com-
plications during labour and birth could, and
did, arise. They expressed caution and concern:

My plan was to ensure mum and baby were kept
as safe and comfortable as possible during the
process. (099)

Fathers wished to ensure that the mothers
were getting the best care available. This
involved the professionalism demonstrated by
the lead maternity carer and other medical pro-
fessionals (obstetricians, registrars, anaesthetists,

nurses and hospital midwives most commonly
mentioned) and the perceived safety of the envi-
ronment in which the birth was planned to take
place; that is, mothers were giving birth in what
the partner perceived to be a safe and controlled
environment. When these conditions were met,
the father expressed his satisfaction. Underlying
the joy at a good outcome was the relief felt that
mother and baby had come through safely as
reflected in the following comments:

[the mother] survived the experience … was not
how we planned but mum and baby alive and […]
well and looked after well by hospital staff. (053)

Healthy mother and baby. Fathers were con-
cerned both for a healthy baby and that the
mother came through unscathed and in good
health. When either mother or baby suffered
health complications, the father was alarmed
and apprehensive, and his satisfaction was
inhibited:

Didn’t enjoy it at all. Lots of worry about her and
the baby … seeing the baby pretty dormant when
she came out. (066)

[I was] very dissatisfied as we had quite a wee
shock when he came out, firstly he had his cord
all wrapped around him and then he stopped
breathing after he came out. (043)

When things went well, fathers expressed
their satisfaction:

Little one and partner were healthy in the end, so
it was a win. (042)

Table 1. Mean scores from the Mackey
Satisfaction with Childbirth Rating Scale (scores
from 1 to 5).

Fathers Mothers Belgium
mothersa

Netherlands
mothersa

General 4.11 3.79 4.14 3.93
Self 3.81 3.71 3.99 3.66
Baby 4.20 4.16 4.49 4.34
Midwife 4.25 4.33 4.62 4.33
Physician 3.24 2.98 4.37 4.05
Partner 3.97 4.55 4.74 4.59

aBelgium and Netherlands data from Christiaens and
Bracke (2009).

Table 2. Outline of the major themes with their sub-themes showing influences on first-time father’s
birth satisfaction.

Major
themes

Safety of mother and
baby

Understanding support
role

Mother in control
and managing pain

Care and
communication
after birth

Sub-
themes

Safety as a priority
Healthy mother and
baby
Professional support

Support role
understood
Teamwork with mother
and professionals
Making a difference

Mother seemed
to be in control
of birth process
Issues with pain

Complications
and interventions
Communication
Bonding

934 Journal of Health Psychology 24(7)

Very happy that she was healthy … Happiest
moment ever. (187)

Staff professionalism was described when
individuals demonstrated a high knowledge
base, a high level of skills and the competence
to use these appropriately for each individual
circumstance. Fathers also felt greater confi-
dence in the professionalism of midwives and
medical staff when they worked well together
as a team, when they were prepared to call in
someone more knowledgeable if the situation
warranted and if they communicated well. They
made comments such as

Dedicated midwife; Special mention to the sound
reaction by the obstetrician once the baby’s heart
rate started increasing. I was very impressed by
how well managed the c-section was […] and
how well we were looked after. (122)

Excellent. Our experience ended up being very
‘medical’, however everyone – including the
anaesthetist and registrar – were very personable
and relaxed. (042)

Not all fathers felt their carers demon-
strated professional behaviours, and this left
them distressed and concerned for the well-
being of their loved ones. They were dissatis-
fied with this aspect of their experience of the
birth of their babies and expressed their con-
cerns accordingly:

The midwife put her own interests first, didn’t
provide the care we expected […]. Once baby
was born the midwife was angry and was most
interested in getting home. (172)

Hospital staff were terrible, unhelpful, left us
feeling very alone and unsure of what to do. (128)

Theme 2: understanding support role

Support role understood. Fathers wanted to feel
included and involved in the mother’s labour,
especially if complications occurred and plans
had to change with new decisions, often unex-
pected, to be made. Those who felt included

and involved expressed their satisfaction, while
those fathers who felt excluded were dissatis-
fied and felt that their experience of the birth of
their child had been compromised:

I asked my partner if she had asked the midwife to
call me of which she stated that she had asked the
midwife many times to call me and she always
had an excuse to not do so … The midwife totally
destroyed the experience for both of us. (111)

Those fathers who established their role in the
mother’s labour and delivery of their child and
prepared themselves accordingly or who simply
found themselves responding positively to the
labour and birth reported greater satisfaction:

I didn’t want to be very involved beforehand, but
when it all started, it was just me in there with the
midwife, so I ended up getting a lot more involved
than I had wanted to, but it was great. (043)

than those partners who found themselves
wanting to have a role to play but having no
idea what it was and consequently feeling
helpless:

[I] didn’t really know what to say or do, bit
stunned. (185)

Teamwork. Those fathers who felt themselves
included/involved commented on the sense of
teamwork they experienced working with the
mother to assist her to give birth to their child.
This sense of teamwork, along with feeling
included/involved, enhanced the family bond-
ing process:

Wonderful feeling of teamwork and bonding
between us. (051)

When the midwife and other medical pro-
fessionals facilitated the fathers’ ability to
support and encourage the mother, they felt a
greater sense of satisfaction even when they
had not initially known what their role was.
Those who received advice and guidance from
their professional felt that they were better
supporters:

Howarth et al. 935

She [midwife] encouraged me and advised where
the best place to be was in each situation, and
really encouraged me to be part of it. (152)

When the father felt confident that he had
made a difference by offering his support and
encouragement to the mother he was filled with
a sense of satisfaction with both himself and his
overall experience of the birth of his child:

I coped far better than I thought – probably
because the nerves got pushed to the background
as I focused on the moment and I felt I was
helping. (038)

Theme 3: mother in control and
managing pain

Mother seemed in control. When the father per-
ceived the mother to be coping, his anxiety was
reduced and he felt less distress. This carried
through to situations where medical interven-
tions became essential. If the father perceived
her to be handling the situation, his sense of sat-
isfaction with the birthing process was
enhanced, as was his admiration for the mother
and he commented on

how well she coped throughout. Although she
was clearly in a lot of pain she made it through by
focusing on herself and was able to still make
good decisions and was open to assistance from
myself and the midwives. (038)

Fathers were sensitive to the manner in
which mothers managed their birthing process.
If mothers were perceived as being in control of
their body and decision-making, the father felt
greater satisfaction with his experience too.
They also felt pride in her achievement and
admiration for their partner and expressed in
comments such as

The way my wife handled herself was second to
none. I was so proud of her. She could not have
done any better. (103)

Issues with pain. The father felt a sense of relief
when the mother was able to manage the pain

using the strategies she had selected and not
become overwhelmed and distressed. They also
felt admiration and pride in her achievement, and
this enhanced the fathers’ sense of satisfaction:

Partner did very well managing her pain as much
as she could. (005)

Fathers found it difficult seeing the mothers
in pain, especially when over a prolonged
period of time and when they felt helpless to do
anything to relieve that pain. They reported less
satisfaction with their experience of childbirth:

Probably one of the most harrowing experiences
of my life to see and hear someone I love in that
much pain and to be so helpless to do anything
about it. (053)

The father felt happier when she managed to
give an impression that she was not experienc-
ing too much pain or when she was given medi-
cation to make the pain more tolerable:

One of the perks of having an epidural is not
having to see your partner in pain. Despite
wanting minimal medication, the epidural was
unplanned, it was awesome and nice that my
partner had no pain throughout the labour. (181)

Theme 4: care and communication
after birth

Complications. The birth itself contributed
towards the father’s satisfaction/dissatisfaction.
Fathers hoped that the mother would experi-
ence a short labour which was not too painful
and that the birth would be easy and without
complications. For some fathers, this was the
case, and it led them to make the following
comments explaining why they experienced
satisfaction:

It was a lot easier for her (and for me) than I
expected. (092)

My partner was cool, calm and collected; medical
interventions were avoided; process went smoothly.
(061)

936 Journal of Health Psychology 24(7)

Not all couples experienced a complication-
free birthing process, with medical intervention
becoming a necessity for some. Fathers did not
want to see their partners develop such compli-
cations during labour and birth. When unex-
pected complications did develop, fathers were
disappointed and could find these scary and dis-
tressing. If the mother was distressed, then it
became even harder for the father to cope, and
his satisfaction with the birth of his baby was
diminished:

It was wrenching when the ventouse proved
insufficient to turn the baby and a caesarian was
required. […] The whole experience was horrific
at the time. (040)

[I felt] an emptiness, indescribable. [Mother]
drugged up, unable to get baby out, on an
operating theatre, awake for 25 hours, had to let
the delivery occur in control of 13 people. (005)

Fathers said that they needed support, expla-
nation, acknowledgement and reassurance and
to feel that their humanity was recognised.
When these needs were met, what initially was
both frightening and a major disappointment
had the potential to reduce the mother’s distress
and calm her which consequently increased the
father’s satisfaction with his birth experience:

[Was a] successful outcome in the end; competent
staff gave me confidence even when medical
issues arose; midwives mostly friendly and
conscientious […] when needed doctors were
fantastic and reassuring [ventouse delivery]. (053)

Communication. Keeping parents informed of
how the birthing process was progressing was
important for all couples but became particu-
larly so when any complications occurred. In
some instances, parents were not only unin-
formed but were excluded for the decision-
making process, or doctors pressed them to
agree to decisions they were not altogether
comfortable with. Fathers were protective of
mothers and were dissatisfied if they felt they
were not being treated with empathy. Conflict-
ing opinions aired in front of parents were also

disturbing as were staff who did not communi-
cate well with each other or the parents. Such
experiences left fathers expressing their dissat-
isfaction with comments including

You can really feel left out of decision making in
hospital especially when things go wrong …
anaesthetist was great but OB registrar not so
forthcoming with thoughts or letting us know
what was going on. (053)

Once the specialists took over Partner and I were
not included in any decisions. (095)

3 groups were disagreeing/stressed (2 midwives,
NICU, emergency team). (120)

Other couples felt that they had been kept
very well informed by midwives and other med-
ical professionals and that they were able to
understand what was happening and take part in
decision-making processes. And if that was not
possible because of an emergency situation,
they were appropriately debriefed afterwards.
Fathers expressed their satisfaction, even when
the actual experience might have been difficult:

We were both well informed during each step and
I felt our midwife and others provided information
fast and clearly which kept us both with the
feeling that things were well under control. (099)

[There was] great communication by medical
staff during the birth. (040)

[There was] no time for consultation but talked to
us after. (177)

Bonding. Seeing baby finally arrive was a very
special moment for both parents:

Then finally seeing the baby come out when he
was almost there was very amazing. (043)

Seeing my baby for the first time and knowing
what we have been waiting for. (134)

Once baby was born, fathers were excited that
they could finally hold their baby for the first
time. However, fathers, while wanting to hold

Howarth et al. 937

the baby as soon as possible, were also con-
cerned that the mothers got the opportunity.
Fathers also expressed satisfaction with their part
in the first moments of baby’s life when they had
the opportunity to cut the umbilical cord. Fathers
also expressed satisfaction with their part in the
first moments of baby’s life when they had the
opportunity to cut the umbilical cord. Comments
such as the following conveyed this satisfaction:

He got loads of skin on skin with his mum which
was lovely. (184)

[I] wasn’t sure if I wanted to cut the cord but was
fine at the time and really glad I did. (93)

When fathers assisted with delivery and/or
got the opportunity to hold baby for the first
time, it was a very special moment for them,
and they expressed their satisfaction with their
experience:

Due to partner needing to be taken to theatre I was
given Baby for skin to skin within 15 minutes of
her being born and [I] cuddle[d] her for over
3 hours until partner was brought back. (181)

Sharing this journey of birth had the capacity
to bring couples closer together and strengthen
relationships. The time together with the baby
immediately after the birth was important:

Our relationship is much stronger for having
survived the experience. (053)

Difficult journey but overall helped me appreciate
and love my wife more for it. […] The chance to
deliver my son helped with bonding process. (034)

New families wanted the space and privacy
to begin adjusting to this life-changing event.
When hospital facilities were inadequate to
support, the continuation of this process distress
was caused. Fathers were unhappy if mothers
were transferred soon after birth to wards that
meant room sharing with other new mothers.
The following father clearly expressed the emo-
tional impact being separated from his new
family so soon after the birth had on him:

[It] was heart breaking when they said I couldn’t
stay the night. I had been with her that whole time
and suddenly I had to go. (027)

Discussion

Fathers in this study recognised that the birth of
their child was a life-changing event for them-
selves as well as mothers. Birth satisfaction has
been identified as a key element affecting
fathers’ as well as mothers’ psychosocial well-
being (Boyce et al., 2007; Castle et al., 2008;
Deave and Johnson, 2008; Fenwick et al., 2012;
Friedewald, 2007; Greenhalgh et al., 2000;
Longworth and Kingdon, 2011; Lothian, 2008).
Fathers in this study were clear about what
enhanced their satisfaction with their birth
experience and what did not. Their experiences
provide an understanding of what the fathers
felt they needed.

Interestingly, quantitative results from the
Mackey Childbirth Satisfaction Rating Scale
show fathers feel similar to mothers about
childbirth satisfaction. The participants in this
study were also similar to those surveyed inter-
nationally. Ledenfors and Berterö (2016) report
that fathers are generally satisfied with the birth
experience despite feeling like an outsider.
They attribute this to feelings of gratitude and
relief. Notably, the New Zealand sample was
less satisfied with medical assistance than other
countries, but this could be an artefact of the
midwife-led system in New Zealand. Birthing
mothers will only need to see medical staff
when complications arise, which may lead to
lower satisfaction rating of the medical staff.

In this study, the safety of mother and baby,
as found by Premberg et al. (2011), was under-
standably of greatest of concern for the father.
When fathers perceived that staff professional-
ism was ensuring, the mother and baby were
getting the best care suited to their situation they
expressed greater birth satisfaction than those
fathers who perceived the care the mothers and/
or babies got was inadequate. This finding sup-
ports research suggesting fathers’ concerns
about safety need to be treated respectfully and
empathetically (Johansson et al., 2012). Fathers

938 Journal of Health Psychology 24(7)

helped to decide whether hospital or home was a
safe option for delivery of their baby and confi-
dence in this decision added to feelings of safety.
This is similar to the Swedish study by Johansson
et al. (2012) where a theme that emerged was
competence of health-care professionals and
encompasses similar concerns of professional-
ism of staff and medical care of partner. A
healthy baby and healthy mother was under-
standably the outcome desired by all fathers,
supporting the finding of Premberg et al. (2011).
As Johansson et al. (2012) found, anything that
threatened that outcome created stress that
detracted from the perception of the whole expe-
rience for fathers in this study.

Fathers expressed satisfaction with their
experience when they understood their support
role. Previous research has found being
included may reduce the risk of post-traumatic
stress disorder for fathers following a trau-
matic birth (White, 2007). When the father
perceived that he had really made a positive
difference to the mother’s experience of labour
and childbirth, he expressed greater satisfac-
tion than those fathers who struggled to feel
included and involved. These results find sup-
port from another study by Longworth and
Kingdon (2011) who found men struggled to
find their role in childbirth. Hildingsson et al.
(2011) also reported that support from the
midwife was an important factor reflecting
fathers’ birth satisfaction. Johansson et al.
(2012) reported several themes related to this
including support by midwives, information
received, treatment of father with respect and
empathy and to be involved.

Mother in control and managing pain, the
third theme to emerge from the data. This was
similar for the participants in the Premberg
et al. (2011) study. When fathers perceived that
the mother felt in control of her process and that
she was managing her pain effectively, he felt
comforted. For the father, seeing the mother in
pain was difficult and made worse when she
was perceived as being overwhelmed and dis-
tressed. In their recent meta-analysis, Johansson
et al. (2015) found that men particularly strug-
gled with the pain of labour. Deave and Johnson

(2008) reported that the father often felt
excluded and helpless when the mother was
focused internally. Poor management of pain
led to lower satisfaction. This sense of satisfac-
tion was increased when the father felt that he
played a positive support role which encour-
aged and valued her efforts. As Chapman (2000)
also found, those fathers who struggled and
whose partners were given epidurals felt relief
which contributed towards their sense of birth
satisfaction.

Care and communication after birth was a
major area of satisfaction for fathers. Typical of
findings in other studies, fathers appreciated
being informed that progress was normal
(Hildingsson et al., 2011; Johansson et al.,
2012). When complications arose and interven-
tions were required to ensure the safety of
mother and baby, fathers became anxious and
worried. Medical personnel who kept the par-
ents fully informed and welcomed their input
when decisions had to be made helped with
anxiety and adaptation to changes, a finding
consistent with other research (Howarth et al.,
2012; Johansson et al., 2012, 2015).

Fathers wanted to be able to see their new
baby and hold their new baby as soon as possi-
ble. Delays because of complications were dis-
tressing and again impacted negatively on the
satisfaction they felt with the whole process.
Fathers also wanted to be a part of the bonding
process between parents and child. When hos-
pital accommodation resources were inade-
quate, so that they were forced to leave the
mother and their baby before the family felt
ready to part, distress was experienced by the
fathers.

Taken together, these data suggest possible
improvement to the maternity system which
would help fathers feel greater satisfaction.
Preparation is seen as a key part of experiencing
birth satisfaction (Howarth et al., 2011b), per-
haps more attention could be given in antenatal
classes to the role of the father in delivery.
Green (1999) suggests that preparation is a key
area of concern for fathers who felt helpless
when they did not know what they could do to
assist their partners during labour and birth.

Howarth et al. 939

Limitations

Qualitative studies are exploratory with a number
of known weaknesses including researcher bias,
lack of generalisability and response bias. This
study was limited to first-time fathers. Fathers
who are having subsequent children may have
different perspectives of the birth experience.
There was little representation from socio-eco-
nomically deprived groups in this study which
would add a different perspective. Redshaw and
Henderson (2013) reported a considerable socio-
demographic variation in partner support in a
large UK study. The New Zealand childbirth
environment may be unique in a number of ways:
there is a high level of immigration, a midwife-
led system and free maternity services. Each of
these factors may have a unique contribution to
opinions held by this group of first-time fathers.

Conclusion

In common with other Western countries, more
and more fathers are becoming an integral part of
the childbirth process in New Zealand. How they
experience the pregnancy and birth of their child
may impact their psychological well-being
(Fenwick et al., 2012; Friedewald, 2007;
Longworth and Kingdon, 2011). Fathers in this
study report high levels of childbirth satisfaction,
despite reporting some concerns. Issues identi-
fied as relevant to fathers experience need to be
prioritised in birthing care. This article suggests
that many of these issues are about care and
safety of mothers but also a strong need to be
involved and included as participants in this pro-
cess along with the birthing mothers. The find-
ings in this study give a deeper understanding of
the father’s experience of childbirth.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of inter-
est with respect to the research, authorship, and/or
publication of this article.

Funding

The author(s) disclosed receipt of the following
financial support for the research, authorship, and/or
publication of this article: Preparation of this article

received the support of the Graduate Research
Committee, by means of the University of Otago
Postgraduate Publishing Bursary (doctoral).

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42 | wileyonlinelibrary.com/journal/birt Birth. 2019;46:42–50.© 2018 Wiley Periodicals, Inc.

1 | I N T R O D U C T I O N
The childbirth experience (especially of the first birth) rep-
resents an enduring milestone in a childbearing woman’s
development as a mother,1-4 and has implications for her psy-
chological health,5-7 bonding with her newborn,7 and plans to
have subsequent children.7 Women who deliver by cesarean

report substantially less positive childbirth experience,8,9
with less positive memories about the delivery enduring for
years afterward.10,11

In recent years, there has been increasing recognition
of the importance of the first few minutes after delivery as
a window of opportunity to promote maternal- newborn
bonding, successful breastfeeding, and a positive childbirth

Received: 23 April 2018 | Revised: 21 June 2018 | Accepted: 21 June 2018
DOI: 10.1111/birt.12378

O R I G I N A L A R T I C L E

Early maternal- newborn contact and positive birth experience

Laura H. Brubaker RN, MD, MPH1 | Ian M. Paul MD, MSc2 | John T. Repke MD1 |
Kristen H. Kjerulff MA, PhD3

1Department of Obstetrics and
Gynecology, Penn State Health, Milton
S. Hershey Medical Center, Hershey, PA
2Department of Pediatrics, Penn State
Health, Milton S. Hershey Medical Center,
Hershey, PA
3Departments of Public Health Sciences
and Obstetrics and Gynecology, College of
Medicine, Penn State University, Hershey,
PA

Correspondence: Kristen H. Kjerulff,
Department of Public Health Sciences,
A210, Penn State University College of
Medicine, 90 Hope Drive, Hershey, PA
(khk2@psu.edu; kkjerulf@phs.psu.edu).

Funding information
Supported by the Eunice Kennedy Shriver
National Institute of Child Health and
Human Development, National Institutes of
Health, Grant R01- HD052990

Abstract
Background: In recent years, there has been increasing recognition of the impor-
tance of early maternal- newborn contact for the health and well- being of the new-
born and promotion of breastfeeding. However, little research has investigated the
association between early maternal- newborn contact and the mother’s birth
experience.
Methods: As part of a large- scale prospective, cohort study (the First Baby Study
[FBS]), nearly 3000 women who delivered in Pennsylvania (2009- 2011) reported
how soon after delivery they first saw, held, and fed their newborns. Birth experience
was measured via telephone interview 1 month postpartum, using the FBS Birth
Experience Scale, a 16- item scale which addresses women’s feelings about the deliv-
ery. General linear models were used to measure associations between time to first
maternal- newborn contact and birth experience, controlling for relevant confound-
ers, including maternal age, race/ethnicity, insurance coverage, delivery mode, ges-
tational age, and pregnancy and delivery complications.
Results: The sooner that new mothers first saw, held, and fed their newborns after
delivery the more positive their childbirth experiences (all P- values < 0.001). Women who delivered by cesarean were less likely to see, hold and feed their new- borns shortly after delivery than those who delivered vaginally (all P- values < 0.001), and reported less positive birth experiences (P < 0.001). However, if they first saw, held, and fed their newborns shortly after delivery, they reported more positive birth experiences than those who delivered vaginally (P = 0.010). Discussion: Early maternal- newborn contact after delivery was associated with posi- tive birth experiences for new mothers, particularly those who delivered by cesarean.

K E Y W O R D S
cesarean delivery, childbirth experience, maternal-newborn contact

http://orcid.org/0000-0002-5376-2581

mailto:khk2@psu.edu

mailto:kkjerulf@phs.psu.edu

| 43BRUBAKER Et Al.
experience for the mother and her family.12-14 First maternal-
newborn interactions, such as seeing, holding, and feeding
the newborn, are part of the complex and not yet fully under-
stood psychobiological process of maternal- newborn bond-
ing.13-16 Recent research has documented the positive effects
of early maternal- newborn contact on the newborn’s thermo-
regulation, stress reactivity, and autonomic functioning.17,18
However, hospitals have postdelivery routines in place that
may involve immediate or early separation of the mother and
newborn to assess the newborn and care for the mother.12
In addition, there is a variety of circumstances in which the
newborn or mother may require post- delivery medical care
that precludes immediate or early maternal- newborn contact.
In the case of cesarean delivery, the focus is generally on the
postincision care of the mother and there may be little or no
opportunity for the mother to see, hold, or feed her newborn
for several hours after the delivery.19

Although there is growing evidence of the value of imme-
diate or early maternal- newborn contact, particularly within
the first hour after delivery,19,20 we found little research
which quantified time to first maternal- newborn contact or
investigated factors associated with how soon after deliv-
ery new mothers first see, hold, and feed their newborns in
United States hospitals. In addition, we found little research
measuring variation in time to first maternal- newborn con-
tact in relation to maternal birth experience. While it is well-
documented that women who deliver by cesarean report a
more negative birth experience than those who deliver vag-
inally,7-9 it is not clear how time to first maternal- newborn
contact plays a role in this association between mode of de-
livery and birth experience, if at all.

As part of a large- scale prospective, cohort study of first
childbirth, we asked new mothers how soon after delivery
they first saw, held, and fed their newborns. This provided
a unique opportunity to investigate associations between
demographic and clinical factors and time- intervals before
first maternal- newborn contact, and the effects of these time-
intervals on maternal experience of childbirth, controlling for
confounding variables.

2 | M E T H O D S

2.1 | Design and participants
This was a planned secondary analysis of data from the First
Baby Study (FBS).21 The FBS was a prospective cohort
study designed to investigate the association between mode
of delivery at first childbirth and subsequent childbearing.
Women were recruited from a variety of settings, including
childbirth education classes, low- income clinics, targeted
mailings, local magazine ads, and postings at participating
hospitals. Interviews were conducted by telephone. Women

met inclusion criteria if they were English- or Spanish-
speaking, nulliparous, aged 18- 35 years old, expecting a sin-
gleton, and planning to deliver at a hospital in Pennsylvania.
Women were excluded if they had had a prior pregnancy of
20 weeks’ gestation or longer, were a surrogate, were plan-
ning for adoption, or were planning to deliver outside the
hospital. Participants delivered between 34 and 42 weeks’
gestation. Deliveries occurred between January 2009 and
April 2011 in 76 hospitals across Pennsylvania. The baseline
and 1- month postpartum interviews were completed by 3006
women. This study was approved by the Penn State College
of Medicine Institutional Review Board and all participants
provided written informed consent. Statistical analyses were
conducted using the statistical software package SPSS 25
(SPSS Inc., Chicago, IL, USA).

2.2 | Measures
The outcome of interest for this analysis was maternal birth
experience, measured by a 16- item instrument administered
at the 1- month postpartum telephone interview, the FBS Birth
Experience Scale. This scale was developed by the FBS inves-
tigators based on qualitative interviews of new mothers, and
pilot- tested before use. Respondents were asked “Thinking
back to right after you had your baby (or if unconscious, after
you woke up), please tell me how you felt, using the follow-
ing scale—extremely, quite a bit, moderately, a little bit and
not at all.” The interviewer asked about 16 feelings. These
feelings were “exhausted,” “on cloud nine,” “disappointed,”
“in pain,” “sick,” “delighted,” “upset,” “excited,” “worried,”
“calm,” “like a failure,” “thankful,” “traumatized,” “sad,”
“angry,” and “proud of myself.” Items that measured positive
feelings were reverse scored. Total scores on this instrument
could range from 16 (very negative birth experience) to 80
(very positive birth experience). The overall Cronbach’s α
was 0.74 and the instrument exhibited strong construct valid-
ity as a measure of childbirth experience, as can be seen in
several previous publications.7,22

As part of the 1- month postpartum interview, the new
mothers were asked: “Thinking about when your baby was
born, how soon after delivery were you able to see your baby
for the first time?,” “…hold your baby for the first time?,”
and “…feed your baby for the first time?” These questions
were developed by one of the authors (IP), with the goal of
comparing time to first maternal- newborn contact by mode
of delivery. In response to these questions, participants an-
swered either “right away” or reported the time from de-
livery to first maternal- newborn contact. These variables
were categorized because the distributions were highly kur-
totic (76.2% reported that they first saw their newborn right
away, for example), highly skewed to the right (some women
were not able to first hold their newborn for weeks after de-
livery, for example), and the majority of women answered

44 | BRUBAKER Et Al.
these questions in terms of common time intervals, such as
“10 minutes,” “30 minutes,” or “1 hour,” which created a
multimodal distribution. For each time- interval variable, we
began with 9- 10 categories and combined categories to arrive
at three categories per variable that were significantly differ-
ent from each other in terms of mean birth experience scores.
For the variable of time to first see the newborn, the three
categories were as follows: right away, 1- 30 minutes after
delivery, and >30 minutes after delivery. For the variable of
time to first hold the newborn the categories were 5 minutes
or less, >5- 30 minutes, and >30 minutes. For the variable of
time to first feed the newborn, the categories were 30 minutes
or less, >30 minutes- 2 hours, and >2 hours.

In order to identify variation across the three time- interval
variables taken together, we created a summated scale of
time to first maternal- newborn contact (the Combined Time-
interval Scale), by summing women’s scores on each of the
time- interval variables, each scored 1- 3. Therefore, scores
on this scale ranged from 3 (1 point assigned if the mother
saw her newborn right away, 1 point if she held her new-
born in 5 minutes or less, and 1 point if she fed her newborn
in 30 minutes or less) to 9 (3 points assigned if the mother
did not see her newborn until more than 30 minutes after de-
livery, 3 points if she did not hold her newborn until more
than 30 minutes after delivery, and 3 points if she did not
feed her newborn until more than 2 hours after delivery).
Reliability analyses indicated that these three items worked
well together. The corrected item- total correlations ranged
from 0.46 to 0.59 and the overall Cronbach’s α was 0.69 (ap-
propriate for a 3- item scale).

We used the hospital discharge data linked to the birth
certificate data to develop four dichotomous composite
measures of childbirth morbidity, including high- risk de-
liveries, fetal congenital conditions, maternal morbidities,
and newborn morbidities, based on the childbirth compos-
ite morbidity indicators described in Korst et al,23 using
the International Classification of Diseases 9th Revision,
Clinical Modification (ICD- CM) diagnostic and procedure
codes specified in tables S1- S3 of Korst et al.23 We also
counted a condition as present if it was reported in the birth
certificate data. We developed these composite childbirth
morbidity indicators so that we could measure and control
for pregnancy and childbirth complications that would likely
be associated with how quickly the mother would be able to
first see, hold, and feed her newborn, as well as her feelings
about the childbirth.

2.3 | Statistical analyses
The analyses addressed the following four questions:

1. What demographic and clinical factors were associated
with the time to first maternal-newborn contact?

2. How did the mode of delivery affect the time to first ma-
ternal-newborn contact?

3. How did time to first maternal-newborn contact affect the
association between mode of delivery and maternal birth
experience?, and

4. How did time to first maternal-newborn contact affect ma-
ternal childbirth experience, independent of mode of
delivery?

The associations between the time- interval variables (time
from delivery to first seeing, holding, and feeding the newborn)
and demographic and clinical factors were measured using
Pearson’s χ2 tests. Adjusted odd ratios (aORs) and 95% confi-
dence intervals (CIs) were derived from three multivariable lo-
gistic regression models (with all confounding variables in each
model) to measure the associations between the demographic
and clinical factors and each of the three primary time- interval
variables. For these analyses, the time- interval categories were
dichotomized to compare women who interacted with their
newborns in the shortest time categories within each time-
interval variable (saw newborn right away, held newborn in
5 minutes or less, and fed newborn in 30 minutes or less) to
those who did not.

Sequential general linear models were used to investigate
the effect of each of the time- interval variables on the asso-
ciation between mode of delivery and maternal birth experi-
ence. In the first model, we controlled for the confounding
variables, but did not include any of the time- interval vari-
ables. In the second model, we controlled for the “time to
first see the newborn” variable and the confounding vari-
ables. In the third model, we controlled for the “time to first
hold the newborn” variable and the confounding variables. In
the fourth model, we controlled for the “time to first feed the
newborn” variable and the confounding variables. In the fifth
model, we controlled for the Combined Time- interval Scale
variable and the confounding variables. We carried out an
additional analysis to compare mean FBS Birth Experience
scores for the women who delivered vaginally to those who
delivered by cesarean, among those with a Combined Time-
interval Scale score of 3, via linear regression, controlling for
the confounding variables.

Finally, general linear models were used to measure the
association between each of the time- interval variables and
maternal childbirth experience, controlling for the covari-
ates, including mode of delivery. For these analyses, there
were four models, one for each of the primary time- interval
variables (time to see, hold, and feed the newborn), and
the Combined Time- interval Scale. For the model with the
Combined Time- interval Scale, we conducted a priori con-
trasts to compare the adjusted means of those with a score of
3 to those with scores of 4, 5, 6, 7, 8, and 9, to compare ma-
ternal birth experience among the women with the shortest
time- intervals for all three of the maternal- newborn contact

| 45BRUBAKER Et Al.

domains (those with a combined time- interval score of 3) to
those with longer time- intervals.

In the general linear models described above, any one of the
time- interval variables was included in only one model at a time
because these variables were highly collinear, as one would ex-
pect. It would be difficult to hold the newborn without seeing
the newborn, for example. Because the adjusted mean birth ex-
perience scores resulting from the general linear models were
very similar to the unadjusted mean birth experience scores, we
show the unadjusted mean birth experience scores only.

3 | R E S U LT S
The study participants were predominantly white/non-
Hispanic (83.2%), and covered by private insurance (77.0%),
as seen in Table 1. There were 155 women (5.2%) who had
a planned cesarean delivery before the onset of labor and
an additional 708 (23.6%) who had an unplanned cesarean.
Based on the childbirth morbidity measures,23 44.8% was
classified as high- risk deliveries, 6.3% involved fetal con-
genital conditions, 27.2% involved maternal morbidities, and
13.2% involved neonatal morbidities. The majority of the
women were able to see their newborn right away (76.2%),

Characteristic No. (%)

Combined Time- interval Scale

3e 879 (30.0)

4 649 (22.1)

5 501 (17.1)

6 308 (10.5)

7 309 (10.5)

8 150 (5.1)

9f 136 (4.6)

FBS Birth Experience Scale, mean ± SD 68.65 ± 6.39

Missing data: Race/ethnicity (n = 1); Insurance (n = 2); Fetal congenital condi-
tions (n = 13); Time before mother first saw newborn after delivery (n = 10);
Time before mother first held newborn after delivery (n = 23); Time before
mother first fed newborn after delivery (n = 60); Combined Time- interval Scale
(n = 77); FBS Birth Experience Scale (n = 33).
aWomen were classified as having a high- risk delivery if they had one or more of
23 pregnancy complications listed in table S1 of Korst et al23 such as antepartum
bleeding, diabetes, hypertension, and malpresentation, as indicated by ICD- 9- CM
codes in the hospital discharge data or reported in the birth certificate data.
bNewborns were classified as having fetal congenital conditions if they had one or
more of 29 fetal congenital anomalies or adrenogenital disorders listed in table S1
of Korst et al,23 such as cardiac congenital anomalies, urinary tract congenital
anomalies, and hemolytic disease, as indicated by ICD- 9- CM codes in the hospi-
tal discharge data or reported in the birth certificate data.
cWomen were classified as having maternal morbidities if they had one or more
of 50 delivery- related complications listed in table S2 of Korst et al,23 such as 3rd
or 4th degree perineal laceration, cardiac arrest, and postpartum hemorrhage, as
indicated by ICD- 9- CM codes in the hospital discharge data or reported in the
birth certificate data.
dNewborns were classified as having neonatal morbidities if they had one or more
of 61 complications listed in table S3 of Korst et al,23 such as clavical fracture,
meconium aspiration, respiratory distress syndrome, and transient tachypnea, as
indicated by ICD- 9- CM codes in the hospital discharge data or reported in the
birth certificate data.
eA score of 3 on the Combined Time- interval Scale indicates that the new mother
first saw her newborn right away after delivery and held her newborn in 5 minutes
or less after delivery, and fed her newborn in 30 minutes or less after delivery.
fA score of 9 on the Combined Time- interval Scale indicates that the new mother
first saw her newborn more than 30 minutes after delivery and held her newborn
more than 30 minutes after delivery and fed her newborn more than 2 hours after
delivery.

T A B L E 1 (Continued)T A B L E 1 Characteristics of the study population (N = 3006),
First Baby Study, Pennsylvania, USA, 2009- 2011

Characteristic No. (%)

Maternal age at delivery, y

18- 24 811 (27.0)

25- 29 1193 (39.7)

30- 36 1002 (33.3)

Race/ethnicity

White, non- Hispanic 2502 (83.2)

Black, non- Hispanic 221 (7.4)

Hispanic 166 (5.5)

Other 116 (3.9)

Private insurance 2312 (77.0)

Mode of delivery

Spontaneous vaginal 1882 (62.6)

Instrumental vaginal 261 (8.7)

Planned cesarean 155 (5.2)

Unplanned cesarean 708 (23.6)

Late preterm (34 wk, 0 d to 36 wk, 6 d) 120 (4.0)

High- risk deliverya 1346 (44.8)

Fetal congenital conditionsb 190 (6.3)

Maternal morbiditiesc 818 (27.2)

Neonatal morbiditiesd 397 (13.2)

Midwife or doula attended birth 910 (30.3)

Time before mother first saw newborn after delivery

Right away 2283 (76.2)

1- 30 min 482 (16.1)

>30 min 231 (7.7)

Time before mother first held newborn after delivery

5 minutes or less 1684 (56.5)

>5- 30 min 557 (18.7)

>30 min 742 (24.9)

Time before mother first fed newborn after delivery

30 minutes or less 1191 (40.4)

>30 min- 2 h 1011 (34.3)

>2 h 744 (25.3)

(Continues)

46 | BRUBAKER Et Al.

about half reported holding their newborn in 5 minutes or
less after delivery (56.5%), and less than half reported feed-
ing their newborn in 30 minutes or less (40.4%). Overall,
30% had a Combined Time- interval Scale score of 3, indi-
cating that they were able to see their newborn right away
and hold their newborn in 5 minutes or less and feed their
newborn in 30 minutes or less.

In the unadjusted χ2 analyses, white non- Hispanic women
were more likely to report that they saw their newborn right

away in comparison to minority women, as were women with
private insurance in comparison to women with public in-
surance (Table 2). Less than half of the women who had an
unplanned cesarean delivery (47.9%) saw their newborn right
away, 7.8% held their newborn in 5 minutes or less and 12.0%
fed their newborn in 30 minutes or less. In contrast, 87.6% of
the women who had a spontaneous vaginal delivery saw their
newborn right away, 76.5% held their newborn in 5 minutes or
less, and 52.2% fed their newborn in 30 minutes or less (all 3

T A B L E 2 Unadjusted bivariate analyses of demographic and clinical factors by time- interval before mothers first saw, held, and fed their
newborns after delivery, First Baby Study, Pennsylvania, USA, 2009- 2011

Factors
Mother saw newborn right
away, no. (%)

Mother held newborn in 5 min
or less, no. (%)

Mother fed newborn in
30 min or less, no. (%)

Maternal age at delivery, y

18- 24 598 (74.0) 471 (58.4)* 328 (41.3)

25- 29 932 (78.3) 691 (58.4) 473 (40.6)

30- 36 753 (75.5) 522 (52.6) 390 (39.6)

Race/ethnicity

White, non- Hispanic 1919 (77.0)* 1418 (57.1) 977 (39.8)

Non- white 368 (72.2) 265 (53.2) 214 (43.9)

Insurance

Private 1793 (77.9)*** 1303 (56.7) 932 (41.0)

Public 488 (70.6) 381 (55.7) 259 (38.5)

Mode of delivery

Spontaneous vaginal 1648 (87.6)*** 1436 (76.5)*** 966 (52.2)***

Instrumental vaginal 213 (81.6) 181 (69.6) 113 (43.8)

Planned cesarean 87 (56.1) 13 (8.4) 30 (19.7)

Unplanned cesarean 335 (47.9) 54 (7.8) 82 (12.0)

Late preterm (34 wk, 0 d to 36 wk, 6 d)

Yes 82 (68.3) 55 (46.6)* 30 (25.6)***

No 2201 (76.5) 1629 (56.9) 1161 (41.0)

High- risk delivery

Yes 927 (69.2)*** 590 (44.4)*** 440 (33.5)***

No 1356 (81.9) 1094 (66.1) 751 (46.0)

Fetal congenital conditions

Yes 135 (71.1) 107 (56.9) 67 (35.6)

No 2139 (76.6) 1572 (56.5) 1120 (40.8)

Maternal morbidities

Yes 613 (75.0) 439 (54.1) 289 (36.0)**

No 1670 (76.6) 1245 (57.3) 902 (42.1)

Neonatal morbidities

Yes 240 (60.9)*** 143 (36.6)*** 79 (20.4)***

No 2043 (78.5) 1541 (59.5) 1112 (43.5)

Midwife or doula attended birth

Yes 729 (80.6)*** 582 (64.3)* 392 (43.9)*

No 1554 (74.3) 1102 (53.0) 799 (38.9)

Row percents are shown in this table.
*P < 0.05, **P < 0.01, ***P < 0.001, based on chi- square analyses.

| 47BRUBAKER Et Al.

P- values < 0.001). Women with high- risk deliveries were less likely to see their newborns right away, hold them in 5 minutes or less, and feed them in 30 minutes or less than women who did not have high- risk deliveries (all 3 P- values < 0.001). If there were neonatal morbidities, the mothers were also less likely to see their newborn right away, hold them in 5 minutes or less, and feed them in 30 minutes or less (all 3 P- values < 0.001).

After adjustment for the confounding variables (Table 3), the
women who had spontaneous vaginal delivery had considerably
increased odds of being able to see their newborn right away
(aOR 7.77, 95% CI 6.26- 9.64), hold their newborn in 5 min-
utes or less (aOR 40.31, 95% CI 29.58- 54.92), and feed their
newborn in 30 minutes or less (aOR 8.17, 95% CI 6.32- 10.56),
in comparison to those who delivered by unplanned cesarean.
The women with high- risk deliveries were not significantly less
likely to see their newborn right away or feed their newborn in
30 minutes or less, but were less likely to hold their newborn
in 5 minutes or less in comparison to those who did not have
high- risk deliveries. Fetal congenital conditions were not signifi-
cantly associated with any of the three time- interval measures.
However, when there were neonatal morbidities, the mothers
were significantly less likely to see their newborn right away,
hold their newborn in 5 minutes or less and feed their newborn

in 30 minutes or less. Women whose labor team included a mid-
wife or doula were more likely to see their newborn right away
and hold their newborn in 5 minutes or less than women who did
not have the support of a midwife or doula.

Overall, women who delivered vaginally reported a more
positive childbirth experience than those who delivered by ce-
sarean, controlling for the confounding variables but not the
time to first maternal- newborn contact variables (P < 0.001; Table 4). With the “time to first see the newborn” variable in the equation (the second model), mode of delivery remained significant. In the third model, with the variable of “time to first hold the newborn” in the equation, mode of delivery was borderline significant. In the fourth model, with the “time to first feed the newborn” in the equation, mode of delivery was significant. In the fifth model, with the Combined Time- interval Scale in the equation, mode of delivery was no lon- ger significant (P = 0.829). Although very few of the women who delivered by cesarean had a Combined Time- interval Scale score of 3 (n = 19), the mean FBS Birth Experience score for these women was 72.84, which was significantly higher (P = 0.010) than the mean birth experience score for the 848 women who also had a Combined Time- interval Scale score of 3, but had delivered vaginally, which was 70.17.

T A B L E 3 Multivariable logistic regression analyses of demographic and clinical factors by time intervals before mothers first saw, held and
fed their newborns, controlling for confounders, First Baby Study, Pennsylvania, USA, 2009- 2011

Factor

Mother saw newborn right
away

Mother held newborn in 5 min
or less

Mother fed newborn in
30 min or less

Adjusted OR (95% CI) Adjusted OR (95% CI) Adjusted OR (95% CI)

Maternal age at delivery, y

18- 24 Reference Reference Reference

25- 29 1.27 (0.96- 0.69) 1.22 (0.93- 1.60) 1.08 (0.86- 1.37)

30- 36 1.19 (0.88- 1.60) 1.09 (0.81- 1.47) 1.16 (0.90- 1.50)

White non- Hispanic 0.94 (0.72- 1.23) 1.01 (0.77- 1.34) 0.65 (0.51-0.83)

Private insurance 1.51 (1.15-2.00) 1.12 (0.85- 1.49) 1.26 (0.99-1.62)

Mode of delivery

Spontaneous vaginal 7.77 (6.26-9.64) 40.31 (29.58-54.92) 8.17 (6.32-10.56)

Instrumental vaginal 4.71 (3.29-6.74) 30.15 (20.19-45.02) 6.18 (4.36-8.76)

Planned cesarean 1.46 (1.01-2.11) 1.19 (0.63- 2.28) 1.71 (1.06-2.75)

Unplanned cesarean Reference Reference Reference

Not late preterm (gestational age of
37 wk or later)

1.29 (0.81- 2.04) 1.44 (0.90- 2.31) 1.88 (1.19-2.97)

Not high- risk delivery 1.18 (0.97- 1.44) 1.24 (1.02-1.51) 1.07 (0.90- 1.26)

No fetal congenital conditions 1.10 (0.76- 1.60) 0.68 (0.45- 1.02) 1.05 (0.74.- 1.47)

No maternal morbidities 1.15 (0.93- 1.42) 1.40 (1.14-1.73) 1.42 (1.18-1.70)

No neonatal morbidities 2.16 (1.6-2.79) 2.92 (2.23-3.83) 2.68 (2.04-3.54)

Midwife or doula attended birth 1.29 (1.04-1.60) 1.44 (1.17-1.78) 1.09 (0.91- 1.30)

Each of the three multivariable logistic regression models controls for maternal age, race, insurance coverage, mode of delivery, late preterm delivery, high- risk delivery,
fetal congenital conditions, maternal morbidities, neonatal morbidities, and the support of a midwife or doula during labor.
Bolding denotes statistical significance, P < 0.05.

48 | BRUBAKER Et Al.

Even after controlling for the confounding variables (in-
cluding mode of delivery), each of the time- interval variables
remained highly significantly associated with birth experi-
ence (Table 5). The new mothers with the highest birth ex-
perience scores were those with a Combined Time- interval
Scale score of 3, while those who had a Combined Time-
interval Scale score of 9 had the lowest birth experience
scores. In the a priori contrasts (controlling for the confound-
ing variables), the mean FBS Birth Experience Scale score of
the women with a Combined Time- interval Scale score of 3
was not significantly different from the mean birth experience

score of those with a Combined Time- interval Scale score
of 4 (P = 0.169), but it was significantly different from the
mean birth experience scores of those with Combined Time-
interval Scale scores of 5 (P < 0.01) and 6, 7, 8, and 9 (all 4 P- values < 0.001).

4 | D I S C U S S I O N
The results from this secondary analysis from the First Baby
Study demonstrated that the shorter the time- intervals before

T A B L E 4 General linear models of the association between mode of delivery and maternal satisfaction with the childbirth experience (FBS
Birth Experience Scale), controlling for each of the time- interval variables and the confounders, First Baby Study, Pennsylvania, USA, 2009- 2011

FBS Birth Experience Scale, Mean ± SD

F P- value

Mode of delivery

Vaginal Cesarean

Model 1: controlling for confounders, but not
time-interval variables

69.47 ± 5.79 66.64 ± 7.33 93.95 <0.001

Model 2: controlling for time to first see the newborn and confounders

Time before mother first saw newborn after delivery

Right away 69.69 ± 5.60 67.71 ± 6.88 27.36 <0.001

1- 30 min 68.16 ± 6.55 66.23 ± 7.35

>30 min 66.83 ± 7.63 64.64 ± 7.91

Model 3: controlling for time to first hold the newborn and confounders

Time before mother first held newborn after delivery

5 min or less 69.83 ± 5.46 69.55 ± 6.25 3.20 0.074

>5- 30 min 69.20 ± 5.75 68.00 ± 6.66

>30 min 66.24 ± 8.00 65.93 ± 7.48

Model 4: controlling for time to first feed the newborn and confounders

Time before mother first fed newborn after delivery

30 min or less 70.07 ± 5.30 68.54 ± 7.28 40.68 <0.001

>30 min- 2 h 69.62 ± 5.54 67.44 ± 6.53

>2 h 67.59 ± 6.99 65.32 ± 7.85

Model 5: controlling for Combined Time-interval Scale score and confounders

Combined Time- interval Scale

3a 70.17 ± 5.29 72.84 ± 5.27 0.046 0.829

4 69.72 ± 5.29 69.43 ± 5.35

5 69.54 ± 5.60 67.46 ± 7.12

6 67.57 ± 7.21 67.55 ± 6.42

7 66.26 ± 6.90 66.12 ± 7.70

8 64.68 ± 9.97 65.82 ± 7.25

9b 65.05 ± 8.35 63.81 ± 8.13

Means shown are unadjusted.
Each of the five general linear models controls for the confounders of maternal age, race, insurance coverage, late preterm delivery, high- risk delivery, fetal congenital
conditions, maternal morbidities, neonatal morbidities, and the support of a midwife or doula.
aA score of 3 on the Combined Time- interval Scale indicates that the new mother first saw her newborn right away after delivery, held her newborn in 5 minutes or less
after delivery, and fed her newborn in 30 minutes or less after delivery.
bA score of 9 on the Combined Time- interval Scale indicates that the new mother first saw her newborn more than 30 minutes after delivery, held her newborn more than
30 minutes after delivery, and fed her newborn more than 2 hours after delivery.

| 49BRUBAKER Et Al.

first maternal- newborn contact (seeing, holding, and feeding
the newborn) the more positive the childbirth experience was
for new mothers. In fact, the women who delivered by ce-
sarean, but nonetheless were able to see their newborns right
away and hold them in 5 minutes or less and feed them in
30 minutes or less, had significantly more positive birth expe-
riences than those who reported the same time- intervals before
first maternal- newborn contact but delivered vaginally. These
results are important because many studies have reported that

women who deliver by cesarean report a less positive birth
experience than those who deliver vaginally,11,22 as we also
found in this study. Short time- intervals before first maternal-
newborn contact go a long way toward making the childbirth
experience positive for new mothers, even those who are de-
livered by cesarean.

Our results are consistent with other studies that reported
that women who have a vaginal birth are usually able to hold
and feed their newborn sooner than women with cesarean de-
livery.24,25 This longer length of time before first maternal-
newborn contact among women who deliver by cesarean in
comparison to vaginally appears to have persisted for de-
cades,26 despite strides toward facilitation of early contact,
such as routine use of spinal anesthesia for cesarean delivery
(as opposed to general anesthesia). Nonetheless, we were sur-
prised to find that more than half of the new mothers who
delivered by unplanned cesarean (52.1%) reported that they
did not see their newborns right away.

4.1 | Strengths and limitations
There are several limitations to this secondary data analy-
sis. First, the participants in the First Baby Study were
more likely to be married, have college degrees, and be
covered by private insurance than the background pop-
ulation of women at first childbirth in Pennsylvania.21
In addition, this study was of first- time mothers only.
These factors limit the generalizability of our findings.
Additionally, this analysis relied on maternal report of
time to first maternal- newborn contact, which is subject
to recall bias. Some women would likely not have remem-
bered accurately how soon they were first able to see,
hold, and feed their newborns. Women’s reports of the
times before they first saw, held, and fed their newborns
were categorized into relatively broad time- intervals so
that we could measure, in a general sense, the association
between time to first maternal- newborn contact and birth
experience. However, such broad time- intervals might be
of limited utility for clinical purposes. Another limitation
of this report is that we did not ask about skin- to- skin con-
tact between the mother and her newborn. We do not know
how often immediate or early holding of the newborns in
this study involved skin- to- skin contact, or how that fac-
tor affected maternal childbirth experience. Finally, these
deliveries occurred in the years 2009 to 2011. We do not
know to what extent the delivery process has changed in
United States hospitals since that time period.

This report also has several strengths. The large sample
size allowed us to identify relatively uncommon subgroups
of women (such as those who delivered by cesarean but
nonetheless saw their newborn right away and held their
newborn in 5 minutes or less and fed their newborn in
30 minutes or less) that would not have been possible with

T A B L E 5 General linear models of the association between each
of the time- interval variables and maternal satisfaction with the
childbirth experience (FBS Birth Experience Scale), controlling for
mode of delivery and the other confounders, First Baby Study,
Pennsylvania, USA, 2009- 2011

FBS Birth Experience
Scale, Mean ± SD F P- value

Model 1

Time before mother first saw newborn after delivery

Right away 69.33 ± 5.90 21.55 <0.001

1- 30 min 67.12 ± 7.05

>30 min 65.18 ± 7.88

Model 2

Time before mother first held newborn after delivery

5 min or less 69.82 ± 5.49 26.23 <0.001

>5- 30 min 68.80 ± 6.09

>30 min 65.99 ± 7.58

Model 3

Time before mother first fed newborn after delivery

30 min or less 69.93 ± 5.53 26.54 <0.001

>30 min- 2 h 68.86 ± 5.99

>2 h 66.46 ± 7.51

Model 4

Combined Time- interval Scale

3a 70.24 ± 5.30 16.08 <0.001

4 69.60 ± 5.29

5 69.10 ± 6.01

6 67.56 ± 6.75

7 66.16 ± 7.48

8 65.62 ± 7.77

9b 64.01 ± 8.15

Means shown are unadjusted.
Each of the four general linear models controls for maternal age, race, insurance
coverage, mode of delivery, late preterm delivery, high- risk delivery, fetal con-
genital conditions, maternal morbidities, neonatal morbidities, and the support of
a midwife or doula during labor.
aA score of 3 on the Combined Time- interval Scale indicates that the new mother
first saw her newborn right away after delivery, held her newborn in 5 minutes or
less after delivery and fed her newborn in 30 minutes or less after delivery.
bA score of 9 on the Combined Time- interval Scale indicates that the new mother first
saw her newborn more than 30 minutes after delivery, held her newborn more than
30 minutes after delivery, and fed her newborn more than 2 hours after delivery.

50 | BRUBAKER Et Al.
a smaller sample. In addition, we controlled for the ef-
fects of childbirth morbidities and complications. Studies
of factors associated with birth experience rarely control
for childbirth complications, in part because they are
often small sample, qualitative studies.8 However, in this
analysis, it was particularly important that we control for
childbirth morbidities and complications because these
factors would reasonably be expected to affect how soon
new mothers could interact with their newborns. In this
analysis, we found that in the event of neonatal morbidi-
ties, the mothers were significantly less likely to see, hold,
and feed their newborns in the earliest time intervals after
delivery.

4.2 | Conclusion
In summary, the results of this analysis demonstrate that

the time before first maternal- newborn contact after deliv-
ery matters to new mothers, and the shorter the times before
new mothers first see, hold, and feed their newborns the
more positive they feel about the childbirth in retrospect.

O RC I D

Kristen H. Kjerulff http://orcid.
org/0000-0002-5376-2581

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How to cite this article: Brubaker LH, Paul IM,
Repke JT, Kjerulff KH. Early maternal- newborn
contact and positive birth experience. Birth.
2019;46:42–50. https://doi.org/10.1111/birt.12378

http://orcid.org/0000-0002-5376-2581

http://orcid.org/0000-0002-5376-2581

http://orcid.org/0000-0002-5376-2581

https://doi.org/10.1111/birt.12378

Developmental Science. 2019;00:e12892. wileyonlinelibrary.com/journal/desc  |  1 of 13
https://doi.org/10.1111/desc.12892

© 2019 John Wiley & Sons Ltd

1   |   I N T R O D U C T I O N

Imitation plays a critical role in human social learning and cultural

traditions (see, e.g. Boyd & Richerson, 1996; Henrich & McElreath,
2003; Legare & Nielsen, 2015; Tomasello, Kruger, & Ratner, 1993),
and so charting its ontogeny is of great importance to integrative
theories of social cognitive development. An innate propensity to
imitate from birth would suggest that human brains are pre‐wired

with a solution to the “correspondence problem” of coordinating
one’s own and others’ actions (Brass & Heyes, 2005). Most remark‐
ably, it would suggest that we are born with a capacity to link our
own felt but unseen facial actions with the seen but unfelt facial ac‐
tions of others. Alternatively, if newborns do not imitate, then it
would appear that we instead acquire the capacity during infancy
(Piaget, 1962), perhaps as a function of both innate and environmen‐
tal factors (see, e.g. Bjorklund, 2018; Byrne, 2003; Heyes, 2016a;

Received: 11 February 2019  | Revised: 20 May 2019  | Accepted: 23 July 2019
DOI: 10.1111/desc.12892

P A P E R

Individual differences in neonatal “imitation” fail to predict
early social cognitive behaviour

Jonathan Redshaw1  | Mark Nielsen1,2  | Virginia Slaughter1  | Siobhan Kennedy‐
Costantini1,3  | Janine Oostenbroek1 | Jessica Crimston1  | Thomas Suddendorf

1

1School of Psychology, University of
Queensland, Brisbane, Australia
2Faculty of Humanities, University of
Johannesburg, Johannesburg, South Africa
3School of Psychology, University of
Auckland, Auckland, New Zealand

Correspondence
Jonathan Redshaw, School of Psychology,
University of Queensland, Brisbane,
Australia.
Email: j.redshaw@uq.edu.au

Funding information
Australian Research Council, Grant/
Award Number: DP0985969; University
of Queensland, Grant/Award Number:
UQFEL1832633

Abstract
The influential hypothesis that humans imitate from birth – and that this capacity is
foundational to social cognition – is currently being challenged from several angles.
Most prominently, the largest and most comprehensive longitudinal study of neona‐
tal imitation to date failed to find evidence that neonates copied any of nine actions
at any of four time points (Oostenbroek et al., [2016] Current Biology, 26, 1334–1338).
The authors of an alternative and statistically liberal post‐hoc analysis of these same
data (Meltzoff et al., [2017] Developmental Science, 21, e12609), however, concluded
that the infants actually did imitate one of the nine actions: tongue protrusion. In
line with the original intentions of this longitudinal study, we here report on whether
individual differences in neonatal “imitation” predict later‐developing social cogni‐
tive behaviours. We measured a variety of social cognitive behaviours in a subset
of the original sample of infants (N = 71) during the first 18 months: object‐directed
imitation, joint attention, synchronous imitation and mirror self‐recognition. Results
show that, even using the liberal operationalization, individual scores for neonatal
“imitation” of tongue protrusion failed to predict any of the later‐developing social
cognitive behaviours. The average Spearman correlation was close to zero, mean
rs = 0.027, 95% CI [−0.020, 0.075], with all Bonferroni adjusted p values > .999. These
results run counter to Meltzoff et al.’s rebuttal, and to the existence of a “like me”
mechanism in neonates that is foundational to human social cognition.

K E Y W O R D S

cognitive development, correspondence problem, like me framework, mirror neurons,
neonatal imitation, social cognition

www.wileyonlinelibrary.com/journal/desc

mailto:

https://orcid.org/0000-0002-7729-1577

https://orcid.org/0000-0002-0402-8372

https://orcid.org/0000-0001-9315-1497

https://orcid.org/0000-0002-6935-176

0

https://orcid.org/0000-0003-2093-601X

https://orcid.org/0000-0003-3328-7442

mailto:j.redshaw@uq.edu.au

2 of 13  |     REDSHAW Et Al.

Paulus, Hunnius, Vissers, & Bekkering, 2011; Ray & Heyes, 2011).
Mirror neurons have been proposed as a neural correlate of imitation
(Iacobini, 2009), but it remains controversial whether these neurons
play an innate and causal role in copying behaviour (Ferrari, Bonini,
& Fogassi, 2009; Simpson, Murray, Paukner, & Ferrari, 2014a) or
whether they are simply an artefact of postnatal associative learning
(Cook, Bird, Catmur, Press, & Heyes, 2014; Heyes, 2010).

Mid‐20th century theorists considered an innate solution to
the correspondence problem to be unlikely, instead suggesting
that the capacity for imitation is acquired late during the first year
of life (Piaget, 1962; Uzgiris & Hunt, 1975). The paradigm shifted,
however, following Meltzoff and Moore’s (1977) report of imitation
in infants under three weeks of age. This result was soon followed
by another influential finding of imitation in the initial days of life
(Field, Woodson, Greenberg, & Cohen, 1982), and it was thus gen‐
erally concluded that infants do indeed possess an innate solution
to the correspondence problem. The phenomenon of neonatal imi‐
tation has since been incorporated not only into leading theories of
cognitive development (Meltzoff, 2007; Nadel & Butterworth, 1999;
Trevarthen & Aitken, 2001), but also into theories of social psychol‐
ogy (Cheng & Chartrand, 2003; Lakin, Jefferis, Cheng, & Chartrand,
2003), comparative psychology (Iacobini, 2009; Simpson, Paukner,
Suomi, & Ferrari, 2014b) and neuroscience (Gallese, 2001; Meltzoff
& Decety, 2003).

The dominant theory of neonatal imitation’s function is the like me
framework (Meltzoff, 2005, 2007; Meltzoff & Brooks, 2001), which
suggests that an innate capacity for copying others is the “engine
and mechanism for the growth of social cognition” (Meltzoff, 2005,
pp.7). This framework interprets infants’ imitative acts in richer,
cognitive terms than alternative, behaviour‐based frameworks of
imitation (see Moore, 2013; Paulus, 2011). In particular, the like me
framework proposes that infants represent their own and others’
action sequences using the same supra‐modal mental code, allow‐
ing them to infer equivalences between their own and others’ inter‐
nal states, such as perceptions, intentions and emotions (Meltzoff,
2007). One implication of this framework, then, is that neonates who
are more proficient imitators might be expected to show earlier and
more robust social cognitive aptitudes than their peers who are less
proficient imitators (Heimann, 2002; Heimann, Nelson, & Schaller,
1989; Simpson, Murray, et al., 2014a; Suddendorf, Oostenbroek,
Nielsen, & Slaughter, 2013). In other words, if neonatal imitation pro‐
vides the bedrock for later emerging social cognitive abilities, then
individual differences in neonatal imitation should predict individual
differences in later‐developing forms of imitation and other social
cognitive behaviours (but see Bjorklund, 1987).

Heimann et al. (1989) were the first to test for such associations
in a short‐term longitudinal study. Imitation of tongue protrusion and
mouth opening was assessed in 32 infants at three time points − 2
to 3 days, 3 weeks and 3 months – with mixed results. Imitation ef‐
fects were only significant for tongue protrusion (at the first two
time points), and only when the definition of this behaviour was
broadened to include actions where “the tongue was not protruded
beyond the lips”. Furthermore, although there were some significant

correlations between tongue protrusion imitation scores across the
first two time points, these correlations were based on a separate,
very narrow definition of tongue protrusion, for which the infants
did not show significant evidence of imitation above chance levels.
The authors concluded that a more comprehensive longitudinal ap‐
proach was needed to provide “an answer to one of the most import‐
ant questions remaining: How [do] individual differences in neonatal
imitation relate to later imitation seen around 9–18 months of age?”
(Heimann et al., 1989, pp. 100). Despite this call to action coming
30 years ago, to date there exist no published longitudinal studies
assessing the relationship between neonatal imitation and later im‐
itative and other social cognitive capacities in humans. The founda‐
tional assumption of the like me framework has therefore not been
empirically established.

We originally set out to conduct just this kind of long anticipated
longitudinal investigation (Suddendorf et al., 2013). We measured
imitation of nine modelled social actions at four time points between
1 and 9 weeks of age, hoping to eventually examine whether individ‐
ual differences in neonatal imitation aligned with individual differ‐
ences in other social cognitive behaviours that we measured during
the early years of life. To our surprise, however, we did not find evi‐
dence of neonatal imitation in our initial measure at all—not for any
of the nine actions at any of the four time points (Oostenbroek et
al., 2016). We were compelled to conclude, therefore, that rather
than providing the foundation for a definitive study of neonatal im‐
itation’s function, our data instead challenged the very existence of
neonatal imitation itself. This unforeseen conclusion has since been
substantiated by several other works:

1. A comprehensive sensorimotor analysis suggesting that neonates
lack voluntary, cortical control over tongue protrusion, thus
making intentional imitation of this action implausible (Keven
& Akins, 2017);

Research Highlights
• A previous large‐scale longitudinal study reported no

evidence of neonatal imitation for any of nine actions at
any of four time points.

• A post hoc, statistically liberal re‐analysis of these
same data, however, suggested that the neonates may
have actually imitated one of the nine actions: tongue
protrusion.

• We tested for associations between this operationali‐
zation of tongue protrusion imitation and various later‐
developing social cognitive behaviours in the original
sample of infants.

• There were no significant correlations between neo‐
natal “imitation” scores and any later‐developing social
cognitive behaviours, controverting the dominant like
me framework of neonatal imitation’s function.

     |  3 of 13REDSHAW Et Al.

2. A study suggesting that previously blind, newly sighted children
show greatly impaired automatic imitation of manual actions,
meaning that this capacity is either not innate or vulnerable to
degradation in specific domains (McKyton, Ben‐Zion, & Zohary,
2018);

3. A study showing that mothers’ tendency to imitate their 4‐month‐
old infants’ actions predicted these infants’ own rudimentary
signs of imitation (measured by EMG), suggesting that infants may
learn to imitate via repeated associative pairings of their own and
others’ actions (de Klerk, Lamy‐Yang, & Southgate, 2018);

4. A systematic meta‐analysis suggesting that automatic imitation in
adults is also best explained by an associative learning framework
(Cracco et al., 2018), meaning that the existence of neonatal imi‐
tation would require the non‐parsimonious addition of a second,
innate mechanism to explain the same phenomenon;

5. A statistically robust re‐analysis of data previously used to sup‐
port the existence of neonatal imitation in rhesus macaques
(Paukner, Pederson, & Simpson, 2017), showing that neonatal
macaques have in fact failed to produce imitative actions at levels
greater than chance (Redshaw, 2019);

6. A study suggesting that newborn primates are not born with an
innate capacity to recognize faces, meaning they would be un‐
able to link the actions of other faces with those of their own face
(Arcaro, Schade, Vincent, Ponce, & Livingstone, 2017); and

7. An unpublished PhD thesis that similarly found no evidence of
neonatal imitation in a longitudinal study of 90 human infants
measured at four time points (Barbosa, 2017).

Despite these dovetailing discoveries, researchers who have previ‐
ously published positive findings of neonatal imitation have defended
their results by questioning the validity of our longitudinal study.
Thirteen prominent neonatal imitation researchers published a rebut‐
tal (Meltzoff et al., 2017), in which they made two seemingly contradic‐
tory arguments: (a) our study was too methodologically flawed to detect
imitation effects, but also (b) our data do in fact contain evidence for
neonatal imitation of tongue protrusion. In a response (Oostenbroek et
al., 2018), we outlined why the so‐called “flaws” were inconsistent with
our actual patterns of results, inconsistent with broader findings in the
literature, and/or incompatible with earlier claims made by Meltzoff
and others. For instance, Meltzoff et al. (2017, pp. 6) argued that having
an unfamiliar model is the “key” to eliciting neonatal imitation, despite
earlier reports that the phenomenon “did not vary as a function of fa‐
miliarity with the model” (Meltzoff & Moore, 1992, pp. 479).

Here, we focus on the second prong of Meltzoff et al.’s (2017)
rebuttal. In their post‐hoc re‐analysis of our data, the authors
showed that infants’ frequencies of tongue protrusion in response
to the tongue protrusion model were significantly greater than
their average frequencies of tongue protrusion in response to the
other 10 control models (which included dynamic faces, manual
actions, object actions and verbalizations). In our original analy‐
ses, by contrast, we conducted pairwise comparisons showing that
infants failed to significantly protrude their tongues more often
in response to the tongue protrusion model than in response to

the mouth opening, happy face, and sad face models. The logic
for conducting pairwise comparisons is to guard against the sim‐
ple possibility that certain categories of control models (e.g. dy‐
namic faces) might elicit higher levels of tongue protrusion than
others (Oostenbroek et al., 2018). If so, then one might expect a
significant finding of “imitation” when averaging across all control
models, even if infants are not in fact matching the specific action
(see Meltzoff & Moore, 1977; Paukner et al., 2017, for similar ar‐
guments). Meltzoff et al.’s (2017) re‐analysis also disregards the
gold standard “cross‐target” approach (Meltzoff, 1996; Meltzoff &
Moore, 1977), which requires that infants demonstrate flexibility
in matching responses across multiple actions before evidence for
imitation is declared.

Nevertheless, by claiming that our data contain evidence for
tongue protrusion imitation, Meltzoff et al. (2017) are in effect for‐
mulating a testable hypothesis for the dominant like me framework
(Meltzoff, 2005, 2007). That is, if (a) the infants in our sample were
in fact imitating tongue protrusion, and (b) the like me framework is
correct, then (c) Meltzoff et al.’s operationalization of tongue pro‐
trusion imitation should be associated with later imitation and other
social cognitive behaviours in our sample (Heimann et al., 1989;
Suddendorf et al., 2013). Given that we had originally planned to
test for such associations, we had in fact collected data on social
cognitive behaviours from many of our participants over the first
18 months of life. Although there was little point in conducting cor‐
relations following our reported results (as they yielded no signs of
neonatal imitation), we are now able to test for associations in light
of Meltzoff et al.’s (2017) re‐analysis.

We therefore examined relationships between Meltzoff et
al.’s (2017) operationalization of tongue protrusion imitation and:
(a) object‐directed imitation measured at 6, 9, 12 and 18 months,
(b) joint attention measured at 9 and 12 months, (c) synchronous
imitation measured at 18 months, and (d) mirror self‐recognition
measured at 18 months. We originally selected this wide range
of measures in order to test the strong continuity and general‐
izability claims at the heart of the like me framework: that neo‐
natal imitation sits at the foundation of not only later‐developing
forms of imitation, but also human social cognition in the broader
sense (Meltzoff, 2005, 2007; Meltzoff & Brooks, 2001). Both
object‐directed imitation (e.g. Carpenter, Nagell, & Tomasello,
1998; Nielsen, 2006) and synchronous imitation (e.g. Asendorpf,
Warkentin, & Baudonniere, 1996; Nielsen & Dissanayake, 2004)
gradually emerge over the initial two years of life, and if these
abilities are indeed continuous with the supposed capacity for
neonatal imitation, then we might expect to find significant cor‐
relations with Meltzoff et al.’s (2017) operationalization of tongue
protrusion imitation. Similarly, both joint attention (e.g. Corkum &
Moore, 1998; Johnson, Slaughter, & Carey, 1998) and mirror self‐
recognition (e.g. Gallup, 1970; Suddendorf & Butler, 2013) develop
during infancy, and if these broader social cognitive abilities are
indeed supported by the same mechanisms as neonatal imitation,
then we likewise might expect correlations with Meltzoff et al.’s
(2017) operationalization.

4 of 13  |     REDSHAW Et Al.

2   |   M E T H O D

2.1 | Participants

Participants included 71 of the original sample of 106 infants from
Oostenbroek et al.’s (2016) study. The remaining 35 original partici‐
pants were assessed at neonatal time points only as part of the PhD
project of one of the authors (JO), and were never intended to form
part of the larger longitudinal assessment. The final 71 infants in‐
cluded 38 females and 33 males. All participants were born full‐term,
with a mean gestational age of 39.88 months (SD = 1.22 months,
range = 36.6–43.0 months). Mean birth weight was 3.59 kg
(SD = 0.43 kg, range = 2.54–4.60 kg), and 51 infants were delivered
vaginally (20 via Caesarean section).

The large majority of these 71 infants contributed data to the
neonatal imitation measure at 1 week (n = 61), 3 weeks (n = 63),
6 weeks (n = 66) and 9 weeks (n = 64), and on the other social cog‐
nitive measures at 6 months (n = 70), 9 months (n = 70), 12 months
(n = 69) and 18 months (n = 69). Infants who did not contribute data
at a given time point were excluded from all analyses involving the
variables measured at that time point.

2.2 | Measures

2.2.1 | Neonatal tongue protrusion “imitation”

Comprehensive details of the neonatal imitation measure are in‐
cluded in the Appendix S1 of Oostenbroek et al. (2016). In brief,
infants were exposed to 1‐minute demonstrations of 11 separate
modelled actions at 1, 3, 6 and 9 weeks of age. These 11 actions
included oral gestures (tongue protrusion, mouth opening), object
actions analogous to the oral gestures (a spoon protruding through
a tube, a box opening), facial expressions (happy face, sad face),
manual gestures (index finger pointing, grasping) and verbaliza‐
tions (mmm sound, eee sound, tongue click sound). We subsequently
coded how frequently infants produced each of these gestures (ex‐
cluding the object actions) in response to each of the modelled dem‐
onstrations. Given that Meltzoff et al. (2017) only suggest that the
tongue protrusion gesture was imitated in the sample, we limit our
current analysis to this gesture.

Scoring

Following Meltzoff et al.’s (2017) operationalization, infants’ tongue
protrusion “imitation” scores at 1, 3, 6 and 9 weeks were calculated
by subtracting the mean frequency of tongue protrusions in response
to non‐matching models from the frequency of tongue protrusions
in response to the matching model. The mean frequency was typi‐
cally calculated across all 10 control models, although in some cases
the infant was not exposed to all 10 controls (e.g. because they were
not alert enough to complete the duration of the experiment) and
so the mean represented the frequency of tongue protrusions in re‐
sponse to a more limited selection of controls. A positive score on
this variable indicated that the infant showed a greater propensity

to protrude their tongue in response to the tongue protrusion model
than to other models on average. Infants who did not see the tongue
protrusion model at a given time point were excluded from all analy‐
ses involving that time point.

2.2.2 | Object‐directed imitation

Each infant was administered three separate object‐directed imita‐
tion tasks, broadly similar to those developed by Carpenter et al.
(1998), at each of 6, 9, 12 and 18 months of age. During all tasks, the
infant was seated on their caregiver’s lap at a table directly across
from the experimenter. Infants could receive either 0, 1 or 2 points
for each task, and the presentation order of all tasks was counterbal‐
anced across infants and time points.

For the door opening task, the experimenter placed on the table
a box apparatus with two openable doors at the front. The exper‐
imenter opened one of the doors, retrieved a toy from inside and
showed it to the infant before placing it back inside and closing the
door. The experimenter then repeated this series of actions five
times in total, never opening or touching the second door. Finally, the
experimenter pushed the apparatus towards the infant. We coded
whether or not the infant opened the target door (0 or 1 point) and
whether or not they touched the toy inside (0 or 1 point) at any time
before the end of the 60 s trial.

For the rattle task, the experimenter placed on the table two
small lidded containers. The experimenter picked up one of the con‐
tainers and shook it to make a rattling sound, and then placed the
container back on the table. The experimenter repeated this series
of actions five times in total, never picking up and shaking the second
container. Finally, the experimenter pushed the containers towards
the infant. We coded whether or not the infant touched the target
container (0 or 1 point) and whether or not they shook the target
container (0 or 1 point) at any time before the end of the 60 s trial.

For the circular container task, the experimenter placed on the
table a circular red container with a green lid. The experimenter
opened the lid and placed it next to the container, before retrieving a
toy from the container. As the experimenter lifted the toy, she began
rattling it to produce a sound before placing it on the table next to
the container. She then lifted the toy up again and began rattling it
before placing it back into the container. The experimenter repeated
this series of actions five times in total, never touching the lid of the
container. Finally, the experimenter pushed the open container, the
lid and the toy (which was also on the table) towards the infant. We
coded whether or not the infant touched the toy (0 or 1 point) and
whether or not they shook the toy and placed it into the container (0
or 1 point) at any time before the end of the 60 s trial.

Scoring

For each infant at each time point, we first calculated an average
score across the door opening, rattle and circular container tasks
(range = 0–2). We then divided this initial score by 2 to give a stand‐
ardized continuous score between 0 and 1. For infants whose data
were missing for one or two of the tasks at a given time point, these

     |  5 of 13REDSHAW Et Al.

averages were calculated across the tasks without missing data (such
that the final standardized score still ranged between 0 and 1).

2.2.3 | Joint attention

Each infant was administered three separate joint attention tasks
at each of 9 and 12 months of age (see, e.g. Behne, Liszkowski,
Carpenter, & Tomasello, 2012; Carpenter et al., 1998; Slaughter &
McConnell, 2003). During the first two tasks, the infant was seated
on their caregiver’s lap at a table directly across from the experi‐
menter. For the gaze following task, the experimenter first captured
the infant’s attention, before looking to her left at a picture on the
wall and making a surprised exclamation. The experimenter briefly
looked back at the child, before again looking to her left for approxi‐
mately 15 s. The experimenter then repeated this exact sequence
of actions for a picture on the wall to her right (the order of gaze
direction was counterbalanced across infants). We coded whether or
not the infant followed the experimenter’s gaze to the left with a full
head turn (0 or 1 point), and whether or not the infant followed the
experimenter’s gaze to the right with a full head turn (0 or 1 point).
The infant could thus receive a score of 0, 1, or 2 for gaze following.

For the gaze and point following task, the experimenter first cap‐
tured the infant’s attention, before turning to her right and pointing
at a picture on the wall and making a surprised exclamation. After
approximately 15 s, the experimenter returned her hand to a normal
position and again captured the infant’s attention. The experimenter
then turned her head to her left and pointed at a picture on the wall
while making a surprised exclamation (the order of pointing direc‐
tion was counterbalanced across infants). We coded whether or not
the infant followed the experimenter’s point to the left with a full
head turn (0 or 1 point), and whether or not the infant followed the
experimenter’s point to the right with a full head turn (0 or 1 point).
The infant could thus receive a score of 0, 1, or 2 for gaze and point
following.

For the point production task, the infant sat at a table next to
the main experimenter, who was looking at a book and ignoring the
infant. Meanwhile, a second experimenter – who was unseen and
standing behind a black curtain in front of the infant – pushed two
rattles through the curtain one at a time (one on the left, one on the
right) and shook them loudly for approximately 15 s each. We coded
whether or not the infant tried to get the attention of the main ex‐
perimenter by pointing in the same direction as the rattle on the left
(0 or 1 point) and the rattle on the right (0 or 1 point). Infant pointing
actions had to be judged as intentional by the coder to receive a
score of 1. The infant could thus also receive a score of 0, 1, or 2 for
point production.

Scoring

For each infant at each time point, we first calculated an average
score across the gaze following, gaze and point following, and point
production measures (range = 0–2). We then divided this initial
score by 2 to give a standardized continuous score between 0 and 1.
Combining the measures into a single score in this way was justified

by the fact that previous studies have found correlations between
gaze/point following and point production (e.g. Behne et al., 2012;
Carpenter et al., 1998), consistent with the existence of a general
“joint attention” construct. For infants whose data were missing for
one or two of the gaze following, point following, or point produc‐
tion measures at a given time point, these averages were calculated
across the tasks without missing data (such that the final standard‐
ized score still ranged between 0 and 1). Six infants who participated
in the study at 9 months provided no data for any joint attention
tasks and so were excluded from all analyses involving joint atten‐
tion at that time point.

2.2.4 | Synchronous imitation

Each infant was administered four separate synchronous imita‐
tion tasks at 18 months of age (see, e.g. Asendorpf et al., 1996;
Nielsen & Dissanayake, 2004). During all tasks, the infant was
seated on their caregiver’s lap at a table directly across from the
experimenter. Prior to each task, the experimenter produced two
identical toys, placing one in front of herself and one in front of
the infant.

For each task, the experimenter repetitively produced two ac‐
tions for approximately 15 s (five times each for approximately 3 s
each time). In the mug task, the experimenter tapped the bottom of
a cup and turned it on its end. In the hammer task, the experimenter
flipped a toy hammer side to side and then tapped the handle with
her hand. In the toothbrush task, the experimenter pretended to
brush her hair and then brushed her arm. In the saw task, the exper‐
imenter pretended to saw her hand and then tapped the blade of
the saw on the palm of her hand. For each of these tasks, we coded
whether or not the infant produced each of the two experimenter
actions simultaneously with the experimenter (0 or 1 point for each
action, with a range of 0–2 for each task).

Scoring

For each infant, we first calculated an average score across the mug,
hammer, toothbrush and saw tasks (range = 0–2). We then divided
this initial score by 2 to give a standardized continuous score be‐
tween 0 and 1. For infants whose data were missing for between
one and three of the tasks, the average was calculated across the
tasks without missing data (such that the final standardized score
still ranged between 0 and 1).

2.2.5 | Mirror self‐recognition

Each infant was administered the mark test for mirror self‐recog‐
nition at 18 months of age. The experimenter directed the infant’s
attention towards a large mirror for a familiarization period of ap‐
proximately 30 s (or until the infant had looked directly at the
mirror), before covering up the mirror with a black sheet. The experi‐
menter then surreptitiously placed a sticker on the infant’s forehead
before uncovering the mirror. We coded whether or not the infant
actively touched the sticker or a region within 2cm of it (score of 0 or

6 of 13  |     REDSHAW Et Al.

1) before approximately 20 s had passed (see Nielsen & Dissanayake,
2004).

2.3 | Procedu

re

Details of the neonatal testing procedure are reproduced in the
Appendix S1 of Oostenbroek et al. (2016). For the later measures, all
testing was conducted in laboratories in the School of Psychology
at the University of Queensland in Brisbane, Australia. Each session
lasted approximately 45–60 min in total.

2.4 | Coding reliability

See the Appendix S1 of Oostenbroek et al. (2016) for comprehensive
coding reliability information for the neonatal imitation measure. All
later developing social cognitive variables were coded by a trained
research assistant (JC). Twenty percent of the data were also coded
by a blind and independent rater for reliability purposes. Inter‐rater
reliability was excellent (Cicchetti, 1994) for five of the eight meas‐
ures, with intraclass correlation coefficients ranging from 0.808 to
0.935. Reliability was good for one measure (object‐directed imi‐
tation at 12 months) and fair for the other two measures (joint at‐
tention at 9 months and synchronous imitation at 18 months), with
intraclass correlation coefficients of 0.680, 0.515 and 0.520. Full
reliability data are reproduced in the Appendix S1.

3   |   R E S U LT S

3.1 | Patterns of results within each task

3.1.1 | Tongue protrusion “imitation” between 1 and
9 weeks

As seen in Figure 1, infants’ tongue protrusion “imitation” scores
were consistently greater than zero, which is broadly consistent with
Meltzoff et al.’s (2017) re‐analysis. One sample t‐tests, however, re‐
vealed that these scores were not significantly greater than zero at
1 week, t (60) = 1.09, p = .278, 3 weeks, t (62) = 1.21, p = .230, or

6 weeks, t (65) = 1.49, p = .140. Only at 9 weeks were scores signifi‐
cantly above zero, t (63) = 2.59, p = .012. The non‐significant results
from the first three time points may reflect the fact that this sample
of infants included a smaller subset of Oostenbroek et al.’s (2016)
original sample. Although Figure 1 may give the impression that
tongue protrusion “imitation” scores increased over time, a post‐hoc
repeated measures ANOVA on the infants who contributed data to
all time points revealed that this apparent trend was not significant,
linear F (1, 45) = 2.53, p = .119. When averaging across all time points,
tongue protrusion “imitation” scores were significantly greater than
zero, t (70) = 3.19, p = .002.

3.2 | Later developing social cognitive variables

3.2.1 | Mean scores and change over time

Infants’ standardized mean scores for object‐directed imitation (6, 9,
12 and 18 months), joint attention (9 and 12 months), synchronous
imitation (18 months) and mirror self‐recognition (18 months) are
presented in Figure 2. Repeated measures ANOVAs confirmed that
object‐directed imitation scores significantly increased with age, lin‐
ear F (1, 65) = 160.46, p < .001, and that joint attention scores sig‐ nificantly increased from 9 months to 12 months, F (1, 62) = 59.85, p < .001. These patterns are consistent with those seen in previous studies (see, e.g. Mundy et al., 2007; Nielsen & Dissanayake, 2004).

3.2.2 | Variation in scores

Figure 3 shows the frequency histograms for children’s scores on
each of the social cognitive measures at each time point. This figure
demonstrates that nearly all infants showed at least minimal signs
of object‐directed imitation and joint attention at all measured time
points, although at no time did the majority of infants score at ceil‐
ing (i.e., a score of 1) on any measure. The figure also demonstrates
that just over half of the infants showed at least minimal evidence of
synchronic imitation at 18 months (with none performing at or close
to ceiling), and just under half showed evidence of mirror self‐recog‐
nition at the same time point. Overall, these histograms indicate that
we were observing the behaviours at rates in line with past studies
(e.g. Nielsen & Dissanayake, 2004), and when infants were at a wide
variety of competence levels. Presumably, we therefore had a good
chance of detecting correlations if they are indeed present in the
population.

3.3 | Associations between different measures

3.3.1 | Consistency of tongue protrusion “imitation”
across time points

Table 1 shows the Spearman correlations between infants’ tongue
protrusion “imitation” scores across neonatal time points, as an as‐
sessment of intra‐individual consistency in the measure proposed
by Meltzoff et al. (2017). Correlation values ranged from −0.210 to

F I G U R E 1   Mean tongue protrusion “imitation” scores across the
first 9 weeks. Scores were calculated using Meltzoff et al.’s (2017)
suggested method. Error bars indicate standard error of the mean,
and asterisks indicate scores that are significantly greater than zero

–

0.05

0
0.05

0.1

0.15

0.2

0.25

0.3

0.35

0.4

1 3 6 9 mean

M
ea

n
to

ng
ue

p
ro

tr
us

io
n

‘im
it

a�
on

‘ s
co

re

Age (weeks)

*

*

     |  7 of 13REDSHAW Et Al.

0.253, and a one sample t‐test indicated that the mean correlation
size (rs = 0.001, 95% CI [−0.179, 0.181]) did not significantly differ
from zero, t (5) = 0.014, p = .989.

The scaled JZS Bayes Factor in favour of the null hypothesis was
equal to 2.68, suggesting that the mean correlation was 2.68 times
more likely to be observed under a true null hypothesis than a true
alternative hypothesis. None of the correlations were significant
after applying a Bonferroni correction, all adjusted p > .30, nor were
any significant after applying the more liberal Benjamini‐Hochberg
(q = 0.05) correction (see Table S5). On the whole, there was nothing
to suggest intra‐individual consistency in “imitation” scores. Namely,
there was nothing to suggest that infants who scored higher at any
given time point on Meltzoff et al.’s (2017) operationalization of

neonatal imitation also scored systematically higher on this variable
at other time points, as would be expected if it were truly measuring
a fundamental social cognitive capacity. Rather, the data are con‐
sistent with our interpretation that this operationalization does not
measure true imitation or any other construct of importance.

3.3.2 | Relationships between tongue protrusion
“imitation” and later social cognitive variables

Table 2 shows the Spearman correlations between neonatal tongue
protrusion “imitation” scores and the later developing social cogni‐
tive variables, as an assessment of predictions following from the
like me framework (Meltzoff, 2005, 2007). Correlation values ranged

F I G U R E 2   Standardized mean scores
for social cognitive variables over the
first 18 months, with error bars indicating
standard error of the mean. The object‐
directed imitation, joint attention and
synchronous imitation scores were
calculated according to the criteria
outlined in the methods. The mirror
self‐recognition score represents the
proportion of infants who passed the
mark test

0
0.1
0.2
0.3
0.4

0.5

0.6

0.7

0.8

0.9

1

6 9 12 18
0(

serocS
nae

M
desidradnatS

-1
)

Age (months)

object-directed imita�on

joint a�en�on

synchronous imita�on

mirror self-recogni�on

F I G U R E 3   Frequency histograms for social cognitive variables over the first 18 months. Object‐directed imitation (ODI), joint attention
(JA) and synchronous imitation (SI) scores are on continuous scales, whereas mirror self‐recognition (MSR) scores are categorical

8 of 13  |     REDSHAW Et Al.

from −0.208 to 0.270, and a one sample t‐test indicated that the
mean correlation size (rs = 0.027, 95% CI [−0.020, 0.075]) did not sig‐
nificantly differ from zero, t (31) = 1.17, p = .250.

The scaled JZS Bayes Factor in favour of the null hypothesis was
equal to 2.84, suggesting that the mean correlation was 2.84 times
more likely to be observed under a true null hypothesis than a true
alternative hypothesis. None of the correlations were significant
after applying a Bonferroni correction, all adjusted p > .999, nor were
any significant after applying a more liberal Benjamini‐Hochberg
(q = 0.05) correction (see Table S5). Overall, there was nothing to
suggest that infants who scored higher at any time point on Meltzoff
et al.’s (2017) operationalization of neonatal imitation also scored
systematically higher on the other later‐measured social cognitive
variables, as would be expected under the like me framework of neo‐
natal imitation (Meltzoff, 2005, 2007). Again, the data are consistent
with our interpretation that this operationalization does not reflect
true imitation, and that the like me framework is controverted.

3.4 | Post‐hoc exploratory analyses

Following suggestions from peer reviewers, we performed two se‐
ries of additional, exploratory analyses of our data. Although neither
series of analyses has a direct bearing on the validity of the like me
framework, they do provide (post‐hoc) tests of alternative hypoth‐
eses regarding the early development of social cognition in our large
sample of infants.

3.4.1 | Consistency and predictive
value of neonates’ tendency to protrude the tongue in
response to facial gestures

Bjorklund (2018) recently highlighted that the neonates in our origi‐
nal study consistently displayed tongue protrusions in response to
facial gestures (compared to other models), and suggested that such
a tendency might serve to maintain face‐to‐face interactions be‐
tween infants and their caregivers. We therefore examined whether
the neonates showed intra‐individual consistency in this tendency
across neonatal time points, and whether individual differences pre‐
dicted later‐developing social cognitive behaviour. For each neonatal
time point in the original full sample from Oostenbroek et al. (2016),
we first obtained a “face‐specific tongue protrusion score” by calcu‐
lating the difference between (a) the average frequency of tongue
protrusions in response to the facial gesture models (tongue protru‐
sion, mouth opening, happy face, sad face) and (b) the average fre‐
quency of tongue protrusions in response to the seven other models.
Supporting Bjorklund’s (2018) observations, a series of one‐sample
t‐tests indicated that these scores were significantly above zero at
3 weeks, t (92) = 4.52, p < .001, 6 weeks, t (100) = 3.58, p = .001 and 9 weeks of age, t (95) = 3.49, p = .001, and above zero but not signifi‐ cantly so at 1 week of age, t (87) = 1.88, p = .063.

T A B L E 1   Spearman correlations among tongue protrusion
“imitation” scores across neonatal time points

1 week 3 weeks 6 weeks 9 weeks

1 week ‐ −0.210 −0.157 0.121

3 weeks – −0.013 0.012

6 weeks – 0.253

9 weeks –

Note: No correlations were significant after Bonferroni or Benjamini‐
Hochberg corrections were applied.
Correlation colour scale. −1 1.

Social cognitive variables

Tongue protrusion “imitation” scores

1 week 3 weeks 6 weeks 9 weeks

Object‐directed imitation
(6 months)

0.190 −0.041 0.244 0.214

Object‐directed imitation
(9 months)

−0.208 0.119 −0.006 0.008

Object‐directed imitation
(12 months)

0.082 0.084 −0.148 0.050

Object‐directed imitation
(18 months)

−0.073 −0.098 −0.003 0.077

Joint attention (9 months) 0.202 −0.094 0.143 0.208

Joint attention (12 months) −0.089 −0.056 0.123 0.270

Synchronous imitation
(18 months)

−0.154 −0.102 0.136 −0.110

Mirror self‐recognition
(18 months)

0.045 −0.160 0.000 0.024

Note: No correlations were significant after Bonferroni or Benjamini‐Hochberg corrections were
applied.
Correlation colour scale. −1 1.

T A B L E 2   Spearman correlations
between tongue protrusion “imitation”
and social cognitive variables

     |  9 of 13REDSHAW Et Al.

As shown in Tables S2 and S5, however, there was no compelling
evidence of intra‐individual consistency in these facial model tongue
protrusion scores across time points, with no correlations having
significant p values using either Bonferroni or Benjamini‐Hochberg
(q = 0.05) corrections. Spearman correlation values ranged from
−0.126 to 0.230, and a one sample t‐test indicated that the mean
correlation size (rs = 0.081, 95% CI [−0.042, 0.203]) did not signifi‐
cantly differ from zero, t (5) = 1.69, p = .151. Furthermore, as shown
in Tables S3 and S5, the facial model tongue protrusion scores failed
to predict later‐developing social cognitive behaviours in the cur‐
rent sub‐sample of infants, with no correlations having significant
p values using either Bonferroni or Benjamini‐Hochberg (q = 0.05)
corrections. Spearman correlation values ranged from −0.273 to
0.261, and a one sample t‐test indicated that the mean correlation
size (rs = 0.004, 95% CI [−0.041, 0.049]) did not significantly differ
from zero, t (31) = 0.17, p = .865. For these mean correlations, the
scaled JZS Bayes Factors in favour of the null hypotheses were 1.05
and 5.22, respectively. Our data therefore contain no evidence to
suggest inter‐individual reliability in neonates’ propensity to pro‐
trude their tongues in response to facial gestures, and no evidence
that scores for such a tendency at any neonatal time point have any
predictive value for the later‐developing social cognitive behaviours
we measured.

3.4.2 | Associations among later‐developing social
cognitive variables

Our second series of post‐hoc analyses examined relationships
among the later‐developing social cognitive variables themselves.
Similar to our analyses involving the neonatal “imitation” scores,
we found no compelling evidence of intra‐individual consistency in
these variables. As shown in Tables S4 and S5, no Spearman correla‐
tions had significant p values when either Bonferroni or Benjamini‐
Hochberg (q = 0.05) corrections were applied. Correlation values
ranged from −0.282 to 0.349, and a one sample t‐test indicated that
the mean correlation size (rs = 0.050, 95% CI [−0.007, 0.107]) did not
significantly differ from zero, t (27) = 1.79, p = .084. For this mean
correlation, the scaled JZS Bayes Factor in favour of the null hypoth‐
esis was 1.22.

4   |   D I S C U S S I O N

The original aim of our research programme was to examine longi‐
tudinal relationships between neonatal imitation and later‐develop‐
ing social cognitive variables (Suddendorf et al., 2013), yet this aim
was abandoned after we failed to obtain any compelling evidence
of imitation when participants were neonates (Oostenbroek et al.,
2016). Following on from Meltzoff et al.’s (2017) re‐analysis of our
data, however, we revisited the possibility of observing such longi‐
tudinal associations. If Meltzoff et al.’s (2017) operationalization of
neonatal imitation is valid, and if the like me framework (Meltzoff,
2005, 2007) is correct, then we would expect imitation scores to

predict measures of social cognitive development (Heimann et al.,
1989; Simpson, Paukner, et al., 2014b; Suddendorf et al., 2013). This
hypothesis was not supported by the results.

Across the four neonatal time points between 1 and 9 weeks,
there was no evidence that infants’ tongue protrusion “imitation”
scores were positively and reliably correlated with each other.
Rather, the average correlation did not significantly differ from zero.
Even granting Meltzoff et al.’s (2017) operationalization of imitation,
this finding fails to support the hypothesis that there exists a spe‐
cial class of “imitators” among the population of neonates (Heimann,
2002). In defence of this idea, Simpson, Murray, et al. (2014a) write
that “only about 50% of neonates consistently engage in imitation of
facial gestures” (pp. 7; also see Paukner, Simpson, Ferrari, Mrozek,
& Suomi, 2014; Simpson, Paukner, et al., 2014b). We suggest, how‐
ever, that this proportion of 50% is no coincidence. Indeed, if au‐
thors are categorizing infants as “imitators” primarily on the basis
that they show greater increases in Action A in response to Modelled
Action A than in response to Modelled Action B (see, e.g. studies
with rhesus macaques by Simpson, Miller, Ferrari, Suomi, & Paukner,
2016; Simpson, Paukner, Sclafani, Suomi, & Ferrari, 2013; Simpson,
Paukner, et al., 2014b; Wooddell, Simpson, Murphy, Dettmer, &
Paukner, 2019), then one would expect about 50% of infants to be
“imitators” by chance alone (note also that these macaque studies do
not report results using appropriate control models; Redshaw, 2019).
We suggest that studies should not classify infants as consistent “im‐
itators” unless it can be shown that (a) there is an overall effect of
imitation in the sample, and (b) there is a positive correlation be‐
tween imitation scores across time points and actions. Although it
is debateable whether the neonates in our sample met criterion (a)
for tongue protrusion (cf. Meltzoff et al., 2018, 2017; Oostenbroek
et al., 2016, 2018), there can be no doubt that they failed to meet
criterion (b).

One might argue that, even given the lack of correlations be‐
tween “imitation” scores across neonatal time points, there may still
be predictive value for the scores from one particular time point.
Indeed, given that tongue protrusion “imitation” scores in this subsa‐
mple of Oostenbroek et al.’s (2016) neonates were only significantly
above zero at 9 weeks, it could be contended that this was the only
time point when we were capturing true imitation variance. If so,
then the like me framework would only predict “imitation” scores
at this time point to significantly correlate with later developing
social cognitive variables. Our data fail to support this possibility.
There was no evidence that tongue protrusion “imitation” scores at
9 weeks – or at any other time point for that matter – predicted any
of the later developing social cognitive variables. Thus, even granting
the most charitable interpretation of Meltzoff et al.’s (2017) re‐anal‐
ysis of our data, there is still no evidence for the prevailing like me
framework of neonatal imitation’s function.

An alternative explanation for the lack of correlations between
neonatal imitation and later developing social cognition is that,
rather than differing across individuals (Heimann, 2002; Simpson,
Murray, et al., 2014a), the capacity is equally available to all typically
developing infants. Under this scenario, any individual differences

10 of 13  |     REDSHAW Et Al.

in measured neonatal imitation scores would exist simply as a func‐
tion of fluctuations in motivation and attention during testing – and
not social cognitive proficiency. This possibility seems unlikely, how‐
ever, given that previous studies have found reliable intra‐individual
stability in neonatal temperament (Wachs, Pollitt, Cueto, & Jacoby,
2004; Worobey & Blajda, 1989). Thus, if measures of neonatal imi‐
tation do indeed capture variance in motivation and attention rather
than capacity, then one would still expect to find consistencies in
neonatal imitation scores as a function of individual differences in
temperament. Our data show no evidence of such consistencies.

Another alternative explanation for the lack of correlations is
that neonatal imitation is indeed a genuine phenomenon, and yet,
contra Meltzoff’s (2005, 2007) like me framework, it has no link
at all to later‐developing forms of imitation and social cognition
(Bjorklund, 1987). Under this view, one might expect individual dif‐
ferences in neonatal imitation to predict only very early forms of
social cognition, such as the tendency to maintain mutual gaze with a
caregiver (see Heimann, 1989), and not the forms we measured here.
Of course, both of these alternative explanations presuppose that
neonatal imitation is a genuine phenomenon, which recent evidence
suggests is unlikely (Arcaro et al., 2017; Barbosa, 2017; Cracco et
al., 2018; Keven & Akins, 2017; de Klerk et al., 2018; McKyton et al.,
2018; Oostenbroek et al., 2016; Redshaw, 2019).

Although our results argue against neonatal imitation as the
foundational building block of the like me framework (Meltzoff,
2005, 2007), we do not consider the framework itself to be com‐
pletely untenable. Indeed, human preschoolers tend to faithfully
copy many actions modelled to them, even those that are clearly
irrelevant to achieving an instrumental outcome (for a recent re‐
view, see Hoehl et al., 2019). Non‐human great apes, on the other
hand, typically copy instrumental actions only (Clay & Tennie, 2017;
Horner & Whiten, 2005). One plausible mechanism for the develop‐
ment of this uniquely human imitative tendency is that, consistent
with the like me framework, children “represent the acts of others
and their own acts in commensurate terms” (Meltzoff, 2007, pp.
126). Our data merely diverge from this framework by suggesting
that the capacity to recognize and act upon such cross‐modal equiv‐
alences may instead emerge postnatally.

4.1 | Exploratory findings, limitations and
future directions

In an exploratory, post‐hoc series of analyses, we found support for
Bjorklund’s (2018) observation that the neonates in our original sam‐
ple tended to protrude their tongues more frequently in response to
facial gesture models than to other models. Bjorklund suggested that
such a tendency – while not imitation – might serve to maintain so‐
cial interactions between infants and their caregivers. Several other
authors have made similar cases about neonatal actions, with vary‐
ing degrees of richness in their interpretations of behavioural match‐
ing (see Bjorklund, 1987; Byrne, 2005; Heimann, 1989; Jones, 2007,
2009; Legerstee, 1991; Nagy & Molnar, 2004). Although infants ap‐
pear to lack cortical control over tongue movements in the first few

months of life (Keven & Akins, 2017), they may still increase their
rates of tongue protrusion as a function of general arousal (Jones,
1996, 2006). Furthermore, parents often imitate their infants’ ac‐
tions (Kokkinaki & Kugiumutzakis, 2000), including tongue protru‐
sion (Jones & Yoshida, 2011), and this tendency appears to predict
infants’ own rudimentary signs of imitation at 4 months of age (de
Klerk et al., 2018). One possibility, therefore, is that neonatal tongue
protrusion does in fact function to increase caregiver bonding and
facilitate the eventual development of imitation, and that neonates’
general arousal when observing facial gestures is a mechanism that
facilitates this process. This would be consistent with Meltzoff’s
(2005, 2007) broader point about neonatal behaviours serving a so‐
cial function, although not in the rich intentional sense that the like
me framework proposes. Note, however, that we found no significant
intra‐individual consistency in neonates’ specific tendency to pro‐
trude their tongue in response to facial gestures. This tendency may
therefore fluctuate as a function of general, species‐wide factors
that vary over time, rather than as a function of genetically ingrained
individual differences. Still, the Bayes Factor for the mean correla‐
tion was close to 1 (i.e., failure to discriminate between the null and
alternative hypothesis), and so future research with increased power
may indeed uncover significant intra‐individual consistency.

In a second series of post‐hoc analyses, we found that the so‐
cial cognitive measures themselves also failed to correlate with each
other across time points. This pattern of results is broadly consistent
with those of several other studies that have failed to find reliable
correlations among several social cognitive variables in infancy (e.g.
Slaughter & McConnell, 2003; Striano & Bertin, 2005; Striano, Stahl,
& Cleveland, 2009). The pattern is inconsistent, however, with that
of Carpenter et al. (1998), who found several correlations between
object‐directed imitation, attention following, and communicative
gesture variables in infants aged between 9 and 15 months. It remains
ambiguous, therefore, just how much unity exists across the various
measures of early social cognitive development (also see Nielsen &
Dissanayake, 2004). One possibility is that previous interpretations of
these measures have been overly rich (cf. Haith, 1998), and that they
simply do not reliably gauge the development of domain‐general so‐
cial cognitive faculties. Again, however, the Bayes Factor for the mean
correlation was quite close to 1, meaning that a higher powered study
may have indeed uncovered significant effects. Only future research
and perhaps meta‐analytic techniques will resolve this issue.

The current study provides the first longitudinal investigation
of associations between neonatal “imitation” and later‐developing
forms of human social cognition since Heimann et al. (1989) initially
called for such an investigation three decades ago. Nevertheless,
despite its comprehensiveness and relatively large sample in infant
psychology terms, the study may still have been limited by power
issues. This limitation, however, must be considered in the light of
our overwhelming pattern of null findings, with not a single p value
crossing the threshold for statistical significance using either con‐
servative (Bonferroni) or liberal (Benjamini‐Hochberg) corrections.
It must also be considered in light of the strong claim at the cen‐
tre of the like me framework – that neonatal imitation is an evolved

     |  11 of 13REDSHAW Et Al.

mechanism functioning as the engine of human social cognition
(Meltzoff, 2005, 2007). If this claim is true, then one might expect
associations with social cognition to more readily evince themselves,
even with sample sizes such as ours.

Other limitations include the fact that our object‐directed im‐
itation tasks did not include a baseline measure, and that some of
the actions contributing to scores on these tasks may have instead
reflected more basic processes such as stimulus enhancement (e.g.
consider the requirement to open a door and touch a target toy in
the door task). Although we wished to keep our tasks relatively short
given the large assessment protocol, it would have indeed been ideal
to have some baseline measure in this particular case. Note, however,
that we detected large degrees of variance in all of our social cogni‐
tive measures, including object‐directed imitation (see Figure 3), and
that we replicated previous findings showing increases in children’s
object‐directed imitative fidelity with age (see Figure 2). Presumably,
at least some of this variance was due to individual differences and
developmental transitions in children’s capacity and propensity to
copy the actions just shown to them by the experimenter. Therefore,
one might still have expected correlations with neonatal “imitation”
scores if such associations genuinely exist in the population.

4.2 | Conclusion

In summary, we find no evidence to support a foundational role
of neonatal imitation in social cognition (Meltzoff, 2005, 2007).
Despite the fact that imitation is critical to human sociality and
cumulative culture (Legare & Nielsen, 2015; Whiten, McGuigan,
Marshall‐Pescini, & Hopper, 2009), the best available evidence sug‐
gests it is not present at birth (Keven & Akins, 2017; Oostenbroek et
al., 2016). And indeed, the current results suggest that even liberal
operationalizations of neonatal imitation (Meltzoff et al., 2017) show
no intra‐individual consistency across time points and no associa‐
tions with later‐developing social cognitive behaviours. Although we
cannot possibly prove absence, our comprehensive set of null results
provides the most compelling form of evidence against neonatal
imitation and the like me framework yet. Unless convincing contra‐
dictory evidence emerges, developmental psychologists must re‐
evaluate the innate and environmental factors that contribute to the
emergence of imitation and more complex social cognitive behaviour
(Heyes, 2016b; Jones, 2017; Oostenbroek et al., 2018).

A C K N O W L E D G E M E N T S

This research was funded by an Australian Research Council
Discovery Project grant (DP0985969) awarded to VS, MN & TS, and
a UQ Development Fellowship (UQFEL1832633) awarded to JR.
We sincerely thank the parents and infants who participated, and
Jennifer Magerl Fuller for her assistance with reliability coding.

C O N F L I C T O F I N T E R E S T

The authors hereby declare no conflicts of interest.

D ATA AVA I L A B I L I T Y S TAT E M E N T

The data that support the findings of this study are available as on‐
line supplementary material to the article, and on the Open Science
Framework at osf.io/s5f2t/ .

O R C I D

Jonathan Redshaw https://orcid.org/0000‐0002‐7729‐1577

Mark Nielsen https://orcid.org/0000‐0002‐0402‐8372

Virginia Slaughter https://orcid.org/0000‐0001‐9315‐1497

Siobhan Kennedy‐Costantini https://orcid.
org/0000‐0002‐6935‐1760

Jessica Crimston https://orcid.org/0000‐0003‐2093‐601X

Thomas Suddendorf https://orcid.org/0000‐0003‐3328‐7442

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Contents lists available at ScienceDirect

International Journal of Nursing Studies

journal homepage: www.elsevier.com/locate/ijns

Effect of non-nutritive sucking and sucrose alone and in combination for
repeated procedural pain in preterm infants: A randomized controlled trial

Haixia Gaoa,⁎, Mei Lib, Honglian Gaoc, Guihua Xua, Fang Lib, Jing Zhoub, Yunsu Zoub,
Honghua Jiangb

a School of Nursing, Nanjing University of Chinese Medicine, Nanjing, China
b Children’s Hospital of Nanjing Medical University, China
c Binzhou Medical University Hospital, Binzhou, China

A R

T

I C L E I N F O

Keywords:
Preterm infants
Pain
Analgesia
Sucrose
Non-nutritive sucking

A B S T R A C T

Background: Sucrose combined with non-nutritive sucking provided better pain relief than sucrose or non-nu-
tritive sucking alone in a single painful procedure. However, whether the combination of non-nutritive sucking
with sucrose could obtain a significant difference in analgesic effect of the repeated procedural pain than any
single intervention has not been established.
Objective: To compare the effect of non-nutritive sucking and sucrose alone and in combination of repeated
procedural pain in preterm infants.
Design: Randomized controlled trial.
Setting: A level III neonatal intensive care unit of a university hospital in China.
Method: Preterm infants born before 37 weeks of gestation were randomly assigned to four groups: routine care
group (routine comfort through gentle touch when infants cried; n = 21), non-nutritive sucking group (n = 22),
sucrose group (0.2 ml/kg of 20%; n = 21), sucrose (0.2 ml/kg of 20%) plus non-nutritive sucking group
(n = 22). Each preterm infant received three nonconsecutive routine heel sticks. Each heel stick included three
phases: baseline (the last 1 min of the

30

min without stimuli), blood collection, recovery (1 min after blood
collection). Three phases of 3 heel stick procedures were videotaped. Premature infant pain profile (PIPP) score,
heart rate, oxygen saturation and percentage of crying time were assessed by five independent evaluators who
were blinded to the purpose of the study at different phases across three heel sticks. Data were analyzed by
analysis of variance, with repeated measures at different evaluation phases of heel stick.
Results: 86 preterm infants completed the protocol. During the blood collection and recovery phases, combi-
nation group, had lower PIPP score (4.4 ± 1.5; 3.0 ± 0.8), lower heart rate (138.6 ± 7.9; 137.4 ± 4.7),
higher oxygen saturation (95.2 ± 1.6; 96.0 ± 1.2), and smaller percentage of crying time (11.5 ± 8.6;
4.6 ± 3.4), compared with the group has given non-nutritive sucking (9.3 ± 1.3, 6.8 ± 1.4; 154.2 ± 9.0,
148.0 ± 9.3; 92.9 ± 2.4, 94.1 ± 1.0; 44.2 ± 9.6,

31

.2 ± 10.5; respectively) or sucrose (10.1 ± 2.0,
7.4 ± 1.6; 151.6 ± 9.6, 147.9 ± 6.9; 93.5 ± 1.7, 94.5 ± 1.2; 53.8 ± 16.7, 35.2 ± 13.9; respectively) or
routine care (13.3 ± 1.6, 10.6 ± 1.9; 156.8 ± 7.2, 151.7 ± 7.9; 92.9 ± 2.1, 93.8 ± 1.6; 80.6 ± 7.6,
68.2 ± 9.9; respectively). Both non-nutritive sucking and sucrose were more effective in reducing preterm
infants’ PIPP score and percentage of crying time than routine care. There was no difference in PIPP score, heart
rate, oxygen saturation and percentage of crying time between the non-nutritive sucking and sucrose groups.
Conclusion: The combination of non-nutritive sucking with sucrose provided better pain relief during repeated
painful procedures than when non-nutritive sucking or sucrose was used alone. The effect of non-nutritive
sucking was similar to that of sucrose on repeated procedural pain.

What is already known about the topic?

• In an neonatal intensive care unit, preterm infants are exposed to
various painful stimuli to guarantee their survival. Repeated painful

stimuli in neonates may have short- and long-term consequences on
preterm infants physically and developmentally.

• Repeated exposure of preterm infants to opioid may have a detri-
mental effect on child neurodevelopmental outcomes.

https://doi.org/10.1016/j.ijnurstu.2018.04.006
Received 8 August 2017; Received in revised form 4 April 2018; Accepted 5 April 2018

⁎ Corresponding author at: School of Nursing, Nanjing University of Chinese Medicine, 138 Xianlin Road, Qixia District, Nanjing, Jiangsu Province 210023, China.
E-mail address: bpn456@163.com (H. Gao).

International Journal of Nursing Studies 83 (2018) 25–

33

0020-7489/ © 2018 Elsevier Ltd. All rights reserved.

T

http://www.sciencedirect.com/science/journal/00207489

https://www.elsevier.com/locate/ijns

https://doi.org/10.1016/j.ijnurstu.2018.04.006

https://doi.org/10.1016/j.ijnurstu.2018.04.006

mailto:bpn456@163.com

https://doi.org/10.1016/j.ijnurstu.2018.04.006

http://crossmark.crossref.org/dialog/?doi=10.1016/j.ijnurstu.2018.04.006&domain=pdf

• The use of sucrose alone or combined with non-nutritive sucking has
been the most frequently studied non-pharmacological intervention
method for single procedural pain. However, there have been no
studies comparing the effect of sucrose and non-nutritive sucking
alone and in combination with repeated procedural pain for preterm
infants.

What this paper adds

• The combination of sucrose and non-nutritive sucking shows better
efficacy for repeated procedural pain than their single use in pre-
term infants.

• The effect of non-nutritive sucking was similar to that of sucrose on
repeated procedural pain.

• When both sucrose and non-nutritive sucking can be provided in a
unit, the combination of them can be recommended as an analgesic
alternative for repeated pain exposure in preterm infants.

1. Introduction

Preterm birth is a significant global health problem. Survival rates
for preterm infants have increased markedly in recent decades due to
significant advances in neonatal intensive care. However, preterm in-
fants are exposed to various painful stimuli to guarantee their survival
during their stay in the neonatal intensive care unit (Chen et al., 2012;
Cruz et al., 2016; Jeong et al., 2014). Greater exposure to neonatal
pain-related stress has been found to be associated with poorer long-
term neurodevelopmental outcomes (Brummelte et al., 2012; Doesburg
et al., 2013; Lax et al., 2013; Skranes et al., 2012; Smith et al., 2011;
Vinall et al., 2013; Nuseir et al., 2015). Therefore, pharmacological or
non-pharmacological pain management must be required for preterm
infants in current neonatal practice.

Opioid analgesia is now widely used in preterm neonates. It is no-
teworthy that several recent studies have demonstrated repeated ex-
posure of preterm infants to opioid may have a detrimental effect on
child neurodevelopmental outcomes (Nuseir et al., 2015). For example,
the result from Nunes et al. study showed that repeated morphine ex-
posure during early life could have intermediate and long-term adverse
effects on the nociceptive responses, which included thermal hyper-
algesia and mechanical allodynia (Nunes et al., 2017). Kocek et al.
observed decreasing cognitive scores at 20 months corrected age in
extremely low birth weight infants who had cumulative opioid ex-
posure while in the neonatal intensive care unit (Kocek et al., 2016).
Furthermore, Ranger et al. reported that higher cumulative doses of
neonatal morphine were related with higher internalizing behaviours at
school age (Ranger et al., 2014). Thus, the adverse effects of opioid
analgesic are not negligible. It is very important to better understand
the potential risks and benefits of repeated opioid exposure in preterm
infants.

In contrast to pharmacological pain management, non-pharmaco-
logical pain management may have lower risk and greater ease of use
for preterm infants. Sucrose and non-nutritive sucking are the most
frequently studied non-pharmacological methods for reducing a single
procedural pain in preterm infants, and have been recommended by
national and international guidelines to alleviate procedural pain.
Furthermore, recent systematic reviews have addressed sucrose and
non-nutritive sucking as effective interventions to provide analgesia
and comfort for infants during painful procedures (Pillai Riddell et al.,
2015; Stevens et al., 2016). However, the evidence regarding the effi-
cacy and safety of repeated sucrose alone or combined with other non-
pharmacological interventions across repeated procedural pain for
neonates was limited (Gao et al., 2016). What’s more, there have been
no studies examining whether the combined intervention of sucrose and
non-nutritive sucking could obtain a significant difference in analgesic
effect on repeated procedural pain compared to any single intervention
for preterm infants, although several studies have reported that sucrose

combined with non-nutritive sucking provided better pain relief than
sucrose or non-nutritive sucking alone in a single painful procedure (Liu
et al., 2017; Naughton, 2013; Thakkar et al., 2016). It is a remarkable
fact that preterm newborns could learn and react to painful experiences
in the neonatal intensive care unit (Goubet et al., 2001), and the re-
peated exposure to painful experiences may reduce the pain threshold
and provoke hyperalgesia (Gibbins et al., 2008; Grunau, 2002). Thus, it
is vital to determine if the effects of the combination of sucrose and
non-nutritive sucking are better than their single-use on repeated pro-
cedural pain for preterm infants. In addition, animal studies have
shown that continuous consumption of sucrose can induce some be-
havioral and physiological responses similar to those elicited by drugs
of abuse like cocaine or amphetamine (Avena et al., 2008). Therefore,
the safety of repeated administration of sucrose or non-nutritive
sucking or their combination during painful procedures for preterm
infants needs to be examined.

Hence, the purpose of this study was to compare the efficacy and
safety of sucrose, non-nutritive sucking, and in combination with re-
peated procedural pain in preterm infants. We hypothesized that: (1)
Combined intervention of sucrose and non-nutritive sucking could be
more effective than any single intervention across repeated procedural
pain; (2) It is safe for preterm infants to use non-nutritive sucking or
sucrose alone or their combination repeatedly across repeated painful
procedures.

2. Methods

2.1. Design

This randomized controlled trial evaluated and compared the ef-
fectiveness of sucrose and non-nutritive sucking alone and in combi-
nation with repeated procedural pain across three nonconsecutive
routine heel sticks in preterm infants. Preterm infants were randomly
allocated before the heel stick by a research nurse using a random
computer-generated table to one of the four groups: routine care group,
non-nutritive sucking group, oral sucrose group, combined oral sucrose
and non-nutritive sucking group.

2.2. Setting and sample

Preterm infants were recruited by convenience sampling from a
level III neonatal intensive care unit (NICU) of a university hospital in
China from August 2015 to February 2016. Infants were included if
they met the following inclusion criteria: (1) Singleton born before 37
weeks of gestation, (2) Cared for in an incubator, (3) Anticipated re-
ceiving at least three routine heel sticks for capillary blood sampling
within two weeks after birth, (4) Hospitalized for the first time, (5)
Non-nutritive sucking rate at a minimum of 30 times/min (Blass and
Watt, 1999), and (6) Not scheduled to receive sedatives, muscle re-
laxants, or analgesic drugs 24 h before a study session. Infants were
excluded by these criteria: (1) Apgar Score of less than five at five
minutes, (2) Required mechanical ventilation, (3) Suffered from a
neurologic disorder, (4) Had congenital anomalies, (5) Undergone
surgery, (6) Born to substance-abusing mother, (7) Had hyperglycemia,
and (8) Nothing by mouth status for any reason.

To identify unforeseen problems and calculate the sample size, we
conducted a pilot study. Our pilot study showed the average Preterm
Infant Pain Profile (PIPP) score in 10 preterm infants during heel sticks
were 11.7 (SD = ± 5.5) in routine care group, 10.8 (SD = ± 4.2) in
non-nutritive sucking group, 9.0 (SD = ± 3.6) in oral sucrose group,
7.3 (SD = ± 2.0) in combined oral sucrose and non-nutritive sucking
group. To detect a significant difference in PIPP score among the four
groups, considering a power of 0.90, alpha of 0.05, and a 10% attrition
rate, a sample size of 22 was required in each group.

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33

26

2.3. Conditions in the four groups

All preterm infants, wearing only a diaper, were placed prone or in a
side-lying position in the incubator and remained undisturbed for
30 min before the heel stick procedure. The assigned treatment condi-
tion was administered by one researcher (the first author).

2.3.1. The condition in the routine care group
The preterm infant received only routine comfort through gentle

touch when he cried after the heel stick procedure. The effectiveness of
gentle touch as analgesia has been established in controlled clinical
trials (Bahman Bijari et al., 2012; Herrington and Chiodo, 2014). Thus,
for ethical reasons, preterm infants in the routine care group were given
gentle touch to alleviate procedural pain if they were crying.

2.3.2. The condition in the non-nutritive sucking group
The preterm infant was given a standard silicone newborn pacifier

to stimulate sucking in 2 min before, and throughout the recovery phase
of the heel stick.

2.3.3. The condition in the sucrose group
Sucrose 20% (0.2 ml/kg) was administrated to the preterm infant’s

mouth by 1 ml syringe without the needle in 2 min before the heel stick
procedure (Cignacco et al., 2012).

2.3.4. The condition in the combined oral sucrose and non-nutritive sucking
group

Sucrose 20% (0.2 ml/kg) was administrated to the preterm infant’s
mouth by 1 ml syringe without the needle in 2 min before the heel stick
procedure (Cignacco et al., 2012), and then a standard silicone new-
born pacifier was given to stimulate sucking until the recovery phase of
the heel stick.

2.4. Measures

Outcome variables included preterm infants’ procedural pain, phy-
siological response, behavioral response, and incidence of any adverse
events.

2.4.1. Measurement of procedural pain
The preterm infants’ procedural pain was measured by the

Premature Infant Pain Profile (PIPP) scale. The PIPP scale is a validated
seven-indicator scale for the assessment of procedural pain in pre-
mature and term infants (Stevens et al., 1996). It measures pain ac-
cording to two contextual indicators (gestational age and behavioral
state), two physiological indicators (heart rate and oxygen saturation),
and three behavioral indicators (brow bulge, eye squeeze, and nasola-
bial furrow). Each indicator is numerically scaled and scored on a 4-
point scale (0, 1, 2, 3), the total scores obtained for the seven indicators
range from 0 to 21. Higher total scores indicate greater pain response.
PIPP score < 6 means no pain, PIPP score ≥6 indicates pain, PIPP scores ≥12 signals moderate to severe pain. Validity and reliability of the PIPP instrument in infants at various gestational ages has previously been determined. For translation of PIPP scale from English into Chi- nese, the standard forward-backward procedure was applied. Transla- tion of the PIPP scale (English to Chinese) was independently per- formed by two professional translators, and then the temporary version was provided. The temporary version of the PIPP scale was backward translated into English by a native English translator who was blinded to the original instrument and not previously involved in the study. The back-translator and the expert committee evaluated the back-translated version, then the final version of the PIPP scale was provided.

Physiological indicators were continuously monitored by a pulse
oximeter set on the preterm infant’s foot and videotaped by one digital
camera (Canon sx30is). Behavioral indicators and behavioral state in-
dicator were continuously videotaped by another digital camera (Canon

sx30is) which was in close up focus on preterm infants’ face and al-
lowed for high-quality facial images. The two digital cameras (Canon
sx30is) were used synchronously by the research assistant. The beha-
vioral state indicator was evaluated using Prechtl’s categories of quiet
sleep or quiet awake or active sleep or active awake (Prechtl, 1974;
Prechtl and Beintema, 1977). Gestational age was determined ac-
cording to the electronic medical record. PIPP score was measured by
two trained evaluators (the second and third author) who were una-
ware of the purpose of the study during the blood collection phase and
recovery phase of each heel stick procedure. In order to ensure accep-
table inter-rater agreement, the two evaluators respectively assessed
PIPP score for each preterm infant at the blood collection phase of the
first heel stick, the inter-rater reliability among evaluators was 97%.
Intra-rater reliability was checked every three months, remaining more
than 90%.

2.4.2. Measurement of physiological response
The preterm infant’s physiological response to procedural pain was

assessed by the change in heart rate and oxygen saturation throughout
repeated heel sticks. Oxygen saturation and heart rate were con-
tinuously monitored by a pulse oximeter set on the preterm infant’s
foot, were manually recorded every 30 s by a nurse student, and then
were used to calculate the mean heart rate and oxygen saturation across
the baseline, blood collection and recovery phases of each heel stick
procedure.

2.4.3. Measurement of behavioral response
The preterm infant’s behavioral response to procedural pain was

measured by the percentage of crying time respectively in the blood
collection phase and recovery phase. Crying was defined as audible
vocalization that lasted five seconds or more (Ludington-Hoe et al.,
2005). Preterm infants’ voices were videotaped by a digital audio re-
corder (MODEL F97), and then two assessors calculated the percentage
of crying time through playing the tapes. To examine the inter-rater
agreement, the two assessors, respectively calculated the percentage of
crying time at the blood collection phase of the first heel stick, and the
inter-rater reliability between the assessors was 98%. Intra-rater relia-
bility was checked every three months, remaining more than 90%.

2.4.4. Measurement of incidence of adverse events
The safety of different interventions (non-nutritive sucking, sucrose,

and combined use of them) was assessed by the incidence of adverse
events during the study period. The adverse events included: (1)
Choking, coughing, vomiting, abdominal distension, oral infection,
necrotizing enterocolitis; (2) Sustained tachycardia (heart rate > 200
beats/min), bradycardia (heart rate < 80 beats/min), tachypnea (re- spiratory rate > 80 beats/min), dyspnea (respiratory rate < 20 beats/ min), or oxygen desaturation < 80% for > 15 s; (3) Hyperglycemia.
The adverse events were monitored and recorded by two trained re-
search nurses who were blind to the purpose of the study. A safety
committee was established prior to study commencement. If severe
adverse event such as choking or need for immediate medical inter-
vention (e.g., intubation or resuscitation) following the administration
of non-nutritive sucking, sucrose, or their combination occurred, the
trial would be stopped by the safety committee.

2.5. Procedures

The study protocol (Fig. 1) and consent forms were approved by the
institutional review board of the participating centre (approval number:
201507001-1). One research assistant screened admission log every
other day in the neonatal intensive care unit, and finalized potential
eligible infants, and informed the preterm infant’s parent of the purpose
of the study, and obtained parental oral consent. Participating preterm
infants were randomly assigned to the routine care group, non-nutritive
sucking group, oral sucrose group, or combined intervention group. The

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33

27

research assistant collected preterm infant’s characteristics, set pulse
oximeter on the preterm infant’s foot at about 5 min before the heel-
stick procedure. One researcher administered the intervention ac-
cording to the assigned condition, and then the experienced laboratory
employee performed heel stick in a standardized manner. One research
nurse videotaped preterm infant’s physiological indicators in 15 s be-
fore and 30 s after the heel stick, and in 15 s before and 30 s after the
end of the heel stick, and videotaped preterm infant’s facial actions in
30 s after the heel stick and 30 s after the end of the heel stick. The other
research nurse videotaped preterm infants’ voices occurring in the heel
stick procedure by a digital audio recorder. Because the timing of blood
sampling was determined by clinical needs, there were no fixed time
points for data collection. Most heel-stick events took place in the
morning and the intervals of them ranged from 3 to 48 h.

Each heel stick included three phases: (1) Baseline: 1 min of baseline
was collected at the end of the 30 min without stimuli. (2) Blood col-
lection: includes locating the site, disinfecting, sticking, squeezing,
applying adhesive bandage to the site for hemostasis, which lasted
about 60 s according to our previous observation. (3) Recovery: one
min after blood collection. The mean heart rate and oxygen saturation
during three phases of each heel stick, which displays in a pulse oxi-
meter, were collected by a nurse student (see Section 2.4.2). Preterm
infants’ PIPP score and percentage of crying time across the whole heel
stick were evaluated by four assessors (see Sections 2.4.1; 2.4.3). All
personnel was trained separately by the first author.

Study fidelity was established by the first author having separate
weekly meetings with the investigators, research assistant, nursing
student, and laboratory employees.

2.6. Data analysis

SPSS version 21.0 software package was used to conduct all the
descriptive and comparative statistical analysis. Data were presented as
means and standard deviations for continuous variables and frequencies
for categorical variables. Preterm infant’s characteristics such as birth
weight were evaluated for significant differences between the four
groups by one-way ANOVA test or Kruskal–Wallis analysis when the
assumption of normality test could not be found. For preterm infant’s
characteristics such as sex and the incidence of adverse events, Chi-
square test was used to determine whether there was significant dif-
ference between groups. For comparisons among the different phases,

measurement parameters (PIPP score, heart rate, oxygen saturation,
and the percentage of crying time) through the repeated heel sticks
were averaged separately. Repeated measurement analysis of variance
was performed to analyze both between- and within-groups difference
in three phases, followed by the Bonferroni post-hoc test. For all com-
parisons, a p- value of less than 0.05 was considered statistically sig-
nificant.

3. Results

There were 137 preterm infants were screened during the data
collection period. 103 were eligible for the criteria and were ap-
proached, and 91 agreed to participate. The reasons for refusals in-
cluded parents: did not want their infants to be videotaped due to their
small size (n = 7), refused anything extra done to their infants (n = 3),
were not interested (n = 2). Five infants dropped out of the study be-
cause they were discharged from the unit prior to the required heel
stick (Fig. 2). Preterm infant’s characteristics did not vary significantly
between infants whose parents declined to participate or dropped out of
the study (n = 17) and those who completed the study protocol
(n = 86).

3.1. Preterm infant characteristics

The characteristics of preterm infants completed the study protocol
are shown in Table 1. The sample included 86 preterm infants with a
mean gestational age of 31.7 ± 0.9 weeks. The majority was male
(60%) and born by cesarean delivery (71%). The preterm infants’ mean
birth weight was 17

32

.0 ± 267.9 g, mean Apgar score at 5 min was
8.8 ± 0.7, and they had 15.7 ± 2.4 previous invasive procedures. No
significant differences were noted among the four groups with regard to
the preterm infants’ characteristics.

3.2. Comparison of pain measurement parameters during the three repeated
heel sticks between groups

3.2.1. Between-group differences in pain measurement parameters during
the repeated three heel sticks

We compared the effectiveness of routine care, non-nutritive
sucking, sucrose and their combination in reducing procedural pain
during repeated heel sticks. The results of repeated measurement

Fig. 1. The study protocol.

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33

28

analysis of variance between groups revealed significant interactions of
all the pain measurement parameters except PIPP score between
treatment conditions and evaluation phases (PIPP score: F = 1.995,
p = 0.121; heart rate: F = 11.509, p < 0.0001; oxygen saturation: F = 2.886, p = 0.016; percentage of crying time: F = 72.517, p < 0.0001). Moreover, there was a significant main effect of the treatment groups for all the pain measurement parameters (PIPP score: F = 168.360, p < 0.0001; heart rate: F = 16.983, p < 0.0001; oxygen saturation: F = 10.165, p < 0.0001; percentage of crying time: F = 275.310, p < 0.0001). Post hoc analyses were performed to compare the treatment conditions with each other (Table 2). In the baseline phase, there was no significant difference in heart rate, oxygen saturation and percentage of crying time respectively between groups with each other. Thus, all pain parameters during the blood collection phase and the recovery phase were comparable between groups. During the blood collection phase and recovery phase, regarding PIPP score, the combination group was significantly lower than the other three groups, both the sucrose group and non-nutritive group were lower than the routine care group. Regarding heart rate and oxygen satura- tion, the combination group had achieved a significant improvement compared with the other three groups, while there were no significant difference among the routine care group, sucrose group and non-nu- tritive sucking group. Regarding the percentage of crying, the combi- nation group was significantly smallest, the routine care group was significantly biggest, the non-nutritive sucking group was significantly

similar to the sucrose group.

3.2.2. Within-group differences in pain measurement parameters during the
repeated three heel sticks

PIPP score, heart rate, oxygen saturation and percentage of crying
time showed similar patterns in the four treatment groups, which
changing significantly followed by the blood collection phase and re-
covering afterwards (Table 3). In the blood collection phase, the mean
PIPP scores at heel stick 1, 2, and 3 for the four treatment groups were
as follows: 13.2 ± 2.1, 13.1 ± 1.7, 13.4 ± 2.6 respectively in the
control group, 9.9 ± 2.4, 8.5 ± 2.7, 9.5 ± 2.6 respectively in the
non-nutritive sucking group, 11.1 ± 2.1, 10.1 ± 3.9, 8.9 ± 4.0 re-
spectively in the sucrose group, 4.2 ± 2.1, 4.8 ± 2.9, 4.4 ± 2.0 re-
spectively in the combination group. In the recovery phase, the mean
PIPP score at heel stick 1, 2, and 3 for the four treatment groups were as
follows: 10.5 ± 2.5, 10.7 ± 1.9, 10.5 ± 2.5 respectively in the con-
trol group, 7.6 ± 2.2, 6.0 ± 2.6, 6.9 ± 2.6 respectively in the non-
nutritive sucking group, 7.9 ± 1.8, 7.3 ± 3.3, 7.1 ± 2.7 respectively
in the sucrose group, 3.1 ± 2.0, 3.1 ± 1.7, 2.8 ± 1.0 respectively in
the combination group. The dada above showed that preterm infants in
the combination group didn’t feel pain at each heel stick, infants in the
sucrose and non-nutritive sucking group felt mild pain, while infants in
the control group felt moderate to severe pain.

Within-group comparison showed that significant differences in
heart rate and oxygen saturation between the baseline phase and

Assessed for eligibility (n=137)

Excluded (n =46)
Mee ng exclusion criteria (n =34)
Refused to par cipate (n = 12)

n =91
Randomly allocated

Allocated to rou ne care
group (n=23)

In all three nonconsecu ve
heel s cks, infants received
allocated incubator
condi on
Heel s ck 1 (n=23)
Heel s ck 2 (n=23)
Heel s ck 3 (n=21) :
2 infants discharged prior to
the third heel s ck

Allocated to nonnutri ve
sucking group (n=23)

In all three nonconsecu ve
heel s cks, infants received
allocated nonnutri ve
sucking
Heel s ck 1 (n=23)
Heel s ck 2 (n=23)
Heel s ck 3 (n=22) :
1 infant discharged prior to
the third heel s ck

Allocated to sucrose group
(n=23)

In all three nonconsecu ve
heel s cks, infants received
allocated oral sucrose
Heel s ck 1 (n=23)
Heel s ck 2 (n=23)
Heel s ck 3 (n=21):
2 infants discharged prior
to third heel s ck

Allocated to combina on
group

(n=22)

In all three nonconsecu ve
heel s cks, infants received
allocated combined
treatment
Heel s ck 1 (n=22)
Heel s ck 2 (n=22)
Heel s ck 3 (n=22)

Analyzed
Repeated three heel s cks

(n=21)

Analyzed
Repeated three heel s cks
(n=22)
Analyzed
Repeated three heel s cks
(n=21)
Analyzed
Repeated three heel s cks
(n=22)

Fig. 2. Flow diagram of the recruitment and randomization process.

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33

29

recovery phase approached for all groups except the combination
group. For the routine care group, sucrose group, non-nutritive sucking
group, heart rate remained significantly quicker in recovery phase than
in baseline phase, oxygen saturation remained significantly lower in
recovery phase than in baseline phase. However, both heart rate and
oxygen saturation in the combination group remained steady across all
phases. In addition, compared to the other three group infants, com-
bination group infants’ mean percentage of crying time in the recovery
phase was near to the baseline phase percentage, although significant
differences occurred in all groups between the baseline phase and the
recovery phase.

3.3. Comparison of incidence of adverse events in the study period between
groups

The incidence of adverse events in the study period was as follows:
three preterm infants vomited (1 in the combination group, 1 in the
routine care group, 1 in the non-nutritive sucking group); two preterm
infants had abdominal distension (1 in the combination group, 1 in the
routine care group). The Chi-square test exhibited that there were no
statistically significant differences between groups in the incidence of
adverse events (vomit: χ2 = 1.006, p = 0.800; abdominal distension:
χ2 = 2.050, p = 0.562).

Table 1
Comparisons of characteristics of preterm infants between groups.

Variable Routine care group Nonnutritive sucking group Sucrose group Combination group P value

Gestational age, week
30–32a 21 16 17 18
33–34a 0 6 4 4 0.102

Gender
Malea 13 15 10 14
Femalea 8 7 11 8 0.550

Method of delivery
Vaginal deliverya 5 9 6 5
Cesarean deliverya 16 13 15 17 0.530

Birth weight, gb 1682.7 ± 200.2 1767.3 ± 302.7 1780.8 ± 304.6 1697.1 ± 254.7 0.547
Gestational age at birth, weekb 31.3 ± 0.6 31.9 ± 1.1 31.7 ± 0.9 32.0 ± 0.8 0.068
5 min Apgar scoreb 8.7 ± 0.6 8.8 ± 0.6 8.9 ± 0.7 8.8 ± 0.8 0.846

Postnatal days
Heel stick 1b 3.2 ± 0.6 3.5 ± 0.6 3.4 ± 0.6 3.2 ± 0.7 0.262
Heel stick 2b 5.4 ± 0.6 5.4 ± 0.7 5.3 ± 0.6 5.6 ± 0.7 0.580
Heel stick 3b 9.5 ± 1.0 8.2 ± 2.0 8.5 ± 1.4 9.0 ± 2.9 0.179

Previous invasive proceduresb 15.7 ± 2.2 14.9 ± 2.9 16.1 ± 2.0 16.0 ± 2.3 0.359

Duration of blood collection phase, seconds
Heel stick 1b 61.9 ± 12.5 61.5 ± 9.3 59.8 ± 9.7 57.7 ± 9.9 0.544
Heel stick 2b 65.5 ± 9.6 62.7 ± 12.8 66.9 ± 18.2 61.6 ± 13.7 0.573
Heel stick 3b 64.1 ± 9.2 58.7 ± 11.1 63.2 ± 9.0 59.1 ± 13.2 0.240

Behavioral state score at baseline phase
Heel stick 1b 0.9 ± 0.7 0.8 ± 0.7 0.8 ± 0.7 0.9 ± 0.9 0.893
Heel stick 2b 1.1 ± 0.7 0.7 ± 0.6 0.8 ± 0.7 0.9 ± 0.6 0.216
Heel stick 3b 0.4 ± 0.5 0.4 ± 0.5 0.4 ± 0.5 0.3 ± 0.5 0.938

a n.
b Mean (standard deviation).

Table 2
Between-group comparison of pain measurement parameters during the repeated three heel sticks.

RC group −NS group RC group −S group RC group −C group NS group-S group NS group- C group S group- C group

PIPP score
Blood collectiona P < 0.0001 P < 0.0001 P < 0.0001 0.694 P < 0.0001 P < 0.0001 Recoverya P < 0.0001 P < 0.0001 P < 0.0001 1.000 P < 0.0001 P < 0.0001

Heat rate (beats/min)
Baselinea 0.203 1.000 1.000 0.283 1.000 1.000
Blood collectiona 1.000 0.305 P < 0.0001 1.000 P < 0.0001 P < 0.0001 Recoverya 0.621 0.610 P < 0.0001 1.000 P < 0.0001 P < 0.0001

Oxygen saturation (%)
Baselinea 1.000 1.000 1.000 1.000 1.000 1.000
Blood collectiona 1.000 1.000 0.002 1.000 0.002 0.035
Recoverya 1.000 0.602 P < 0.0001 1.000 P < 0.0001 0.001

Percentage of crying time (%)
Baselinea – – – – – –
Blood collectiona P < 0.0001 P < 0.0001 P < 0.0001 0.035 P < 0.0001 P < 0.0001 Recoverya P < 0.0001 P < 0.0001 P < 0.0001 1.000 P < 0.0001 P < 0.0001

Note: Data are listed as mean ± SD. PIPP: premature infant pain profile; RC: Routine care; NS: Nonnutritive sucking; S: Sucrose; C: Combination of nonnutritive
sucking and sucrose.

a Bonferroni correction for multiples comparisons.

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33
30

4. Discussion

Studies have demonstrated that preterm infants could mount both
physiological and behavioral responses to painful stimuli. Repeated
painful stimuli in neonates may have short- and long-term con-
sequences on preterm infants physically and developmentally.
Therefore, it is imperative to provide relief for preterm infants during
repeated painful procedures. Sucrose and non-nutritive sucking have
been established for managing a single procedural pain. However, to
our knowledge, this is the first study to examine the analgesic effect of
non-nutritive sucking across repeated painful procedure, and to de-
termine if the combined intervention of sucrose and non-nutritive
sucking could obtain a significant difference in analgesic effect on re-
peated procedural pain compared to any single intervention for preterm
infants.

Our study represents that both sucrose and non-nutritive sucking
could reduce preterm infants’ PIPP score and percentage of crying time,
but neither of them could decrease preterm infants’ physiological re-
sponse during the repeated heel sticks, which is consistent with the
previous studies (Table 2). Gaspardo et al. study found that preterm
neonates in the sucrose group had significantly fewer facial actions and
crying than the control group, but no statistical difference in the per-
centage of neonates with a heart rate of > 160 beats/min between
groups during repeated procedural pain (Gaspardo et al., 2008).
Cignacco et al. study, using the Bernese Pain Scale for Neonates to
measure preterm infants’ pain response caused by five heel sticks, re-
ported that sucrose was significantly more effective in relieving re-
peated procedural pain than facilitated tucking (Cignacco et al., 2012).
Boyer et al. study reported routine sucrose alone had no effect on the
change in cortisol level and variability of heart rate which resulted from
repeated procedural pain for preterm infants (Boyer et al., 2004).
However, these previous studies differed from our study in the fol-
lowing respects: (1) The method of evaluating procedural pain: we
assessed preterm infants’ pain not only using Preterm Infant Pain

Profile, but also using physiological and behavioral response, whereas
other studies only used a pain scale, or physiological and behavioral
response to measure preterm infants’ pain. (2) The methodological as-
pect of study design: enough sample size used in our study, while small
sample size in Gaspardo et al. study and moderate attrition rates in
Boyer et al. study. These results suggest that clinicians in Neonatal
Intensive Care Unit can provide non-nutritive sucking and sucrose to
reduce preterm infants’ repeated procedural pain.

It is worthwhile to note that we could not find any study that
compared the analgesic effects of non-nutritive sucking in preterm in-
fants to the analgesic effects of sucrose during repeated painful proce-
dure. Our findings indicated that the analgesic effects of non-nutritive
sucking in preterm infants was similar to that of sucrose during re-
peated painful procedure. These study results provide an alternative to
sucrose to relieve preterm infants’ repeated procedural pain.

However, we consider that either sucrose or non-nutritive sucking is
not perfect analgesics, because both of them couldn’t reduce preterm
infants’ physiological response following by repeated procedural pain.
This present study demonstrated that the PIPP score, percentage of
crying time, and magnitude of physiological response following by re-
peated painful procedures were lowest in the combination of sucrose
and non-nutritive sucking group, which indicated that sucrose plus non-
nutritive sucking produced the most efficacious means of pain reduc-
tion for repeated painful procedures. To date, only one study has
evaluated the effect of sucrose combined with non-nutritive sucking on
repeated procedural pain for preterm infants, which reported PIPP
score was significantly lower in the sucrose with pacifier intervention
group compared with the standard care group (Stevens et al., 2005). Yet
in Stevens et al. study, the Premature Infant Pain Profile (PIPP) scores
were not available on all preterm infants at all fixed data collection
points due to some of the infants did not receive routine painful pro-
cedure at each time point, which may affect the reliability of the con-
clusion. The specific contribution of our study was that we analyzed
exclusively sucrose in comparison to nonnutritive sucking, their

Table 3
Within-group comparison of pain measurement parameters during the repeated three heel sticks.

Baselinea Blood collectiona Recoverya P (one-way RM ANOVA)

PIPP score
Routine care group – 13.3 ± 1.6 10.6 ± 1.9 P < 0.0001 Nonnutritive sucking group – 9.3 ± 1.3 6.8 ± 1.4 P < 0.0001 Sucrose group – 10.1 ± 2.0 7.4 ± 1.6 P < 0.0001 Combination group – 4.4 ± 1.5 3.0 ± 0.8 P < 0.0001

Heat rate (beats/min)
Routine care group 133.1 ± 5.8b,c 156.8 ± 7.2 151.7 ± 7.9 P < 0.0001 Nonnutritive sucking group 137.0 ± 5.8b,d 154.2 ± 9.0 148.0 ± 9.3 P < 0.0001 Sucrose group 133.4 ± 5.6b,e 151.6 ± 9.6 147.9 ± 6.9 P < 0.0001 Combination group 134.7 ± 6.1b,f 138.6 ± 7.9 137.4 ± 4.7 0.080

Oxygen saturation (%)
Routine care group 95.7 ± 1.5b,c 92.9 ± 2.1 93.8 ± 1.6 P < 0.0001 Nonnutritive sucking group 95.8 ± 0.9b,d 92.9 ± 2.4 94.1 ± 1.0 P < 0.0001 Sucrose group 96.1 ± 1.5b,e 93.5 ± 1.7 94.5 ± 1.2 P < 0.0001 Combination group 96.1 ± 1.2b,f 95.2 ± 1.6 96.0 ± 1.2 0.024

Percentage of crying time (%)
Routine care group 0b,c 80.6 ± 7.6 68.2 ± 9.9 P < 0.0001 Nonnutritive sucking group 0b,d 44.2 ± 9.6 31.2 ± 10.5 P < 0.0001 Sucrose group 0b,e 53.8 ± 16.7 35.2 ± 13.9 P < 0.0001 Combination group 0b,g 11.5 ± 8.6 4.6 ± 3.4 P < 0.0001

Note: Data are listed as mean ± SD. PIPP: premature infant pain profile.
a Mean (standard deviation).
b Bonferroni correction for multiples comparisons.
c Significant difference when compared with recovery–Routine Care group (P < 0.05). d Significant difference when compared with recovery–Nonnutritive sucking group (P < 0.05). e Significant difference when compared with recovery–Sucrose group (P < 0.05). f No significant difference when compared with recovery–Combination group (P > 0.05).
g Significant difference when compared with recovery–Combination group (P < 0.05).

H. Gao et al. International Journal of Nursing Studies 83 (2018) 25–33
31

combination and routine care, whereas Stevens et al. used combined
sucrose plus pacifier in the same group in comparison with pacifier plus
water and standard care.

Furthermore, our results found that preterm infants’ mean heart rate
and oxygen saturation in the recovery phase had been back to baseline
phase, and the percentage of crying time in the recovery phase had
been near to baseline phase in the combination group (Table 3). The
ability to recover quickly is a sign of ability to maintain homeostasis, a
major task that the very preterm neonate must accomplish in order to
grow and develop (Moore and Anderson, 2007). In summary, the
combination of sucrose and non-nutritive sucking could have a better
analgesic effect on repeated procedural pain than both methods sepa-
rately. The plausible reason could be the multimodal stimulation that
the preterm infant experiences when sucrose and non-nutritive sucking
were administered together. These findings can guide nurses and other
clinicians to combine sucrose and non-nutritive sucking to minimize
preterm infants’ repeated procedural pain.

Establishing the safety of sucrose, non-nutritive sucking and their
combination for repeated procedural pain might be the first priority.
Our study demonstrated no significant difference in the incidence of
adverse events between different groups. Thus, it indicates sucrose,
non-nutritive sucking or their combination had no short-term side ef-
fects on the health status of the preterm infants. Other authors have
reported the similar results (Banga et al., 2016; Gaspardo et al., 2008;
Stevens et al., 2005; Taddio et al., 2008).

The strengths of the present study included: (1) It was a randomized
controlled trial with sufficient sample size. (2) Multiple outcome vari-
ables (PIPP score, behavioral and physiological response) were used to
evaluate the effect of sucrose, non-nutritive sucking, and in combina-
tion on repeated procedural pain, which not only provided a detailed
analysis over the entire sampling period, but also examined their ef-
fectiveness on the overall changes in the summary scores. (3)
Videotaping, evaluating, offering treatment conditions were performed
by different persons respectively, which enhanced the internal validity
of the study results.

Despite its strengths, the study had some limitations: (1) Preterm
infants enrolled in the study were stable and aged more than 30 weeks.
Thus, its results can not be generalized to the unstable and extremely
preterm infants. (2) The study only focused on the analgesic effects of
sucrose, non-nutritive sucking and their combination on repeated heel
sticks, yet whether they could have the same analgesic effects on other
repeated procedural pain as on repeated heel sticks had not been de-
termined by the study. (3) The study examined the short-term safety of
repeated sucrose, non-nutritive sucking and their combination for
preterm infants, while the long-term impact of repeatedly offering a
pacifier or sucrose or in combination during repeated procedural pain
on preterm infants’ readiness for breastfeeding, weight gain and even
neurobehavioral development had not been discussed. (4) The
Premature Infant Pain Profile especially its grimacing indicator evalu-
ating procedure was impossible to be completely blind, because non-
nutritive sucking had to be continued until 1 min after the painful
procedure. (5) The control condition for our study was routine care,
which might have led to unnecessary pain for preterm infants assigned
to this condition, although this limitation was minimized by offering
preterm infants in this condition gentle touch.

The implications for future research and practice may be as follows:
Firstly, future studies should include the preterm infants with gesta-
tional age less than 30 weeks and being medically unstable, and then
examine and compare the efficacy and safety of sucrose, non-nutritive
sucking, and their combination for repeated procedural pain in them.
Secondly, researchers can further evaluate the effects of sucrose, non-
nutritive sucking, and their combination on different types of repeated
procedural pain except heel stick pain in preterm infants. Thirdly,
further randomized controlled trials are needed to examine the long-
term impact of repeatedly offering a pacifier or sucrose or their com-
bination in repeated procedural pain on preterm infants during their

stay in neonatal intensive care unit.

5. Conclusion

Both sucrose and non-nutritive sucking have a good analgesic effect
for preterm infants on repeated procedural pain, but a combination of
the two interventions shows better efficacy. Our results provide evi-
dence supporting clinicians’ incorporation of the combined use of su-
crose and non-nutritive sucking into clinical practice while preterm
infants undergo repeated painful procedures. Thus, when both sucrose
and non-nutritive sucking can be provided in a unit, the combination of
them could be recommended as an analgesic alternative for repeated
pain exposure in preterm infants.

Acknowledgments

We acknowledge the financial contribution of National Natural
Science Foundation of China (81703246), the Preponderant Discipline
Project of Universities in Jiangsu Province, Nursing Science Open Fund
of Nanjing University of Chinese Medicine (YSHL2016-018), Top-notch
Academic Programs Project of Jiangsu Higher Education Institutions
(PPZY2015C258) and Project of nursing science in Nanjing University
of Chinese Medicine (NZYHLXPPJG2017-54).

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• Effect of non-nutritive sucking and sucrose alone and in combination for repeated procedural pain in preterm infants: A randomized controlled trial

What is already known about the topic?
What this paper adds
Introduction
Methods
Design
Setting and sample
Conditions in the four groups
The condition in the routine care group
The condition in the non-nutritive sucking group
The condition in the sucrose group
The condition in the combined oral sucrose and non-nutritive sucking group
Measures
Measurement of procedural pain
Measurement of physiological response
Measurement of behavioral response
Measurement of incidence of adverse events
Procedures
Data analysis
Results
Preterm infant characteristics
Comparison of pain measurement parameters during the three repeated heel sticks between groups
Between-group differences in pain measurement parameters during the repeated three heel sticks
Within-group differences in pain measurement parameters during the repeated three heel sticks
Comparison of incidence of adverse events in the study period between groups
Discussion
Conclusion
Acknowledgments
References

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Psychological Science

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The online version of this article can be found at:

DOI: 10.1177/0956797609360758
2010 21: 343 originally published online 29 January 2010Psychological Science

Krista Byers-Heinlein, Tracey C. Burns and Janet F. Werker

The Roots of Bilingualism in Newborns

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The human affinity for language begins at or before birth.
Neonates show many perceptual sensitivities that are impor-
tant for language acquisition (Gervain & Werker, 2008). In
monolingual acquisition, infants must detect and learn the
regularities that characterize a single language. In bilingual
acquisition, infants must simultaneously detect and learn the
regularities of each of two languages. This requires recogniz-
ing both languages as native while continuing to discriminate
them. What tools do neonates have available to negotiate a
bilingual environment?

To break into two languages and bootstrap acquisition, one
source of information that bilingual infants might use is rhyth-
micity (Mehler, Dupoux, Nazzi, & Dehaene-Lambertz, 1996).
Traditionally, the world’s languages have been classified into
three rhythmic classes: stress-timed (e.g., Dutch), syllable-
timed (e.g., French), and mora-timed (e.g., Japanese). Ramus,
Nespor, and Mehler (1999) identified two acoustic dimensions
that correlate with rhythmic-class distinctions: the standard
deviation of the duration of consonantal intervals within each
sentence (ΔC) and the percentage of vocalic intervals (i.e.,
vowels) within each sentence (%V; see Grabe & Low, 2002,
for an alternate measurement scheme). Studies have revealed
that although categorical divisions are useful, languages fall
somewhat continuously along these dimensions (see Fig. 1).

Research has demonstrated the importance of rhythmicity
in early language processing. Newborn infants exposed
to only a single language prenatally show greater interest in
their native language than in an unfamiliar language from a

different rhythmic class (Mehler et al., 1988; Moon, Cooper,
& Fifer, 1993). Preferential attention to the native language
shows an early effect of learning on language processing,
either during prenatal development or immediately after birth.1
Studies also show that monolingual neonates can discriminate
two languages from different rhythmic classes even if both are
unfamiliar but typically fail at discriminating languages within
the same class (Mehler et al., 1988; Nazzi, Bertoncini, &
Mehler, 1998; Ramus, 2002; Ramus, Hauser, Miller, Morris,
& Mehler, 2000). These findings are understood as evidence
that although language preference is learned through experi-
ence, the ability to discriminate languages from different
rhythmic classes is an evolutionarily deep perceptual bias that
operates independently of learning (Ramus et al., 2000).
Moreover, it has been asserted that the ability to discriminate
languages is foundational to bilingual acquisition (Nazzi et al.,
1998). No studies to date, however, have actually tested either
language preference or language discrimination in neonates
with prenatal bilingual exposure. Here, we provide the first
empirical test of the hypothesis that the same initial perceptual
biases and early learning mechanisms that underlie monolin-
gual acquisition operate in the bilingual neonate to propel
bilingual acquisition.

Corresponding Author:
Janet F. Werker, Department of Psychology, University of British Columbia,
2136 West Mall, Vancouver, British Columbia, Canada V6T 1Z4
E-mail: jwerker@psych.ubc.ca

The Roots of Bilingualism in Newborns

Krista Byers-Heinlein1, Tracey C. Burns2, and Janet F. Werker1
1Department of Psychology, University of British Columbia, and 2Organisation for Economic Co-operation
and Development, Paris, France

Abstract

The first steps toward bilingual language acquisition have already begun at birth. When tested on their preference for English
versus Tagalog, newborns whose mothers spoke only English during pregnancy showed a robust preference for English. In
contrast, newborns whose mothers spoke both English and Tagalog regularly during pregnancy showed equal preference for
both languages. A group of newborns whose mothers had spoken both Chinese and English showed an intermediate pattern
of preference for Tagalog over English. Preference for two languages does not suggest confusion between them, however.
Study 2 showed that both English monolingual newborns and Tagalog-English bilingual newborns could discriminate English
from Tagalog. The same perceptual and learning mechanisms that support acquisition in a monolingual environment thus also
naturally support bilingual acquisition.

Keywords

newborns, bilingualism, language discrimination, perceptual learning

Received 11/26/08; Revision accepted 7/26/09

Research Report

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344 Byers-Heinlein et al.

To test this hypothesis, we explored the earliest foundations
of two capacities crucial to bilingual acquisition. We com-
pared preference for (Study 1) and discrimination of (Study 2)
English and Tagalog (languages from different rhythmic
classes) in bilingual newborns, whose mothers spoke both lan-
guages regularly during pregnancy, with those of monolingual
newborns, whose mothers spoke only English during preg-
nancy. Although it could be the case that infants only gradually
develop the skills to negotiate a bilingual environment (Arn-
berg & Arnberg, 1985), our results demonstrate that from
birth, the recognition and discrimination skills that support
monolingual acquisition also support bilingual acquisition.

Study 1a
No previous studies have investigated language preference
in bilingual neonates. Although monolingual neonates orient
more toward their native language than toward an unfamiliar
language in preferential listening tasks, for optimal learning,
infants growing up bilingual should orient to both of their
native languages. To investigate the impact of prenatal

experience on language preference at birth, we tested newborn
infants for their preference for syllable-timed Tagalog (a major
language of the Philippines; Bird, Fais, & Werker, 2005), rela-
tive to English, a stress-timed language (Ramus et al., 1999;
see Fig. 1). Two groups of neonates were tested: English mono-
linguals (whose mothers spoke only English during pregnancy)
and Tagalog-English bilinguals (whose mothers spoke both
English and Tagalog regularly during pregnancy). We expected
that monolinguals would be significantly less interested in
Tagalog than in English, as Tagalog was unfamiliar (Mehler
et al., 1988; Moon et al., 1993). The previously untested pre-
diction was that bilinguals would be interested in both of their
native languages.

Method

Testing was conducted at a maternity hospital in Vancouver,
British Columbia, Canada, a multicultural city where English
is the majority language but many other languages are widely
used. Thirty newborn infants (0–5 days old), half from mono-
lingual English backgrounds and half from bilingual

English (stress)

0.060

0.05

5

0.050

∆
C 0.045

0.040

0.035

0.0

30

35 40 45 50
%V

55 60 65

Dutch (stress)

Tagalog (syllable)

French (syllable)
Mandarin (syllable)

Cantonese (syllable)

Japanese (mora)

Experimental Languages Example Languages

Fig. 1. Mean location of languages in the (%V, ΔC) plane. ΔC represents the standard deviation of the
duration of consonantal intervals within each sentence; %V represents the percentage of vocalic intervals
(i.e., vowels) within each sentence. Measurements for English and the languages used as rhythmic-class
examples in this article are from Ramus, Nespor, and Mehler (1999). Measurements for Tagalog are from
Bird, Fais, and Werker (2005); those for Cantonese are from (Mok, in press); and those for Mandarin are
averaged from Mok (in press) and Lin and Wang (2007).

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The Roots of Bilingualism in Newborns 345

Tagalog-English backgrounds (henceforth called Tagalog
bilinguals) completed the study.2 Mothers of Tagalog bilin-
guals reported speaking each language 30% to 70% of the
time.

Stimuli were sentences matched for pitch, duration, and
number of syllables. They were recorded from native English
and native Tagalog speakers and low-pass filtered to a cutoff
of 400 Hz, to remove surface segmental cues while preserving
rhythmicity. Infants were tested using a high-amplitude sucking-
preference procedure, which capitalizes on newborns’ sucking
reflex. Newborns sucked on a rubber nipple and were played a
sentence contingently on producing a suck in the upper 80% of
their sucking range, as calculated by the computer during an
initial silent baseline minute. Infants were presented with 10
min of speech, alternating each minute between English and
Tagalog. Four different English and four different Tagalog
sentences were used, recorded from three native English and
three native Tagalog speakers. The order of the two languages
was counterbalanced. To assess preference, the number of
high-amplitude sucks produced during Tagalog minutes ver-
sus English minutes was compared.

Results

A preference score was computed for each infant, as the differ-
ence in the average number of high-amplitude sucks produced
during Tagalog minutes minus those produced during English
minutes (see Fig. 2). One English monolingual and one Taga-
log bilingual outlier, whose preference scores were more than
2 SDs from their group’s mean, were removed.3 Preliminary
analyses suggested heterogeneity among group variances,
Levene’s F(1, 26) = 4.87, p =.036; therefore, subsequent anal-
yses used Welch’s correction. This correction often yields
noninteger estimates of degrees of freedom.

To determine whether the groups could be characterized
as having significant absolute preference for one language
over the other, two-tailed one-sample t tests were conducted,
comparing infants’ preference scores with zero. Monolingual
English infants were significantly less interested in Tagalog
than in English, t(13) = –3.44, p = .004. Tagalog bilinguals
did not show a significant preference for either language,
t(13) = 1.76, p = .103. To directly compare the performance
of the two groups, a planned directional comparison of

Tagalog
Bilinguals

Tagalog Bilinguals

Chinese
Bilinguals

Chinese Bilinguals

Englis

h

Monolinguals

English Monolinguals

20

15

Ta
ga

lo
g

P
re

fe
re

nc
e

S
co

re
E

ng
lis

h

p > .

10

p > .10

p = .004

p = .046

p = .035

p = .003

10
5
0

−5

−10

−15

Fig. 2. Individual preference scores (colored symbols) and group means (open symbols) for monolingual
English, Chinese-English bilingual, and Tagalog-English bilingual infants in Studies 1a and 1b. Preference
scores were calculated by subtracting the average number of high-amplitude sucks produced during English
minutes from the average number of high-amplitude sucks produced during Tagalog minutes. Significance
values for between-group comparisons are shown with brackets; significance values adjacent to group
means are for comparisons to zero. Error bars represent standard errors of the mean.

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346 Byers-Heinlein et al.

infants’ difference scores was conducted. Relative to their
interest in English, English monolinguals had significantly
less interest in Tagalog than did Tagalog bilinguals, t(18.8) =
3.08, p = .003.

Discussion
The results of this study demonstrate that prenatal bilingual
exposure affects infants’ preferences. English monolingual
newborns were less interested in Tagalog than in English, but
Tagalog bilinguals were similarly interested in their two native
languages. Bilinguals’ attention to both languages is consistent
with their having learned about two languages prenatally.

A counterexplanation consistent with these data would be
that Tagalog bilinguals recognized neither language as native.
Because bilinguals’ time is divided between two languages,
their experience with each language may have been insufficient
to have an effect on perception. The insufficient-experience
explanation leads to a clear prediction: Regardless of the par-
ticular native languages, any group of bilingual newborns will
show the same pattern of language preference. Conversely,
evidence that two groups of bilingual newborns demonstrate
different patterns of preference would support the position that
bilingual newborns have had sufficient experience to learn
about each language prenatally.

Study 1b
To directly test the insufficient-experience explanation, we sought
a second group of bilingual newborns to evaluate on their pref-
erence for Tagalog versus English. Because English was a
common language to the two groups tested in Study 1a, it was
necessary to find another group of bilinguals who had heard
English prenatally. Chinese-English bilinguals were such a
group that was available in our community.

Similarities and differences between Tagalog and Chinese
make Chinese-English bilinguals an interesting test case. Both
Chinese (Mandarin and Cantonese) and Tagalog have been
classified within the larger typological category of syllable-
timed languages (Bird et al., 2005; Lin & Wang, 2007; Mok, in
press). But as shown in Figure 1, Tagalog and Chinese show
rhythmical differences, and there is evidence that 4-month-old
bilingual infants are sensitive to intraclass differences (Bosch
& Sebastián-Gallés, 1997, 2001). Further, Chinese is charac-
terized by lexical tone (perceptible by adults even in filtered
speech; Fu, Zeng, Shannon, & Soli, 1998), whereas Tagalog is
not. Overall, we expected that Tagalog would be somewhat,
although not completely, familiar to the Chinese bilingual
infants. Thus, because Tagalog is neither completely novel (as
it is to English monolinguals) nor completely familiar (as it is
to Tagalog bilinguals), we predicted that Chinese bilingual
infants would show a preference intermediate to the prefer-
ence shown by the two other groups and statistically different
from each of them.

Method

Fourteen neonates whose mothers spoke both English and Chi-
nese (Cantonese, Mandarin, or in two cases both) regularly dur-
ing pregnancy were tested for their preference for Tagalog
versus English, in a procedure identical to that used in Study 1a.

Results and discussion
The results demonstrated that Chinese bilingual neonates did not
show an outright preference for either English or Tagalog, t(13) =
–0.49, p = .63. As predicted, however, these infants showed a
pattern of preference distinct from that of either English mono-
linguals or Tagalog bilinguals (see Fig. 1). Planned directional
comparisons showed that their interest in Tagalog relative to
English was greater than that of English monolinguals, t(25.5) =
1.89, p = .035, but less than that of Tagalog bilinguals, t(20.4) =
1.77, p = .046. Therefore, relative to their interest in English,
Chinese bilingual infants were less interested in Tagalog than
were Tagalog bilingual infants (for whom Tagalog was native)
but were more interested in Tagalog than were English monolin-
gual infants (for whom Tagalog shares few similarities with the
native language). These results demonstrate that bilingual new-
borns’ language preference is affected by the specific languages
they heard before birth, indicating that bilingual newborns have
indeed learned about both their native languages prenatally.

Study 2
Study 1 demonstrated that by birth, bilingual neonates have
already learned about their two languages and, like monolin-
guals, use this information to direct their attention. However, to
successfully acquire the structures of two languages, bilingual
infants must also separate and discriminate these languages. A
possible interpretation of the results of Study 1a is that experi-
ence with two languages can overwrite the perceptual biases
that facilitate language discrimination and that Tagalog bilin-
gual neonates have no preference because they lump English
and Tagalog into a broad class of familiar language sounds.

Previous research supports the idea that any newborn can dis-
criminate two languages as long as the languages are from differ-
ent rhythmic classes (Mehler et al., 1988; Nazzi et al., 1998;
Ramus, 2002). However, systematic studies have not been con-
ducted to date with bilingual newborns. Because monolinguals
are familiar with only one language, discrimination of any par-
ticular language pair involves either discriminating a rhythmi-
cally familiar language from an unfamiliar one or discriminating
two rhythmically unfamiliar languages. For bilingual infants,
successful acquisition requires their discrimination of two famil-
iar languages, a potentially challenging and as yet untested task.

To investigate whether newborns with prenatal bilingual
experience discriminate their native languages, Study 2 tested
50 newborn infants for their discrimination of English and
Tagalog in a high-amplitude sucking habituation procedure.

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The Roots of Bilingualism in Newborns 347

As in Study 1a, newborns from a Tagalog-English bilingual
background were compared with newborns from a monolin-
gual English background.

Method
Infants were habituated to either four English or four Tagalog
low-pass-filtered sentences (counterbalanced) until sucking
declined, so that the number of high-amplitude sucks across a
2-min window was at least 25% fewer than that produced in the
previous minute. Infants habituated in an average of 7 min
(range: 5–15), and the mean time to habituation did not differ
across groups, F(2, 47) = 0.49, p = .62. At test, infants in the
experimental condition heard two novel sentences from a new
speaker in the other language (n = 32; 16 monolingual, 16 bilin-
gual infants) for 4 min. To rule out spontaneous recovery (Jef-
frey & Cohen, 1971), a control group (n = 18 monolinguals)
heard two novel sentences from a new speaker in the same lan-
guage. Bilingual controls were not tested, because spontaneous
recovery was not expected to differ across groups. If infants
could discriminate the languages, then those in the experimental
condition would show increased sucking at test whereas those in
the control condition would not.

Results and discussion
Both English monolingual and Tagalog bilingual infants dis-
criminated between the two languages (see Fig. 3). The num-
ber of high-amplitude sucks was computed in three blocks:
last 2 habituation minutes, first 2 test minutes, and second 2
test minutes. Preliminary analyses showed no effects or inter-
actions with test order (English first vs. Tagalog first). A mixed
3 (block) × 2 (condition: control, experimental) analysis of
variance (ANOVA) showed a significant Block × Condition
interaction, F(2, 96) = 3.20, p = .045. A follow-up repeated
measures ANOVA showed that in the control group, sucking
did not differ as a function of block, F(2, 34) = 2.04, p = .15.
In the experimental group, a similar ANOVA with an addi-
tional factor of exposure group (English monolingual, Tagalog
bilingual) showed a significant effect of block, F(2, 60) =
4.64, p = .013, but no Block × Exposure Group interaction,
F(2, 60) = 0.40, p = .67. Planned directional t tests compared
sucking in the final habituation block with the average across
the 4 test minutes (both test blocks). Both English monolin-
gual infants, t(15) = 2.00, p = .032, and Tagalog bilingual
infants, t(15) = 1.99, p = .033, showed a significant recovery
of sucking during test. Tagalog bilingual infants, then, were
still able to discriminate their two languages, despite having
shown similar preference for the languages in Study 1a.

General Discussion
Previous work with bilingual infants has shown that 4-month-
olds can discriminate their languages auditorily (Bosch &
Sebastián-Gallés, 1997) and visually (Weikum et al., 2007).

The current work reveals that language discrimination in bilin-
guals is robust at birth and that language preference at birth
reflects previous listening experience. Monolingual newborns’
preference for their single native language directs listening
attention to that language. Bilingual newborns’ interest in both
languages helps ensure attention to, and hence further learning
about, each of their languages.

This study investigated neonates who were learning rhythmi-
cally distinct languages. Still unanswered is whether the same
sensitivity to rhythm can also support infants’ acquiring two lan-
guages from the same rhythmic class. The differential preference
for Tagalog by Tagalog-English bilinguals in comparison with
Chinese-English bilinguals hints that bilingual neonates have
some sensitivity to intraclass rhythmic differences or to other dif-
ferences between language pairs in the same rhythmic class. Fur-
ther research is required to directly test these possibilities.

In sum, these findings show that from the very beginning,
the same perceptual and learning mechanisms that support
monolingual acquisition are also available to support bilingual
acquisition. Moreover, our results confirm that infants exposed
to two languages throughout gestation have already begun the
process of bilingual acquisition at birth.

0

Final
Habituation

Test
Block 1

Test
Block 2

5
10
15
20

25

A
ve

ra
ge

N
um

be
r

of
H

ig
h-

A
m

pl
itu

de
S

uc
ks

/M
in

30

Tagalog Bilingual Experimental
Group

English Monolingual Experimental
Control

p = .03

p = .045

p > .10

Fig. 3. Average number of high-amplitude sucks per minute as a function
of group and experimental block in Study 2, which tested the ability to
discriminate English and Tagalog. Results are shown for the Tagalog-English
bilingual and English monolingual experimental groups and for the control
group. Error bars represent standard errors of the mean.

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348 Byers-Heinlein et al.

Acknowledgments

We thank Marisa Cruickshank, Erin Moon, Vivian Pan, Ke Heng
Chen, Ayasha Valji, Mohinish Shukla, and Laurel Fais for their com-
ments, assistance, and support.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interests with
respect to their authorship and/or the publication of this article.

Funding

This research was funded by grants from the Social Sciences and
Humanities Research Council of Canada, the Human Frontier
Science Program, the Natural Sciences and Engineering Research
Council of Canada, and the James S. McDonnell Foundation to Janet
F. Werker; by a University of British Columbia psychology postdoc-
toral fellowship to Tracey C. Burns; and by a Natural Sciences and
Engineering Research Council of Canada fellowship to Krista
Byers-Heinlein.

Notes

1. It is difficult if not impossible to separate the influence of pre-
natal experience from the possible effects of very early postnatal
experience. However, given the much greater amount of prenatal
as compared with postnatal listening, we have highlighted prenatal
experience throughout this article.
2. Data were excluded from an additional 28 infants in Study 1 (pref-
erence) and 87 infants in Study 2 (discrimination) because of crying
(12 preference, 27 discrimination), falling asleep or stopping sucking
(12, 31), experimenter or technical error (3, 3), spitting out the rubber
nipple (1, 5), high-amplitude sucks during less than 2 test minutes (0,
10), failure to habituate (0, 6), parental or hospital-staff interference
(0, 4), and hiccups (0, 1).
3. Including these infants yielded the same pattern of results.

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PAPER

Effect of socioeconomic status (SES) disparity on neural
development in female African-American infants at age 1 month

Laura M. Betancourt,1 Brian Avants,2 Martha J. Farah,3 Nancy L. Brodsky,1

Jue Wu,2 Manzar Ashtari4 and Hallam Hurt1,5

1. Department of Neonatology, The Children’s Hospital of Philadelphia, USA
2. Department of Radiology, University of Pennsylvania, USA
3. Department of Psychology, University of Pennsylvania, USA
4. Department of Radiology, The Children’s Hospital of Philadelphia, USA
5. The Perelman School of Medicine at the University of Pennsylvania, USA

Abstract

There is increasing interest in both the cumulative and long-term impact of early life adversity on brain structure and function,
especially as the brain is both highly vulnerable and highly adaptive during childhood. Relationships between SES and neural
development have been shown in children older than age 2 years. Less is known regarding the impact of SES on neural development
in children before age 2. This paper examines the effect of SES, indexed by income-to-needs (ITN) and maternal education, on
cortical gray, deep gray, and white matter volumes in term, healthy, appropriate for gestational age, African-American, female
infants. At 5 weeks postnatal age, unsedated infants underwent MRI (3.0T Siemens Verio scanner, 32-channel head coil). Images
were segmented based on a locally constructed template. Utilizing hierarchical linear regression, SES effects on MRI volumes were
examined. In this cohort of healthy African-American female infants of varying SES, lower SES was associated with smaller
cortical gray and deep gray matter volumes. These SES effects on neural outcome at such a young age build on similar studies of
older children, suggesting that the biological embedding of adversity may occur very early in development.

Research highlights

• Utilizes a birth cohort of term, healthy, appropriate
for gestational age, African-American, female infants.

• Examines relation between SES and cortical volume
in infants at age 4–6 weeks.

• Lower SES associated with smaller cortical gray and
deep gray matter volumes.

• Findings push back the age at which SES effects are
observed, from early childhood to early infancy.

Introduction

Childhood socioeconomic status (SES) is associated with
lifelong mental health and intellectual attainment, pre-
sumably through its effects on neural development. On

average, poor children differ from their higher SES
counterparts, achieving less success in school (Nisbett,
Aronson, Blair, Dickens, Flynn et al., 2012; Sirin, 2005)
and suffering at a higher rate from mental disorders
including ADHD, anxiety, and depression (Goodman,
1999; Kessler, Berglund, Demler, Jin, Merikangas et al.,
2005). In evaluations of SES effects on neurocognitive
skills of school-age children the largest disparities are
found in executive function, memory and language, skills
that are linked to academic success (Farah, Shera,
Savage, Betancourt, Giannetta et al., 2006; Landry,
Smith & Swank, 2002; Noble, McCandliss & Farah,
2007; Noble, Norman & Farah, 2005). Similarly, in a
limited number of studies, SES effects on cognitive
function in young children at toddler and preschool ages
have shown differences in language (Fernald, Marchman
& Weisleder, 2013; Wild, Betancourt, Brodsky & Hurt,

Address for correspondence: Laura M. Betancourt, Neonatology Research, Department of Pediatrics, 3535 Market Street, Room 1433, Philadelphia,
PA 19104, USA; e-mail: betancourtl@email.chop.edu

© 2015 John Wiley & Sons Ltd

Developmental Science 19:6 (2016), pp 947–956 DOI: 10.1111/desc.12344

2013) and executive function (Lipina, Martelli, Vuelta &
Colombo, 2005). Assessment of SES effects on these
skills is more common at these older ages; however, it is
likely that SES effects on development are present earlier
in infancy, during the first year of life, when development
proceeds most rapidly (Holland, Chang, Ernst, Curran,
Buchthal et al., 2014).
Recent brain imaging studies have investigated SES

effects on neural development utilizing MRI measures of
gray and white matter, both of which have established
associations with neurocognitive abilities. Positive rela-
tions between SES and gray matter volume have been
reported in some studies (Hanson, Chandra, Wolfe &
Pollak, 2011; Hanson, Hair, Shen, Shi, Gilmore et al.,
2013; Luby, Belden, Botteron, Marrus, Harms et al.,
2013) but not others (Brain-Development-Cooperative-
Group, 2012). Similarly, findings regarding SES effects
on white matter vary, with some investigators reporting
effects (Luby et al., 2013) and others reporting no effects
(Brain-Development-Cooperative-Group, 2012). Analy-
ses of repeated assessments of frontal gray matter
volumes between ages 5 months and 4 years (mean age
of first scan: 13.5 months) have shown a positive
relationship with SES (Hanson et al., 2013). Voxel-based
morphometry (VBM) and region of interest (ROI)
analyses have demonstrated regional gray matter corre-
lates of SES in children. While analyses of a large cohort
of children aged 4–18 years found no SES effects on
specific lobar volumes (Brain-Development-Coopera-
tive-Group, 2012), cortical thickness in certain prefrontal
regions was smaller for the lower SES participants in the
sample (Lawson, Duda, Avants, Wu & Farah, 2013;
Noble, Houston, Kan & Sowell, 2012). Raizada et al.
(2008) utilized scans collected from 14 5-year olds to
detect a marginally significant positive relationship
between SES and gray matter volume in the left inferior
frontal gyrus (IFG) (Raizada, Richards, Meltzoff &
Kuhl, 2008). In 5–17-year-olds, Noble and colleagues
(2012) found no main effect of SES; however, they did
find an interaction between SES and age with progres-
sively larger left IFG volumes for high SES children as
their age increased. Overall, ROI analyses have docu-
mented SES differences in hippocampal, amygdala,
middle temporal gyri, left fusiform and right inferior
occipito-temporal gyri (Hanson et al., 2011; Hanson,
Nacewicz, Sutterer, Cayo, Schaefer et al., 2015; Jed-
norog, Altarelli, Monzalvo, Fluss, Dubois et al., 2012;
Luby et al., 2013; Noble et al., 2012). These studies
taken together provide consensus that SES influences
developing neuroanatomy in children; less is known
about this relationship in younger infants and toddlers.
Given the findings in cohorts of older children, it is

likely that SES influences neuroanatomy earlier in

development. In the first year of life neural development
is dynamic, characterized by rapidly changing and
complex patterns of growth in gray matter (Gilmore,
Lin, Prastawa, Looney, Vetsa et al., 2007; Holland et al.,
2014; Knickmeyer, Gouttard, Kang, Evans, Wilber
et al., 2008) and of myelination and synaptic pruning
in white matter tracts (Dubois, Dehaene-Lambertz,
Kulikova, Poupon, H€uppi et al., 2014; Uda, Matsui,
Tanaka, Uematsu, Miura et al., 2015). A number of
investigators have shown that early neural structures are
the foundation for both concurrent and later cognitive
processes (Can, Richards & Kuhl, 2013; Jednorog et al.,
2012; Spann, Bansal, Rosen & Peterson, 2014). For
example, Short, Elison, Goldman, Styner, Gu et al.
(2013) and Deoni, O’Muircheartaigh, Elison, Walker,
Doernberg et al. (2014) report positive associations
between myelination of white matter tracts and infant
working memory and language function in the first year
of life. Longitudinal studies provide evidence that larger
volumes of gray and white matter, assessed using MRI,
are associated with better cognitive function in later
years (Can et al., 2013; Jednorog et al., 2012; Spann
et al., 2014). Despite the emerging consensus that early
neural development is highly responsive to environmen-
tal variation, including variation in SES levels (Hack-
man, Farah & Meaney, 2010), few studies have
specifically examined the impact of SES on neural
development and behavior at very young ages.
Although additional research is needed to firmly

establish the existence of structural brain correlates of
childhood SES and to identify specific patterns across
areas affected, the available research supports the conclu-
sion that SES does affect brain development in childhood.
To date, however, such investigations have utilized cohorts
of children who were both older than 2 years and were
mostly non-poor. Given that neural development during
the first year of life is rapid and dynamic (Gilmore et al.,
2007; Holland et al., 2014), it is likely that environmental
differences may shape brain development earlier than
previously reported. In contrast to the question of whether
SES has structural brain correlates in childhood, which
has a provisional answer, two related questions remain
entirelyopen. First, at what age are effects of SES on brain
structure detectable and, second, are there differences
within the lower range of SES? The present study is the
first to address these two questions.
The first question, concerning the age at which effects

of SES are manifest in child brain structure, is relevant to
the developmental origins of morphological differences.
In a cross-sectional investigation of neural development
between ages 3 and 20 years, results showed that income
and education were associated with increasing surface
area but not cortical thickness, with the largest effects

© 2015 John Wiley & Sons Ltd

948 Laura M. Betancourt et al.

among those at lowest income levels (Noble, Houston,
Brito, Bartsch, Kan et al., 2015). The youngest children
analyzed for SES effects on brain structure are in a cohort
of children aged 5 months to 4 years (Hanson et al.,
2013). Visual inspection of the growth curves for total
gray matter for this sample of low, middle, and high
income children shows overlap at 5 months of age and
divergence only later, with the low income group sepa-
rating from middle and high income groups at about
1 year. However, few subjects in this sample were
5 months old; the mean age of subjects at the first of
the longitudinally collected scans was 13.5 months. In
addition, curves were fit to data from multiple ages, so
that the values shown at age 5 months were influenced by
measurements at later ages. Presumably for these reasons,
the authors did not state any conclusions regarding the
age at which effects of SES emerge. There are no other
reports of SES and brain structure before toddlerhood.

The second question addressed here concerns the
effects of variation along the lower range of SES versus
variation from low to high SES. In contrast to SES,
which may refer to the full range of variation in income,
education and occupational status, poverty refers to the
very lowest levels of financial status with accompanying
social factors including low educational attainment. For
both policy and research purposes, poverty is typically
gauged by the ratio of income to needs, with the US
‘poverty line’ defined as an income-to-needs ratio (ITN)
of 1. No previous study of brain structure has compared
children who were poor, by this criterion, with non-poor
children; indeed the largest studies to date utilize a
sample that was predominantly middle class (Brain-
Development-Cooperative-Group, 2012; Hanson et al.,
2011; Hanson et al., 2013; Lange, Froimowitz, Bigler &
Lainhart, 2010; Lawson et al., 2013). Furthermore,
stringent exclusionary criteria for this sample eliminated
children disproportionately from lower SES levels
(Waber, De Moor, Forbes, Almli, Botteron et al.,
2007), raising questions about the typicality of the lower
SES children (Hanson et al., 2013). An exception pub-
lished by Noble et al. (2015) showed increased sensitivity
to SES influence along the lower range of (a relatively
broad distribution) of family income and education.
Taken together, the samples cited above are of broader
ranges of SES, with none including primarily poor and
near-poor children. The sample studied for the current
report is approximately half poor and half near-poor.
With 22% of American children classified as poor
according to the Federal standards (Canada, 2014),
utilization of a cohort of primarily the lower SES
participants rather than those from middle and upper
ranges allows for a comparison that is both socially and
scientifically relevant.

On the basis of the research reviewed above, we
hypothesized an early association of SES and cortical
gray matter volume in infants at 1 month of age. In
addition we analyzed the association between SES and
deep gray matter and white matter volumes. To limit the
number of confounding variables in a small-sized cohort,
we restricted gender and ethnicity to only female
African-American infants.

Methods

Participant recruitment and inclusion criteria

Mothers and their infants were recruited at delivery from
a single hospital for a larger study of the effects of SES
on both neural and cognitive development. Mothers
were eligible if they were between 18 and 45 years of age
and declared that both parents were American-born
African-American. Potential participants were excluded
if they were non-English speaking, had significant
psychiatric diagnoses, were enrolled in an alcohol or
drug rehabilitation program, or had significant medical
or obstetrical conditions as defined by the obstetrical
service. Infants eligible for inclusion were female single-
tons born at 38–42 weeks gestation, with birth weights
appropriate for gestational age and 5-minute Apgar
scores ≥8. Infants were excluded if they were diagnosed
with any condition associated with developmental delay,
were hospitalized more than 3 days, failed the hearing
screen, or were not discharged to their biologic mother.
Target enrollment was 30 low SES infants and mothers
and 30 higher SES infants and mothers. Upon enroll-
ment all participants signed informed consent approved
by the Institutional Review Board of the Children’s
Hospital of Philadelphia.

Socioeconomic status (SES): income-to-needs (ITN) and
education

SES was indexed by ITN and maternal education. Low
SES (poor group) was defined as ITN at or below
government poverty line plus no more than high school
education for either parent. Higher SES (near-poor) had
ITN above the poverty line plus at least a high school
education for both parents. The ITN variable was based
on the 2013 US government official poverty definition
(US Census Bureau, 2013) and was ascertained by
maternal self-report of household income and composi-
tion. Mothers and infants were categorized into one of
five ITN categories according to income and family size.
For example, the poverty threshold for a family of two is
$15,510 per year. Families making less than this amount

© 2015 John Wiley & Sons Ltd

Socioeconomic effects on infant neural development 949

are classified as below the poverty line (ITN = 1). A
family of two making $62,040 per year is classified in the
higher end of the range at 400% above the poverty line
(ITN = 5). The remaining three ITN categories were
distributed between the low and higher income range.
Education was ascertained from maternal self-report and
ranged from some high school through graduate school.
An SES Composite score was computed by rescaling
ITN values to match the scale for values of maternal
education and summing them, giving these two dimen-
sions of SES equal weight. Because nearly two-thirds of
the infants in the current cohort were living in house-
holds without their biological father, we used maternal
but not paternal education in the composite (Entwislea
& Astone, 1994). The current report includes neural data
from the infant participants collected at age 1 month
using MRI.

Image acquisition and processing

Infants underwent MRI scans at approximately 5 weeks
post estimated date of confinement (EDC). No sedation
was utilized. Appointments were scheduled for parent-
reported infant nap times. Infants were fed, swaddled,
and acclimated to the scanner room before placement in
the scanner. High resolution T1- and T2-weighted and
diffusion-weighted images were obtained utilizing a 3T
Siemens Verio Scanner with a 32-channel head coil.
All subjects’ images were converted into anonymous

Neuroimaging Informatics Technology Initiative (Nifti)
format. A population-specific template was built using
data from 15 participants with high quality data. The
final template was labeled with six spatial probability
functions (priors) that defined the voxel-wise probability
of six distinct tissue/anatomical classes: cortical gray
(includes hippocampus and amygdala), deep gray (in-
cludes thalamus and basal ganglia), white matter, brain-
stem, cerebellum, and cerebrospinal fluid (Shi, Yap, Wu,
Jia, Gilmore et al., 2011). Our method iteratively opti-
mized both template shape and appearance to estimate
an average brain that best represented the expected
anatomy in the cohort (Tustison, Cook, Klein, Song,
Das et al., 2014). See Figure 1 for segmentation process
illustration. Estimation of hippocampal volume was not
performed because variability in qualitative and quanti-
tative aspects of existing manual segmentation protocols
leads to significant disagreement in measured volumes of
hippocampal and parahippocampal substructures
(Yushkevich, Amaral, Augustinack, Bender, Bernstein
et al., 2015).
Diffeomorphic image registration (SyN algorithm,

implemented in ANTs; Avants, Tustison, Stauffer, Song,
Wu et al., 2014; Tustison et al., 2014) was used to map

between template and subject space. This mapping was
used to transfer the six template prior probability maps
into the space of the individual’s T2 MRI. T1 and
diffusion-weighted MRI also were mapped into the space
of the T2 via a low-dimensional registration. These
modalities were complemented by the Laplacian of the
T2 image to form a rich feature space for basis of 6-tissue
multivariate segmentation. The final segmentation pro-
cedure incorporated both T2 and T1 features with the
probability maps via a Bayesian tissue segmentation
algorithm, Atropos (Tustison et al., 2014).
To verify quality, each segmentation was visually

inspected, along with the original T1 and T2 data, and

Registration / Segmentation

A. Template B. Subject

4 Tissue Priors Tissue Segmentation

Figure 1 Segmentation process for images from infants at age
5 weeks. Six spatial probability functions (priors) define the
voxel-wise probability of distinct tissue/anatomical classes: (1)
Cortical Gray (includes the hippocampus and amygdala); (2)
Deep Gray (includes thalamus and basal ganglia); (3) White
Matter; (4) Brainstem; (5) Cerebellum; and (6) Cerebrospinal
Fluid. Column A (left) shows the template and 4 of 6 priors
used for segmentation process. Column B (right) shows the
subject image before and after segmentation with the priors.
Cortical Gray is shown in green. Deep gray is shown in yellow.
White matter is shown in blue. CSF is shown in red. Brain stem
and cerebellum not shown.

© 2015 John Wiley & Sons Ltd

950 Laura M. Betancourt et al.

data were reviewed for motion artifact. To assist
successful 6-tissue segmentation, we first used joint label
fusion to perform brain extraction (MICCAI Society,
2013; Wang, Suh, Das, Pluta, Craige et al., 2013). Final
tissue segmentation was performed within this brain
mask defined by the labels available from the Makro-
poulous cohort (Makropoulos, Gousias, Ledig, Aljabar,
Serag et al., 2014). The full processing pipeline is
publicly available (Avants et al., 2014; Tustison et al.,
2014). MRI data for this report include cortical gray,
deep gray, and white matter volumes. Examiners were
masked to SES status.

Analyses

Preliminary analyses included SES group comparisons of
maternal and child characteristics using t-tests and chi
square analysis. Pearson correlations tested associations
between demographic and MRI variables. Main analyses
consisted of hierarchical linear regressions using the SES
composite as a continuous variable to examine SES
effects on neural outcomes. Covariates were birth weight
and post-conception age at scan (at this age more
predictive of developmental maturity than post-natal
age) (Hanson et al., 2013; Martin, Fanaroff & Walsh,
2011). Analyses were performed using SPSS 22.0.

Results

Of 46 scans completed, data from two subjects (both
ITN of 1 and maternal education of high school level)
were not utilized due to motion and poor resolution.
Characteristics at time of enrollment and MRI are
shown in Table 1 for the 44 participants with successful
scans (25 Low SES, 19 Higher SES). Low SES mothers
were younger than Higher SES mothers and, per
enrollment criteria, reported less education. Also per
enrollment criteria, ITN category for the Low SES group
was 1 and for the Higher SES group was 2 or greater
(74% ITN = 2, 26% ITN ≥ 3). Infant birth characteris-
tics and age at time of MRI were similar.

Correlations between cortical gray, deep gray, and
white matter volumes and participant characteristics are
shown in Table 2. Cortical gray matter volume corre-
lated with the SES Composite, ITN, maternal education,
gestational age, birth weight, head circumference and
length, and post-conception age at MRI. Deep gray
matter volume correlated with the SES Composite,
maternal education, birth weight, head circumference
and length and post-conception age at MRI. White
matter volume correlated with only birth weight, head
circumference and post-conception age at time of MRI.

To examine the relations between SES and volumes of
cortical gray, deep gray, and white matter, three hierar-
chical linear regressions were conducted for each out-
come, controlling for post-conception age and birth
weight (Hanson et al., 2013; Martin et al., 2011). In the
first step of each regression, birth weight and post-
conception age at MRI were entered stepwise (Model 1).
In the second step (Model 2) the SES Composite was
added to the regression.

Table 1 Infant characteristics at time of enrollment and MRI
by SES group

Low SES
group
n = 25

Higher SES
group
n = 19 p-value

Enrollment characteristics
Mother’s age, yr 24.1 � 4.9a 27.1 � 5.6 <.001 ITN Below poverty line 25 (100%) 0 Above the poverty line 0 19 (100%)

Mother’s education <.001 1. Less than high school 16 (64%)b 0 2. High school/GED 6 (24%) 3 (16%) 3. Technical/Vocational 3 (12%) 1 (5%) 4. Some college 0 5 (26%) 5. Two-year degree 0 5 (26%) 6. Four-year degree 0 4 (21%) 7. Some graduate school 0 0 8. MA, PhD, Professional 0 1 (5%)

Gestational age, weeks 39.4 � 1.0 39.6 � 0.9 .35
Birth weight, kg 3.29 � 0.44 3.42 � 0.44 .36
Birth HCc, cm 33.5 � 1.3 34.0 � 1.4 .33
Birth length, cm 50.2 � 2.3 50.3 � 2.3 .91
1-month characteristics
Age at MRI
Post-conception, wks 44.7 � 0.5 45.0 � 0.9 .17
Post-natal, wks 5.0 � 0.9 5.0 � 1.2 .90

amean � SD, bn (%); cHead circumference.

Table 2 Correlations between cortical volumes and
participant characteristics

Cortical gray
matter

Deep gray
matter

White
matter

SES Composite 0.38 (0.01)a 0.34 (0.024) 0.25 (0.096)
Income-to-needs 0.37 (0.014) 0.28 (0.063) 0.11 (0.48)
Maternal education 0.41 (0.006) 0.34 (0.022) 0.22 (0.15)

Paternal education 0.13 (0.40) 0.27 (0.076) 0.22 (0.15)
Maternal age �0.069 (0.66) 0.16 (0.29) �0.043 (0.78)
Gestational age 0.30 (0.046) 0.19 (0.214) 0.18 (0.23)
Birth weight 0.64 (0.000) 0.47 (0.001) 0.53 (0.000)
Head circumference 0.64 (0.000) 0.46 (0.002) 0.45 (0.003)
Birth length 0.30 (0.050) 0.31 (0.047) 0.16 (0.32)
Age at MRI
Post-conception,
wks

0.49 (0.001) 0.40 (0.007) 0.48 (0.001)

Post-natal, wks 0.078 (0.61) 0.068 (0.66) 0.12 (0.46)

aPearson r (p-value), n = 44.

© 2015 John Wiley & Sons Ltd

Socioeconomic effects on infant neural development 951

For cortical gray matter, in Model 1, birth weight, but
not age at MRI, was retained in the model (R2 = 0.38, F
(1, 42) = 25.17, p < .001). Addition of the SES Com- posite in Model 2 resulted in a significant increase in variance accounted for by the model (ΔR2 = 0.082, F(1, 41) = 6.21, p = .017). In the regression on deep gray matter volume, birth weight but not MRI age was retained in Model 1 (R2 = 0.22, F(1, 42) = 1.87, p = .001). Adding SES improved the model significantly (ΔR2 = 0.073, F(1, 41) = 4.22, p = .046). In the regres- sion for white matter volume, birth weight and MRI age were retained after the stepwise entry in Model 1 (R2 = 0.32, F(1, 41) = 9.85, p < .001). The addition of SES in Model 2 did not significantly improve the model (ΔR2 = 0.015, F(1, 40) = 6.85, p = .35). Table 3 shows

the regression statistics for the models for each outcome.
Figure 2 illustrates the positive relationships between
SES and cortical gray and deep gray matter volumes
adjusted for variables retained in the final models.
We did not examine the effects of SES components,

income and education on brain volumes independently
of one another as these two variables were highly
correlated (r = 0.86, p < .001).

Discussion

In this cohort of healthy term female African-American
infants, MRI showed SES-dependent differences in gray
matter volume at the young age of 5 weeks with effects
being present along the lower range of the distribution of
SES. Both cortical gray matter, which includes the cortex
of the two hemispheres and hippocampi, and deep gray
matter, which includes the thalamus and basal ganglia,
were significantly smaller in low SES infants. No
difference was observed in white matter volume. While
low SES is associated with lower birth weights and
increased risk for prematurity, both of which are closely
linked to brain development (Aber, Bennett, Conley &
Li, 1997; Osofsky, 1974; Parker, Greer & Zuckerman,
1988), the present results are from a cohort of healthy
term infants showing SES effects on brain development
independent of birth weight and post-conception age.
The results reported here both add to a growing

consensus that SES impacts brain development and push
back the age at which such effects can be observed from
early childhood to early infancy. To our knowledge no
other studies have examined this relationship as early as
5 weeks of age. Two studies, however, have reported
functional brain activity differences within the first year
of life: Tomalski et al. (2013) reported EEG differences

Table 3 Hierarchical linear regression analyses predicting
cortical gray matter, deep gray matter and white matter
volumes

Cortical gray
matter
Deep gray
matter
White
matter

Model 1
Age at MRI* – – 0.30 (0.044)
Birth weight 0.61 (.000)** 0.61 (0.000) 0.36 (0.019)
R2 0.38 0.22 0.32
F (df) 25.17 (1,42) 11.87 (1,42) 9.85 (1,41)
p-value <.001 .001 <.001

Model 2
Age at MRI* – – 0.27 (0.077)
Birth weight 0.57 (0.000) 0.43 (0.003) 0.35 (0.021)
SES Composite 0.29 (0.017) 0.27 (0.046) 0.13 (0.35)
R2 0.46 0.29 0.34
ΔR2 0.082 0.073 0.015
F (df) 6.21 (1,41) 4.22 (1,41) 6.85 (1,40)
p-value 0.017 0.046 0.35

*Post-conception, wks. **Standardized regression coefficient (p-values,
2-tailed). Model 2 Predictor: SES Composite.

Figure 2 SES predicts MRI volumes at age 1 month. In final models, higher levels of SES were associated with larger cortical gray
and deep gray matter volumes. X-axis shows z-scores for the SES Composite. Y-axis shows residual values of each dependent
variable after adjustment for birth weight.

© 2015 John Wiley & Sons Ltd

952 Laura M. Betancourt et al.

between low and middle SES infants between 6 and
9 months of age; Gao et al. (2015) reported marginal
effects of SES on fMRI resting functional connectivity at
6 months of age (Gao, Alcauter, Elton, Hernandez-
Castillo, Smith et al., 2015; Tomalski, Moore, Ribeiro,
Axelsson, Murphy et al., 2013). The current results show
that SES effects are manifest in the brain at an even
earlier age. In addition, because findings are not depen-
dent on arousal, distress, sleep deprivation or other states
that affect functional measures, results reported here
point more decisively to anatomical differences in brain
development.

The timing of the emergence of SES effects can be
informative as to their causes. Possible pre- or post-natal
etiologies include the effects of maternal health, toxin
exposure, nutrition, sleep quality or stress (Boyce &
Kobor, 2015; Buss, Lord, Wadiwalla, Hellhammer,
Lupien et al., 2007; Cordero, 1990; DiPietro, 2012;
Hackman et al., 2010). Subjects in the present study
were 5 weeks of age at time of scan, minimizing the
opportunity for postnatal influence, however, such
influences cannot be ruled out. Future studies utilizing
MRI immediately after birth are needed to distinguish
the pre- and post-natal etiologies of SES effects.

Furthermore, differences present at birth may result
from prenatal factors, known to vary with SES, or from
genetic factors, or from their interaction (DiPietro,
Kivlighan, Costigan, Rubin, Shiffler et al., 2010). The
influence of genes on gray matter has been reported
(Knickmeyer, Wang, Zhu, Geng, Woolson et al., 2014);
however, the relation among genes, SES influences, and
neural outcome has yet to be explored. Given our results,
investigations of these relations should be conducted not
only for older children, but also for those at very early
stages of development.

Different components of SES may impact brain devel-
opment (Brito & Noble, 2014). The present study was not
designed to parse the relative effects of income and
education on brain structure. However, in larger samples
of older children, individual effects of income and
education have been evaluated and results have been
mixed. For example, Hanson et al. (2011) reported an
association between lower household income and lower
total gray matter volume, with no influence of maternal
education. Using a subset of the same cohort, Lawson
et al. (2013) found an association between cortical thick-
ness in frontal regions of interest and maternal and
paternal education but not family income. Across ages
3–20, family income showed stronger associations with
surface area than education in a large cohort from abroad
range of SES (Noble et al., 2015). Studies with larger
cohorts of very young infants are needed to evaluate the
relative effects of SES components at young ages.

Our study, for which the long-term goal is examina-
tion of effects of SES disparity on neural and develop-
mental outcome, joins a growing number of
investigations examining brain structure and outcome
of infants and young children. The relation between
neural status at 1 month of age and subsequent
cognitive outcome was reported by Spann et al.
(2014) in 33 infants; associations between cerebral
surface morphology and subsequent motor, language,
and cognitive scores were reported. Can et al. (2013), in
19 infants, scanned at 7 months and evaluated at
12 months, found relations between early gray matter
and white matter concentration and language skills.
Amygdala volume was found to be related to language
outcome in infants scanned at 6 months and evaluated
at 2 years (Ortiz-Mantilla, Choe, Flax, Grant & Bena-
sich, 2010), with another investigation showing an
association of white matter microstructure and infant
working memory in infants imaged at 12 months (Short
et al., 2013). These researchers, however, did not
examine SES effect on the relationship between neural
development and cognitive outcome in their higher SES
cohorts. Our data showing effects of SES on neural
development at 1 month of age will be combined with
later neural and cognitive evaluations to explore such
SES effects.

Limitations of this study are several. First, our
eligibility requirements, chosen to increase power by
eliminating the need to control for the influential
confounders gender (Giedd, Castellanos, Rajapakse,
Vaituzis & Rapoport, 1997) and race/ethnicity (Bai,
Abdul-Rahman, Rifkin-Graboi, Chong, Kwek et al.,
2012), impose predictable limitations on generalizability.
Regardless, findings inform for an understudied minor-
ity, and provide a template for exploration of neural
outcome at very young ages in other cohorts. Second,
sample size may be considered a limitation; however, a
cohort of 44 infants scanned at 1 month of age without
sedation in a study evaluating effect of SES disparity is,
to our knowledge, unique. While motion artifact is a
common challenge in infant imaging studies, only two of
the 46 successful scans were excluded due to motion, a
relatively high success rate (Almli, Rivkin & McKinstry,
2007; Shi et al., 2011). Third, we do not have a robust
prenatal database for this cohort that would allow for a
careful evaluation of prenatal influences on gray and
deep gray matter outcomes. Finally, we do not yet have
data for evaluation of whether effects on neural out-
comes detected at 1 month change by 12 months, or
whether there are relationships between volumetric
findings and infant cognitive outcomes; however, our
ongoing longitudinal follow-up will allow for these
analyses.

© 2015 John Wiley & Sons Ltd

Socioeconomic effects on infant neural development 953

Conclusions

In this cohort of term healthy African-American
females, lower SES was associated with smaller cortical
gray and deep gray matter volumes at age 4–6 weeks.
These differences in neural structure are early indicators
of increased risk for disadvantage in cognitive and
academic skills faced by poor children (Kolb, Mycha-
siuk & Gibb, 2014). On the other hand, it also is well
established that early intervention and enriched envi-
ronments can ameliorate compromised developmental
outcomes (Brooks-Gunn, Klebanov, Liaw & Spiker,
1993; Campbell, Pungello, Miller-Johnson, Burchinal &
Ramey, 2001). These findings underscore the need to
monitor and optimize development of our youngest
through programs and policies directed at reducing
impact of SES disparities (Heckman & Mastrov, 2007;
Knudsen, Heckman, Cameron & Shonkoff, 2006;
Shonkoff, Garner, Siegel, Dobbins, Earls et al., 2012).
The existence of SES differences so early in life suggests
that intervention cannot begin too soon in supporting
families with young children (Austin, Lemon & Leer,
2005; Raikes, Green, Atwater, Kisker, Constantine
et al., 2006; Tamis-LeMonda, Bornstein & Baumwell,
2001). Current efforts directed toward reduction of risks
posed by SES disparity are focused on the preschool
years, possibly well after early foundational neural
growth (Spann et al., 2014); we suggest increased focus
during infancy.

Acknowledgement

All phases of this study were supported by NIH/
NICHD: R21HD072461.

Financial disclosure

The authors have no financial relationships relevant to
this article to disclose.

Conflict of interest

The authors have no conflicts of interest to disclose.

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Alice M. Graham, Philip A. Fisher and Jennifer H. Pfeifer
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What Sleeping Babies Hear: A Functional MRI Study of Interparental Conflict and Infants’ Emotion

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Research Repor

t

Prominent ideas about how the environment shapes
development rest on an understanding that brain plastic-
ity during the first years of life confers vulnerability for
key neural systems involved in stress and emotion-related
functioning. The consequences of early life stress have
been investigated by examining its impact on these sys-
tems (Sánchez, Ladd, & Plotsky, 2001). Research with
infants and young children has employed peripheral
indicators of neuroendocrine functioning (e.g., cortisol;
Loman & Gunnar, 2010) and direct measures of brain
electroencephalographic activity (Nelson & McCleery,
2008) to increase understanding of how early adversity
affects neurobehavioral development.

The high spatial resolution of functional MRI (fMRI),
commonly used with older children and adults, has facili-
tated precise identification of neural networks linking
early adversity with subsequent socioemotional function-
ing. Consistent with animal models examining the conse-
quences of early adversity (Sánchez et al., 2001), this
work reveals the involvement of brain regions tied to

initiation and regulation of the hypothalamic-pituitary-
adrenal (HPA) axis stress response, including limbic
(Tottenham et al., 2011) and medial prefrontal regions
(Treadway et al., 2009). However, the existing knowledge
base in this area derives from fMRI research involving
older children and adults. This makes it difficult to distin-
guish effects of early stress from subsequent processes of
recovery or development of psychopathology. Moreover,
a predominant focus on severe stressors, such as institu-
tional rearing or maltreatment (Hart & Rubia, 2012),
leaves a gap in the empirical literature regarding effects
of more moderate early adversity.

Nonphysical interparental conflict is a more moderate
source of early adversity that nevertheless appears to be
associated with alterations in stress hormones, behavioral

458803PSSXXX10.1177/0956797612458803Graham et al.What Sleeping Babies Hear
research-article2013

Corresponding Author:
Alice M. Graham, Department of Psychology, University of Oregon,
1227 University of Oregon, Eugene, OR 97403-1227
E-mail: agraham2@uoregon.edu

What Sleeping Babies Hear: A Functional
MRI Study of Interparental Conflict and
Infants’ Emotion Processing

Alice M. Graham1,2, Philip A. Fisher1,2, and
Jennifer H. Pfeifer

1

1Department of Psychology, University of Oregon, and 2Oregon Social Learning Center, Eugene, Oregon

Abstract
Experiences of adversity in the early years of life alter the developing brain. However, evidence documenting this
relationship often focuses on severe stressors and relies on peripheral measures of neurobiological functioning during
infancy. In the present study, we employed functional MRI during natural sleep to examine associations between
a more moderate environmental stressor (nonphysical interparental conflict) and 6- to 12-month-old infants’ neural
processing of emotional tone of voice. The primary question was whether interparental conflict experienced by infants
is associated with neural responses to emotional tone of voice, particularly very angry speech. Results indicated that
maternal report of higher interparental conflict was associated with infants’ greater neural responses to very angry
relative to neutral speech across several brain regions implicated in emotion and stress reactivity and regulation
(including rostral anterior cingulate cortex, caudate, thalamus, and hypothalamus). These findings suggest that even
moderate environmental stress may be associated with brain functioning during infancy.

Keywords
psychological stress, neuroimaging, emotional development, infant development

Received 2/28/12; Revision accepted 7/24/12

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What Sleeping Babies Hear 783

symptoms, and socioemotional problems during child-
hood (Cummings & Davies, 2010; Davies, Sturge-Apple,
Cicchetti, & Cummings, 2007). Although more sparse than
research with older children and adults, research with
infants indicates that interparental conflict is associated
with differences in physiological and behavioral indices of
emotional reactivity and regulation as early as 6 months of
age (Crockenberg, Leerkes, & Lekka, 2007; Moore, 2010).
Interparental conflict may have an impact on early emo-
tional development through decreases in sensitive caregiv-
ing (Krishnakumar & Buehler, 2000), as well as direct
exposure to aggressive interactions between caregivers
(Crockenberg et al., 2007). Basic research suggests that
5-month-old infants discriminate between other people’s
different emotional states, with expressions of anger elicit-
ing greater attention and arousal than happy or neutral
expressions (Balaban, 1995; Grossmann, Oberecker, Koch,
& Friederici, 2010; Grossmann, Striano, & Friederici, 2005).
Additionally, Moore (2009) showed that infants who wit-
nessed vocal anger toward their mother demonstrated
altered parasympathetic nervous system responses to an
immediately subsequent stressful interaction with their
mother. Specifically, they showed increased withdrawal of
vagal tone and decreased recovery, both of which are
indicative of greater physiological reactivity, after this brief
exposure to anger (Moore, 2009).

Early exposure to interparental conflict may also
increase risk for later emotional and psychological prob-
lems. In 6-month-old infants, higher levels of interparen-
tal conflict are associated with lower baseline vagal tone
(C. Porter, Wouden-Miller, Silva, & Porter, 2003) and
greater withdrawal of vagal tone during a stressful inter-
action-and-recovery period (Moore, 2010), indicative of
lower parasympathetic tone and greater stress reactivity,
respectively. Variation in vagal reactivity acts as a mod-
erator of risk for school-age children exposed to conflict
(El-Sheikh et al., 2009; El-Sheikh & Whitson, 2006).
Despite the implication that some aspects of nervous-
system functioning may be shaped by family conflict
during infancy, and subsequently increase risk for school-
age children, the ties between early exposure and subse-
quent vulnerability remain poorly understood. The
autonomic and behavioral measures utilized to date rep-
resent outputs from multiple neural networks. Candidate
neural networks linking early adversity with subsequent
risk for psychopathology have not yet been identified.

Recent work demonstrates the feasibility of conduct-
ing fMRI research with infants during natural sleep
(Redcay, Kennedy, & Courchesne, 2007), which allows
for examination of specific neural regions and networks
during the first years of life. This work also draws atten-
tion to the sensitivity of infants to environmental stimuli
during sleep by documenting distinct patterns of neural

activation depending on properties of speech (Dehaene-
Lambertz, Dehaene, & Hertz-Pannier, 2002; Redcay, Haist,
& Courchesne, 2008) and emotional tone (Blasi et al.,
2011). The present study builds on these methodological
advances to characterize infants’ neural responses to
emotional stimuli in the context of varying levels of inter-
parental conflict.

Method

Participants

Families were recruited through flyers posted at local
human-services agencies and advertisements on the local
Craigslist.org Web site. Twenty-four infants (8 females, 16
males) aged 6 to 12 months (M = 8.33, SD = 1.90) com-
pleted an auditory fMRI paradigm during natural sleep;
20 infants had usable fMRI data. Infants had no known
neurological disorders and lived with both biological par-
ents. Exclusion criteria included referrals or investigations
by a public child-protective-services agency. To obtain
sufficient range in the sample, we assessed interparental
conflict during screening using the Problem-Solving
Communication subscale from the Marital Satisfaction
Inventory, Revised (Snyder, 1997) and selected families
based on established norms for distressed versus nondis-
tressed couples (see the Supplemental Material available
online for further information about the participants).

Interparental-conflict measures

Mothers rated nonphysical interparental-conflict levels
since the birth of the child on the Psychological
Aggression subscale of the Revised Conflicts Tactics Scale
(Straus, Hamby, Boney-McCoy, & Sugarman, 1996) and
the O’Leary-Porter Scale (B. Porter & O’Leary, 1980). The
measures were highly reliable (α = .936 and .823, respec-
tively) and correlated, r (22) = .744, p < .001, which allowed for creation of an average composite score of maternal report of interparental conflict (see the Supplemental Material for more information about the administration of these measures and the creation of the composite score).

Auditory stimuli

Auditory stimuli consisted of previously validated non-
sense sentences spoken in very angry, mildly angry,
happy, and neutral tones of voice by a male adult (Pell,
Paulmann, Dara, Alasseri, & Kotz, 2009). Nonsense
sentences possessed phonological and grammatical
properties of English, but content words were replaced
by semantically meaningless sound strings (see the
Supplemental Material for more information).

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784 Graham et al.

fMRI data acquisition

Infants came in for scanning at their regular bedtime.
Neuroimaging data were collected on a Siemens Allegra
3.0T scanner with a phased-array coil. Consistent with
previous neuroimaging research using auditory stimuli
with sleeping toddlers (Redcay et al., 2007), the paradigm
consisted of 20-s blocks separated by 15-s rest periods.
Blocks for each emotion condition (very angry, mildly
angry, happy, and neutral) were presented four times per
run in a semicounterbalanced design based on a
Williams’s Latin square. T2-weighted echo-planar func-
tional scans (9 min, 28 s; 284 whole brain volumes) were
acquired during presentation of auditory stimuli.
Prospective acquisition correction was applied to adjust
slice position and orientation, as well as to regrid residual
volume-to-volume motion in real time during data acqui-
sition for the purpose of reducing motion-induced effects
(Thesen, Heid, Mueller, & Schad, 2000). See the
Supplemental Material for more information on the scan-
ning protocol and data-acquisition process.

fMRI data analysis

Neuroimaging data were converted to Neuroimaging
Informatics Technology Initiative data format using the
MRIConvert program (http://lcni.uoregon.edu/~jolinda/
MRIConvert/). Brain images were extracted using the
Brain Extraction Tool from the FMRIB Software Library
(Beckmann et al., 2006; S. M. Smith, 2002; S. Smith,
Bannister, Beckmann, & Brady, 2001) and the Brain Surface
Extraction tool from BrainSuite09 (Sandor & Leahy, 1997;
Shattuck, Sandor-Leahy, Schaper, Rottenberg, & Leahy,
2001). All other preprocessing steps, including realign-
ment, registration, normalization, and smoothing with a
6-mm full-width half-maximum kernel, were accomplished
using Statistical Parametric Mapping (SPM) software
(SPM8; Wellcome Department of Cognitive Neurology,
London, England). Images were normalized to a standard
template for the 8- to 11-month age range from the MRI
Study of Normal Brain Development (Fonov et al., 2011;
Fonov, Evans, Mckinstry, Almli, & Collins, 2009). Images
with severe motion artifacts (greater than 2 mm of motion
or evidencing visual signs of motion artifacts) were
removed from runs, which resulted in less than 2 mm of
motion per run (maximum = 1.07 mm). At least three (out
of four) blocks of each condition were retained from each
run.

At the individual-subject level, fixed-effects contrasts
were computed to examine neural activation during pre-
sentation of each condition (very angry, mildly angry,
happy, and neutral) versus rest, as well as the specific
contrast of the very angry condition relative to the neu-
tral condition. Motion parameters in six directions were
included as regressors of no interest. Functional runs for

which the contrast of all auditory conditions to rest did
not evidence auditory-cortex activation at a relaxed
threshold ( p < .05, uncorrected) were excluded from analyses because it was not possible to ascertain whether basic sensory processing of stimuli occurred. Four of the 24 infants did not have at least one functional run for which clear auditory activation was detected and were thus excluded from further analyses. The resulting con- trast images were entered into whole-brain random- effects group analyses. We report only results that exceeded a threshold of p < .05, family-wise-error (FWE) corrected for multiple comparisons across the whole brain (specifically, p < .05 and 75 contiguous voxels, as determined by the NeuroElf AlphaSim toolbox, http:// neuroelf.net/). Regions of activation were identified based on anatomical landmarks, although infant template and Montreal Neurological Institute template coordinates are provided in the figure and tables for reference.

Results

Effect of interparental conflict on
processing very angry tone of voice

The primary research question focused on the extent to
which the composite interparental-conflict score was
associated with infants’ neural responses to very angry
auditory stimuli relative to neutral auditory stimuli. A
whole-brain regression with interparental-conflict score
as the independent variable and neural activity during
very angry relative to neutral tone of voice as the depen-
dent variable revealed a significant cluster in rostral ante-
rior cingulate cortex (ACC) as well as a subcortical cluster
encompassing parts of the caudate, thalamus, and hypo-
thalamus (Table 1). Specifically, higher levels of interpa-
rental conflict were associated with greater activation in
these regions during presentation of very angry com-
pared with neutral speech (Figs. 1a and 1b). To depict
this association graphically, we extracted mean parame-
ter estimates of activity (averaged across all voxels in
each cluster) for each participant from both the rostral
ACC and subcortical cluster during the very-angry-versus-
neutral contrast using the MarsBaR region-of-interest
toolbox for SPM (Brett, Anton, Valabregue, & Poline,
2002). These mean parameter estimates for each partici-
pant in each cluster were then plotted as a function of
conflict score. The graphs in Figures 1c and 1d do not
show the results of an additional statistical analysis;
rather, they illustrate the positive association between
conflict and activation of these regions to very angry rela-
tive to neutral speech that was demonstrated statistically
with the fMRI analyses. Results remained consistent when
we controlled for variation in infant age. These results

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What Sleeping Babies Hear 785

–1.2

–

0.8

–

0.4

0.0

0.4
0.8

0 20 40 60 80

M
ea

n
P

ar
am

et
er

E
st

im
at

e

Interparental-Conflict Score

–1.2

–0.8

–0.4

0.0
0.4
0.8
0 20 40 60 80
M
ea
n
P
ar
am
et
er
E
st
im
at
e

Interparental-Conflict Score
z=2

y=-1

x=-2

3
2
1
t

b
x = 2

y = –1

c

d Hypothalamus/Caudate

Rostral ACC
a

Fig. 1. Association between interparental-conflict scores and neural reactivity to very angry speech relative
to neutral speech. Activations that exceeded a threshold of p < .05, family-wise-error corrected for multiple comparisons across the whole brain (specifically, p < .05 and 75 contiguous voxels), are displayed on the group mean structural image. The brain image in (a) shows activation in the rostral anterior cingulate cortex (ACC; infant-atlas coordinates: x = 3, y = 29, z = 13; Montreal Neurological Institute coordinates: x = 4, y = 36, z = 17). The images in (a) and (b) show activation in a subcortical cluster including hypothalamus, caudate, and thalamus (infant-atlas coordinates: x = 3, y = −1, z = 1; Montreal Neurological Institute coordinates: x = 4, y = −1, z = 1), in which higher conflict scores predicted greater neural response to very angry than to neutral speech. The scatter plots (c and d; with best-fitting regression lines) reillustrate the association between conflict score and parameter estimates, separately for these two regions.

Table 1. Results of the Whole Brain Regression: Positive Association Between Interparental
Conflict and Brain Activation in Response to Very Angry Relative to Neutral Tone of Voice

Region Hemisphere

Infant-atlas coordinates MNI coordinates

k tx y z x y z

Anterior cingulate — 3 29 13 4 36 17 88 2.72
Thalamus Right 3 −1 1 4 −1 1 94 2.80
Thalamus Left −6 −4 −2 −7 −5 −3 — 2.29
Caudate Left −6 5 7 −7 6 9 — 2.81
Hypothalamus Left −6 −1 −5 −7 −1 −6 — 2.08

Note: The table reports only results that exceeded a threshold of p < .05, family-wise-error corrected for multiple comparisons across the whole brain (specifically, p < .05 and 75 contiguous voxels). The number of voxels within each cluster is indicated by k. Coordinates without voxel numbers indicate submaxima within the preceding cluster. MNI = Montreal Neurological Institute.

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786 Graham et al.

were specific to the very-angry-relative-to-neutral con-
trast. Exploratory analysis of the association between
interparental conflict and neural processing of happy
speech are presented in the Supplemental Material.

Effect of different emotional tones of
voice

Because conflict was associated with neural responses to
very angry speech, brain activation during presentation
of each emotional tone of voice was examined after
regressing out individual differences in conflict (Table 2).
Direct comparison of activations in response to very
angry relative to neutral stimuli did not reveal any clus-
ters surviving FWE correction, although a cluster in the
left temporal pole was just below this extent threshold.
Comparison of activations in response to happy relative
to neutral stimuli revealed significant areas in the left dor-
solateral prefrontal cortex, putamen, and medial tempo-
ral and occipital cortices.

Discussion

Although unusually adverse experiences such as insti-
tutional rearing or maltreatment are known to affect
development of key neural networks, the present study

suggests potential effects of a more moderate environ-
mental stressor, nonphysical interparental conflict. By
taking advantage of recent methodological advances that
allow for investigation of neural functioning during
infancy with the high spatial resolution afforded by fMRI
(Blasi et al., 2011; Dehaene-Lambertz et al., 2010), this
study provides novel evidence of associations between
interparental conflict and patterns of infant brain func-
tioning elicited by processing emotional speech during
natural sleep.

Higher levels of interparental conflict were associated
with greater activation to very angry tone of voice in the
rostral ACC and subcortical structures, including the
hypothalamus. Although we cannot be certain about the
meaning of the activation patterns in these brain regions,
many studies indicate their involvement in emotion and
stress processing and regulation (Kober et al., 2008). The
rostral ACC is implicated in emotion processing and reg-
ulation in typical populations (Kober et al., 2008), and its
functioning is frequently altered in stress-related disor-
ders (Fonzo et al., 2010; Kim et al., 2008). Research also
demonstrates associations between early adversity and
decreased volume of the ACC for adults with (Treadway
et al., 2009) and without symptoms of psychopathology
(Cohen et al., 2006), although the developmental path-
way through which these structural differences emerge
remains unknown.

Table 2. Activation to Emotion Stimuli After Regressing Out Interparental Conflict

Region Hemisphere

Infant-atlas coordinates MNI coordinates

k tx y z x y z

Conjunction of all conditions > rest
Auditory cortex Right 42 −13 1 51 −16 1 214 4.95
Auditory cortexa Left −42 −16 7 −51 −20 9 50 3.22

Very angry tone of voice > neutral tone of voice
Temporal polea Left −45 −1 −8 −55 −1 −10 53 2.96

Happy tone of voice > neutral tone of voice
Lingual gyrus — 0 −55 5 0 −68 6 473 2.96
Fusiform Left −18 −58 −11 −22 −72 −14 — 2.31
Parahippocampal gyrus Left −15 −19 −17 −18 −23 −22 — 2.14
Putamen Left −21 5 7 −26 6 9 189 2.55
Midcingulate — −9 −1 28 −11 −1 36 — 2.00
Supplementary motor area — −3 −1 49 −4 −1 63 — 2.00
Superior frontal gyrus Left −18 35 22 −22 43 28 107 2.35
Middle frontal gyrus Left −33 20 28 −40 25 36 — 1.98

Note: The table reports results that exceeded a threshold of p < .05, family-wise-error corrected for multiple comparisons across the whole brain (specifically, p < .05 and 75 contiguous voxels), with the exception of one subthreshold cluster for the conjunc- tion analysis and one for very angry tone of voice > neutral tone of voice contrast. The number of voxels within each cluster is
indicated by k. Coordinates without voxel numbers indicate submaxima within the preceding cluster. No clusters were identified
for the mildly angry tone of voice > neutral tone of voice contrast. MNI = Montreal Neurological Institute.
aSubthreshold clusters are reported for these activations ( p < .05, uncorrected; 50 voxels).

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What Sleeping Babies Hear 787

The hypothalamus initiates activity of the HPA axis.
Activity of the HPA axis in response to psychosocial stress
is controlled by limbic brain structures involved in emo-
tion processing and memory, including the amygdala,
hippocampus, and ACC (Pruessner et al., 2010; Ulrich-Lai
& Herman, 2009). The hypothalamus is thus viewed as a
key link between emotional input, neuroendocrine func-
tioning, and stress reactivity (Kober et al., 2008). Extensive
research has focused on alterations in the functioning of
the HPA axis (as indexed by the hormone cortisol) as a
result of early life stress, including more normative stress-
ors, such as interparental conflict (Davies et al., 2007),
and more extreme events, such as neglect and abuse
(Bruce, Fisher, Pears, & Levine, 2009). Specific patterns
of HPA-axis functioning have also repeatedly been asso-
ciated with mood disorders in adolescence and adult-
hood (Lopez-Duran, Kovacs, & George, 2009; Parker,
Schatzberg, & Lyons, 2003).

These findings also converge with extensive research
using animal models, which points to the ACC and hypo-
thalamus as part of neural networks that link early
psychosocial adversity to subsequent difficulties with
regulation of emotions and stress (Loman & Gunnar,
2010). However, this study is the first to document an
association between an environmental stressor and the
functioning of these specific brain regions during infancy.
These regions were identified based on a whole-brain
regression as opposed to a priori specification as regions
of interest. This allowed for a more independent test of
whether the findings in this study converge with existing
knowledge about the role of these brain regions based
on animal models and research with older children and
adults (Hart & Rubia, 2012).

This study also provides novel evidence regarding
infants’ neural processing of happy and angry emotional
speech during sleep, regardless of the level of interparen-
tal conflict. The findings are broadly in line with those of
a recent fMRI study indicating differentiation of sad rela-
tive to neutral vocalizations in sleeping 3- to 7-month-
olds (Blasi et al., 2011), although this study did not find
differentiation between happy and neutral stimuli. We
may have been better able to observe the latter pattern
because of differences in the age ranges sampled and the
stimuli (nonsense speech vs. emotional vocalizations).

Limitations of the present study include the lack of
observational assessment of interparental conflict and of
a high-intensity positive-affect condition (e.g., very
happy) to test whether the effects are specific to anger
rather than high-intensity emotion more generally.
Additionally, recruitment through Craigslist and human-
services agencies may have skewed the sample toward
individuals of lower socioeconomic status. We also were
unable to monitor and control for sleep state, which is an
important issue to be addressed in future work (see the

Supplemental Material). Future research will also benefit
from longitudinal investigations and inclusion of behav-
ioral measures to assess whether changes in neural func-
tioning mediate between exposure to environmental
stress and socioemotional development.

Despite these limitations, the present findings indicate
that during a period when infants are particularly vulner-
able because of their complete dependence on caregiv-
ers and high levels of neural plasticity, moderate sources
of environmental stress may be related to neural func-
tioning in areas central to emotion and stress-related pro-
cesses. Moreover, far from being oblivious to parents’
conflict, infants’ processing of stressor-relevant stimuli,
such as angry tone of voice, may occur even during
sleep.

Acknowledgments

Special thanks are due to Scott Watrous at the University of
Oregon’s Lewis Center for NeuroImaging, Kyndal Howell at the
Oregon Social Learning Center and the University of Oregon
Stress Neurobiology and Prevention Laboratory, and Weili Lin
and Kathy Wilber at the Biomedical Research Imaging Center,
University of North Carolina School of Medicine.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with
respect to their authorship or the publication of this article.

Funding

Support for this work was provided by the Center for Drug
Abuse Prevention in the Child Welfare System (1-P30-DA023920);
the Early Experience, Stress, and Neurobehavioral Development
Center (1-P50-MH078105); a Ruth L. Kirschstein National Res –
earch Service Award (F31-10667639); and the Lewis Center for
NeuroImaging at the University of Oregon.

Supplemental Material

Additional supporting information may be found at http://pss
.sagepub.com/content/by/supplemental-data

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0

https://doi.org/10.1111/desc.12537

© 2017 John Wiley & Sons Ltd

Received: 23 June 2016  | Accepted: 3 November 2016
DOI: 10.1111/desc.12537

P A P E R

Older but not younger infants associate own- race faces with
happy music and other- race faces with sad music

Naiqi G. Xiao1 | Paul C. Quinn2 | Shaoying Liu3 | Liezhong Ge3,4 | 
Olivier Pascalis5 | Kang Lee1

1Dr Eric Jackman Institute of Child
Study, University of Toronto, Toronto, Canada
2Department of Psychological and Brain
Sciences, University of Delaware, Newark, USA
3Zhejiang Sci-Tech University, Hangzhou, China
4Center for Psychological Sciences, Zhejiang
University, Hangzhou, China
5LPNC – Université Grenoble Alpes, CNRS,
Grenoble, France

Correspondence
Kang Lee, Dr Eric Jackman Institute of Child
Study, University of Toronto, 45 Walmer Road,
Toronto, ON, M5R 2X2, Canada.
Email: kang.lee@utoronto.ca

Funding information
Natural Science and Engineering Research
Council of Canada; National Institutes
of Health, Grant/Award Number: R01
HD046526; National Science Foundation of
China, Grant/Award Numbers: 31671146,
31070908, 31300860, and 31470993;
Zhejiang Provincial Natural Science Foundation
of China, Grant Award Number: LY16C90006

Abstract
We used a novel intermodal association task to examine whether infants associate
own- and other- race faces with music of different emotional valences. Three- to
9- month- olds saw a series of neutral own- or other- race faces paired with happy or
sad musical excerpts. Three- to 6- month- olds did not show any specific association
between face race and music. At 9 months, however, infants looked longer at own-
race faces paired with happy music than at own- race faces paired with sad music.
Nine- month- olds also looked longer at other- race faces paired with sad music than at
other- race faces paired with happy music. These results indicate that infants with
nearly exclusive own- race face experience develop associations between face race
and music emotional valence in the first year of life. The potential implications of such
associations for developing racial biases in early childhood are discussed.

R E S E A R C H H I G H L I G H T S

• Three- to six-month-olds did not show association between face
race and music emotional valence.

• Nine-month-olds cross-modally associated own-race faces with
happy musical excerpts.

• Nine-month-olds cross-modally associated other-race faces with
sad musical excerpts.

• Early asymmetrical experience with own- versus other-race faces
has downstream consequences.

1   |   I N T R O D U C T I O N

Experience plays a crucial role in the development of face processing
in infancy. With increased experience, infant face- processing ability
not only improves but also becomes specialized to process the types

of faces experienced most frequently (for a review, see Lee, Anzures,
Quinn, Pascalis, & Slater, 2011). This specialization reflects the fact
that infant face experience is typically asymmetrical. For example,
infants encounter own- race faces significantly more than other- race
faces (Liu, Xiao, Xiao et al., 2015; Rennels & Davis, 2008; Sugden,
Mohamed- Ali, & Moulson, 2014).

Extensive studies have shown that owing to this own- versus other-
race face experience asymmetry, infants process own- and other- race
faces differently in the first year of life (Anzures et al., 2013). Whereas
newborns show no visual preference for own- versus other- race faces,
infants as young as 3 months look longer at own- race faces when they
are paired with other- race faces (Bar- Haim, Ziv, Lamy, & Hodes, 2006;
Kelly, Liu et al., 2007; Kelly et al., 2005; Liu, Xiao, Quinn et al., 2015).
Moreover, whereas infants at 3 months initially recognize faces from
various races equally well, by 9 months, they display superior recogni-
tion for own- race faces (Kelly et al., 2009; Kelly, Quinn, et al., 2007).
In addition, although younger infants sort faces from different races

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2 of 10  |     XIAO et Al .

into distinctive race categories, 9- month- olds group own- race faces
into one category and multiple other- race face classes into another
category (Quinn, Lee, Pascalis, & Tanaka, 2016). Furthermore, with
increased age, infants exhibit specialized eye- movement patterns for
own- race, but not for other- race, faces (Liu et al., 2011; Wheeler et al.,
2011). These differential processing patterns for own- versus other-
race faces reflect emergent expertise in the perceptual processing
of own- race faces by infants as a result of asymmetrical exposure to
own- versus other- race faces (Anzures et al., 2013; Lee et al., 2011).

Despite the substantial evidence regarding the effect of asymmet-
rical experience on the development of own- versus other- race face
recognition and category formation by infants, it is entirely unknown
whether the asymmetrical face race experience has any other down-
stream consequences. Recent studies have shown that preschool-
ers by 3 years of age not only recognize own- race faces better, but
also are biased to associate own- race faces with positive emotional
valence and other- race faces with negative emotional valence (e.g.
Dunham, Chen, & Banaji, 2013; Qian et al., 2016; Xiao et al., 2015; for
reviews, see Dunham, Baron, & Banaji, 2008; Lee, Quinn, & Heyman,
in pres

s)

. However, it is entirely unclear whether such biases already
exist in infancy, and more specifically whether infants, like children,
also associate own- race faces with positive valence and other- race
faces with negative valence. The present study aimed to bridge this
important gap in the literature.

It is reasonable to expect that infants may associate own- race
faces with positive valence, given that much of infant own- race face
experience is acquired through direct interaction with own- race adults
who typically convey positive emotional signals. These positive emo-
tional signals are commonly carried through positive facial expressions
(Malatesta & Haviland, 1982), infant- directed speech (Kim & Johnson,
2014; Trainor, Austin, & Desjardins, 2000), and haptic interaction
(Hertenstein & Campos, 2001; Hertenstein, Holmes, McCullough, &
Keltner, 2009). Owing to the co- occurrence of positive emotional sig-
nals and own- race faces, infants may learn to associate own- race in-
dividuals with positive valence. Although no direct evidence supports
this possibility, existing studies have shown that familiarity plays an
important role in the associations infants make between faces and
positive valence. Specifically, infants tend to associate familiar faces
with positive emotional signals. For example, they associate happy
facial expressions with happy voices when face and voice belong to
their mother, but not when they are from strangers (Kahana- Kalman
& Walker- Andrews, 2001; Montague & Walker- Andrews, 2002). Thus,
given the fact that own- race faces are relatively more familiar than
other- race faces, infants might also associate novel own- race faces
with positive valence. The present study directly tested this ‘own race
is positive’ hypothesis regarding own- race faces.

In contrast, no evidence exists regarding whether infants associate
other- race faces with negative valence. Infants may associate nega-
tive emotional valence with other- race faces because infants develop
stranger anxiety towards unfamiliar own- race individuals, with the
anxiety becoming stronger with age (e.g. Bigelow, MacLean, Wood, &
Smith, 1990; Bronson, 1972). For example, 9- month- olds show accel-
erating heart rate when seeing a stranger of their own race, which is

not observed in infants at 5 months. This finding suggests that infants
between 5 and 9 months develop fearful responses towards unfamil-
iar individuals (Campos, Emde, Gaensbauer, & Henderson, 1975). Given
that other- race faces are perceptually different from faces of own- race
strangers in terms of salient facial information (Anzures, Quinn, Pascalis,
Slater, & Lee, 2010), infants may show even stronger ‘stranger anxiety’
towards other- race faces. Thus, it is plausible that, with increased age,
infants will come to associate negative valence with other- race faces.
According to this hypothesis, infants may treat other- race faces funda-
mentally differently from novel own- race faces by associating other- race
faces with negative emotional signals. The present study also directly
tested this ‘other race is negative’ hypothesis regarding other- race faces.

In order to test the above two hypotheses concurrently regard-
ing own- and other- race faces, we developed a novel intermodal
association paradigm. A typical intermodal association task involves
the presentation of stimuli in two modalities sequentially or simul-
taneously. The association is assessed by examining the different re-
sponses between ‘congruent’ and ‘incongruent’ trials. On congruent
trials, the stimuli in the two modalities share a certain commonality,
such as happy expressive faces paired with happy voices. By contrast,
on incongruent trials, the characteristics in one modality are not con-
sistent with the characteristics in the other modality, such as happy
expressive faces paired with sad voices. Existing studies using such
intermodal association paradigms have consistently found that infants
associate audio and visual signals on the basis of speech content (Kuhl
& Meltzoff, 1984; Patterson & Werker, 2002, 2003; Pons, Lewkowicz,
Soto- Faraco, & Sebastián- Gallés, 2009), emotional valence (Hietanen,
Leppänen, Illi, & Surakka, 2004; Soken & Pick, 1992), gender informa-
tion (Hillairet de Boisferon et al., 2015; Patterson & Werker, 2002),
age characteristics (Bahrick, Netto, & Hernandez- Reif, 1998), and face
race with native or non- native speech (Uttley et al., 2013). However,
no such study has examined the association between face race and
emotional valence. In the current study, we paired unfamiliar own- or
other- race neutral faces sequentially with positive or negative audi-
tory signals in order to examine the associations infants make between
own- versus other- race faces and positive versus negative valence.
The positive versus negative auditory signals were delivered by pre-
senting happy versus sad musical excerpts.

Our paradigm capitalizes on the ability that infants as young as
3 months have to discriminate between faces from different races
(Kelly et al., 2005, 2009; Kelly, Liu et al., 2007; Kelly, Quinn et al.,
2007; Liu, Xiao, Xiao et al., 2015). Furthermore, convergent evidence
suggests that adults and children can reliably identify the emotional
valence of happy and sad musical excerpts (Adachi, Trehub, & Abe,
2004; Balkwill & Thompson, 1999; Balkwill, Thompson, & Matsunaga,
2004; Dalla Bella, Peretz, Rousseau, & Gosselin, 2001; Juslin & Laukka,
2003; Kratus, 1993; Rock, Trainor, & Addison, 1999; Schmidt, Trainor,
& Santesso, 2003; Trainor & Trehub, 1992; for a review, see Trainor
& Corrigall, 2010). More relevant to the present study, studies have
shown that infants between 5 and 9 months are also capable of dis-
criminating happy and sad musical excerpts (Flom, Gentile, & Pick,
2008; Flom & Pick, 2012). They can additionally match happy music
with happy facial expressions (Gentile, 1998; Nawrot, 2003). These

     |  3 of 10XIAO et Al .

studies together suggest that infants can distinguish musical excerpts
in terms of positive versus negative valence.

Using a between- subjects design, we presented four groups
of Chinese 3- to 9- month- olds with videos of either congruent
or incongruent trials. On own- race congruent trials, infants saw
a series of videos of own- race faces with neutral expressions that
were sequentially paired with a series of happy musical excerpts.
On other- race congruent trials, infants saw a series of videos of
other- race faces with neutral expressions that were sequentially
paired with a series of sad musical excerpts (Figure 1). On incon-
gruent trials, the pairings between the race of the faces and the
valence of the musical excerpts were reversed. We examined how
long infants would maintain their attention to the face–music
pairings on the congruent versus incongruent trials. Because
repeated presentation of the same stimulus leads infants to ha-
bituate and thus rapidly decrease attention to the stimulus, we
presented novel faces and novel musical excerpts sequentially that
were never repeated. Presenting stimuli in different modalities is
known to sustain infant attention and to prevent rapid habituation
(Althaus & Mareschal, 2014; Reynolds, Zhang, & Guy, 2013).

We hypothesized that if the above two hypotheses regarding
own- and other- race faces are correct, infants should associate pos-
itive music with own- race faces and negative music with other- race
faces. Consequently, infants should show greater attention towards
the face–music stimuli on the congruent trials than on the incongruent
trials. These predictions are based on the findings that cross- domain
congruency promotes infant exploration of visual and auditory stimuli,
thereby making infants less likely to habituate and leading to longer
maintenance of looking time (Bahrick & Lickliter, 2000; Grossmann,
Striano, & Friederici, 2006; Kubicek et al., 2014). Moreover, because
we hypothesized that the own–positive and other–negative associ-
ations reflect asymmetric face race experience, and given that per-
ceptual specialization for own- relative to other- race faces increases
between 3 and 9 months (e.g. Kelly, Quinn et al., 2007; Kelly et al.
2009; Quinn et al., 2016), we predicted that the associations would
become increasingly evident across the age range tested.

2   |   M E T H O D

2.1 | Participants

A total of 193 full- term Chinese infants from 3 to 9 months of age par-
ticipated in the current experiment after their caregivers gave informed
consent. They were recruited from a community hospital in a large
metropolitan city in China where the infants came to receive wellness
checkups. Forty- nine infants participated in the own- race + happy-
music condition (M = 189.43 days, SD = 66.82 days), 49 infants par-
ticipated in the other- race + sad- music condition (M = 192.57 days,
SD = 65.93 days), 50 infants participated in the own- race + sad- music
condition (M = 188.74 days, SD = 67.50 days), and 45 infants partici-
pated in the other- race + happy- music condition (M = 186.13 days,
SD = 66.55 days). Based on caregiver report, infants had not had any
prior direct contact with individuals from other races. The city from
which the infants were recruited is racially homogenous, with 99.99%
of the population being Han Chinese. None of the infants had previ-
ously seen the face stimuli used in the current study.

We also surveyed infant exposure to happy and sad music in the
parents of 67 infants out of the whole sample. According to parent
reports, 82% (N = 55) of the infants had frequently experienced happy
music, which was derived from toys, songs and TV programs, whereas
18% (N = 12) of the infants had occasionally experienced sad music
from such occurrences as watching a sad TV program or attending a
funeral. A chi- squared goodness- of- fit test showed that more infants
had been exposed to happy music than to sad music (χ2 = 15.38,
p < .001). None of the infants had been previously exposed to the mu- sical stimuli used in the current study.

Twenty- nine additional infants participated, but were excluded
from the data analysis because of failure to complete the procedure
owing to fussiness (n = 20: nown-happy = 4, nown-sad = 2, nother-happy = 9,
nother-sad = 5), calibration failure (n = 3), extremely short total looking
time across the session (i.e. <1 s for each trial, n = 2), parent interfer- ence (n = 2), or premature birth (n = 2). Experiments were approved by the Research Ethics Boards of the University of Toronto and by the

FIGURE 1 The stimulus sequences in the two sets of conditions. In the own- race conditions (the top row), Asian face videos were
sequentially paired with happy musical excerpts in the congruent condition, and with sad musical excerpts in the incongruent condition. In the
other- race conditions (the lower row), African face videos were sequentially paired with sad musical excerpts in the congruent condition, and
with happy musical excerpts in the incongruent condition. When the musical excerpts were played, a crosshair appeared in the middle of the
screen

Face 1 Face 2 Face 3 Face 4 Face 5 Face 6Music 1 Music 2 Music 3 Music 4 Music 5 Music 6

4 of 10  |     XIAO et Al .

Institutional Ethics Board of Zhejiang Sci- Tech University. Informed
consent was obtained from the caregivers of the infants.

2.2 | Stimuli

Videos of six Asian and six African females with frontal views were used
as face stimuli (Age: 21 to 28 years). Each video depicted a face count-
ing numbers silently with a neutral facial expression. The reason why we
presented moving face videos, instead of static face images, was because
prior studies have consistently shown that infants tend to perceive neutral
static faces as emotionally negative (i.e. the still- face effect, Adamson &
Frick, 2003; Toda & Fogel, 1993). The videos were edited to ensure that
faces were similar in size, and placed on a light color background (Figure 1).
In addition, we ensured that the models from both races spoke and moved
at the same tempo, which was achieved by asking the models to count the
numbers at a steady pace. We then used video editing software (Adobe
Premiere Pro) to adjust the speed of each video, thereby ensuring that
each model moved their mouth 10 times (counted 10 numbers) within
10 s. Thus, each face moved at the same tempo. We measured the pace
of the facial movements of the models and found that the own- and other-
race adults did not differ in their facial movement tempo (Mown = 10,
SDown = 0, Mother = 10, SDother = 0). Each face video was played for 10 s.

We also assessed the attractiveness and emotional valence of
the face stimuli by raters who were blind to the purpose of the study.
Twelve Asian female adults (22 to 28 years old) rated the attractive-
ness of the face stimuli with a 9- point Likert scale (1: very unattractive,
5: neutral, and 9: very attractive). The reason we included only females
for the facial attractiveness rating is because the current study used
only female faces and cross- gender attractiveness judgments are less
reliable than same- gender attractiveness judgments (Rhodes, Hickford,
& Jeffery, 2000; Sofer, Dotsch, Wigboldus, & Todorov, 2015). A paired-
sample t- test was used to examine whether the mean attractiveness
rating for own- race faces differed from that for other- race faces. The
results showed that the attractiveness of the own- race Asian faces
(M = 3.47, SD = 1.47) was not significantly different from the attractive-
ness of the other- race African faces (M = 3.63, SD = 1.38), t[11] = 1.04,
p = .323. Twelve additional Asian adults (23 to 26 years old, 6 females
and 6 males) rated the emotional valence of the face stimuli. A 7- point
Likert scale was used (1: very negative, 4: neutral, and 7: very posi-
tive). Neither the Asian (M = 4.05, SD = 0.40) nor the African (M = 4.14,
SD = 0.50) faces differed significantly from neutral (one- sample t- test:
ps > .068). Moreover, the Asian and African faces did not differ from
each other in valence (paired- sample t- test: t[11] = 0.92, p = .378).

Each musical excerpt was a piano piece, and, like each face video,
also lasted 10 s. Six of the excerpts conveyed positive (happy) emotion
and another six conveyed negative (sad) emotion. We matched each mu-
sical excerpt to the same perceived loudness (−23 dB). Since the time of
Euler, emotion in music has been shown mathematically and empirically
to be conveyed primarily by scale and tempo (Gabrielsson & Lindström,
2001; Pesic, 2014). Thus, we specifically chose happy and sad musical
excerpts that differed in these two key musical properties so as to en-
sure that the excerpts clearly presented happy and sad emotional va-
lences. The positive musical excerpts were thus in the major scale with

fast tempo (184.47 to 275.23 bpm). The negative musical excerpts were
in the minor scale with slow tempo (48.30 to 146.25 bpm). In order to
examine whether the musical excerpts indeed conveyed happy versus
sad emotional valence, 12 Asian adult raters (25 to 33 years old, seven
females and five males), who had not received formal musical training,
rated the emotional valence of the musical excerpts. The raters were
blind to the purpose of the study. Each musical excerpt was rated accord-
ing to a 7- point Likert scale (1: very sad, 4: neutral, and 7: very happy).
The happy musical excerpts were rated as significantly happier than
neutral (M = 6.29, SD = 0.36, one- sample t- test: t[11] = 21.85, p < .001), and the sad musical excerpts were rated as significantly more sad than neutral (M = 2.45, SD = 0.59, one- sample t- test: t[11] = −9.10, p < .001).

2.3 | Procedure

Each infant was randomly assigned to one of the four face- race + music
conditions. In the own- race + happy- music condition (own- happy), in-
fants watched six Asian face videos sequentially paired with six musical
excerpts in the following manner. First, a face video was shown for 10 s,
followed by a happy musical excerpt for 10 s, and then a new video with
a new face appeared, followed by a new happy musical excerpt, and so
on until all six face videos and six musical excerpts had been played.
A crosshair appeared on the screen when each musical excerpt was
played. Each participant thus saw six Asian faces interleaved with six
positive musical excerpts. The sequence of the six specific face videos
with the six specific musical excerpts was randomized across partici-
pants. The other- race + sad- music (other- sad), own- race + sad- music
(own- sad), and other- race + happy music (other- happy) conditions were
procedurally the same as the own- happy condition, except for the face-
music composition. African faces and sad musical excerpts were used in
the other- sad condition. African faces and happy musical excerpts were
used in the other- happy condition. Asian faces and sad musical excerpts
were used in the own- sad condition. Following the convention of the
existing literature, we refer to the own- happy and other- sad conditions
as the congruent conditions, and the other two conditions as the incon-
gruent ones (see Figure 1 for a schematic depiction of the procedure).

Infant eye movements were recorded by a Tobii 1750 eye tracker
(50- Hz sampling rate). Each testing session started with an infant-
controlled calibration program to ensure eye tracking precision and
accuracy. During calibration, a cartoon figure was presented on the
screen. If infants successfully fixated on the cartoon figure for 1 s, it
would move to another position. The calibration was achieved when
infants successfully fixated at five locations (four corners and the cen-
ter). Raw eye- tracking data were first filtered to generate the fixation
data. A fixation was defined as at least 100 ms of continuous looking
with a spatial dispersion of no more than 30 pixels (Liu et al., 2011).

3   |   R E S U LT S

We first examined looking time on the first face video in all four condi-
tions because at that point the musical excerpts with different emotional
valences had not been played. We conducted a multi- variable linear

     |  5 of 10XIAO et Al .

regression on the first face looking time as the predicted variable, with
age in days, face race, and their interactions as the predictors. The results
revealed only a significant main effect of age (F[1, 186] = 8.52, p = .004,
η2P = .04): as age increased, looking time on the first face also increased
regardless of face race. However, no significant effects were observed
for face race or any of the interaction terms (ps > .460). Infants spent a
similar amount of time looking at own- race faces (M = 7.18 s, SD = 2.86 s)
and other- race faces (M = 6.90 s, SD = 2.55 s). These results indicate that
own- and other- race faces alone were insufficient to elicit a difference in
looking time. It should be noted that three infants did not look at the first
face but looked at the rest of the faces. We excluded these infants in the
statistical analyses for the first face looking time, but included them in
the subsequent analyses, so the mismatched df values for those analyses
reflected this situation.

The analyses to follow emphasize two aspects of the association
between face race and music emotional valence: (1) developmental
change at the level of individual performance, using age as a contin-
uous variable, and (2) emergence of an association in developmental
time at the level of group performance, in which infant looking is com-
pared across three age groups: 3, 6, and 9 months of age.

3.1 | Developmental change in the association of
face race and music emotional valence

Each infant’s looking times to the subsequent five faces were summed
to provide an index of their total looking time to the five faces after

happy or sad musical excerpts were played. We conducted a multi-
variable linear regression similar to the one described above. Total
looking time was the predicted variable, with age in days, face race,
musical emotion, and their interactions as the predictors. The results
revealed a main effect of age (F[1, 185] = 15.22, p < .001, ηP

2 = .08),
indicating an age- related increase in total face looking time. The
results also revealed a significant race × emotion interaction (F[1,
185] = 5.63, p = .019, ηP

2 = .03). More importantly, there was a sig-
nificant race × emotion × age interaction (F[1, 185] = 21.56, p < .001, ηP

2 = .10), showing that the relationship between age and face looking
time was modulated by face race and emotion (Figure 2). This three-
way interaction indicated that with increased age, infants had differ-
ent face looking responses when the faces were paired with congruent
musical excerpts versus incongruent musical excerpts. We did not
observe any other significant main effects or interactions (ps > .109).

Given the significant three- way interaction, we used Pearson cor-
relation analyses to examine the linear relationship between total face
looking time and participant age in days in each condition. As shown
in Figure 2, for the own- happy condition, the analysis revealed a sig-
nificant positive correlation between own- race face looking time and
age (r = .55, p < .001). Looking time of the infants for own- race faces increased with age if the faces were presented with happy musical ex- cerpts. In contrast, other- race face looking time of the infants increased with age when the faces were presented with sad musical excerpts (r = .59, p < .001). Thus, with increased age, infants became increasingly attentive to congruent face- music sequences: own- race faces presented

FIGURE 2 Each infant’s total face
looking time as a function of age in the
four conditions. The blue line represents
the linear regression line between face
looking time and participant age. Each
panel presents the looking time and
age correlation for a given experimental
condition. The value in the upper- right
corner indicates the Pearson correlation
coefficient for each condition. The asterisks
indicate that the correlation was significant
(p < .05)

r = .55* r = .01

r = -.12 r = .59*

Own-Race Happy Music Own-Race Sad Music

Other-Race Happy Music Other-Race Sad Music

0

10

20

30

40

50

60

0
10
20
30
40
50
60

100 150 200 250 300 100 150 200 250 300
Age (days)

F
ac

e
lo

ok
in

g
ti

m
e

(s
ec

s)

6 of 10  |     XIAO et Al .

with happy music and other- race faces presented with sad music. We
examined whether the correlation coefficient in the own- happy condi-
tion differed from that in the other- sad condition by using a Fisher r- to- z
transformation. The results showed no significant difference between
the two correlation coefficients (z = 0.31, two- tailed p = .756).

For the two incongruent conditions, we did not observe significant
correlations between face looking time and age in the own- sad con-
dition (r = .01, p = .952) or other- happy condition (r = –.12, p = .428),
which were not different from each other (z = 0.62, p = .535). Thus,
when the face–music compositions were incongruent, the face look-
ing time of infants did not systematically change with increased age.
Moreover, the correlation coefficient for the own- happy condition
was significantly higher than that for the own- sad condition (z = 2.92,
p = .003), and the correlation coefficient for the other- sad condi-
tion was significantly higher than that for the other- happy condition
(z = 3.75, p < .001). These results suggest that, with increased age, infants increasingly associate own- race faces with happy music, and other- race faces with sad music.

3.2 | Emergence of the association of face race and
music emotional valence in developmental time

The results just described showed developmental trends in face look-
ing time as a function of the associations of face race and music emo-
tional valence. We further explored the emergence of the associations
by determining the age at which infants showed different patterns
of looking time on the faces for the happy and sad music emotional
valence conditions. We split participants into three age groups (i.e.
3- , 6-, and 9- month- old groups) according to the distribution of their
age in days. Table 1 shows the number of participants in each age
group for each of the four conditions.

We performed a series of independent sample t- tests to examine
the effects of music emotional valence on the looking time for own-
and other- race faces in each age group. As shown in Figure 3, infants
at 9 months of age looked longer at own- race faces paired with happy
music (M = 39.44 s) than at own- race faces paired with sad music
(M = 28.25 s), t(32) = 3.30, p = .002. Nine- month- olds also looked
longer at other- race faces paired with sad music (M = 38.69 s) than at
other- race faces paired with happy music (M = 19.14 s), t(29) = 5.91,
p < .001. By contrast, we did not find any effect of music emotional valence on face looking time in 3- month- olds (own- race faces:

t[28] = 0.71, p = .481; other- race faces: t[27] = 0.563, p = .578) or
6- month- olds (own- race faces: t[33] = 0.20, p = .846; other- race faces:
t[32] = 0.73, p = .471). These results suggest that infants at 3 and
6 months of age did not associate own- race faces with happy music or
other- race faces with sad music. At 9 months, infants were significantly
more inclined to associate own- race faces with happy music than with
sad music, and other- race faces with sad music than with happy music.

4   |   D I S C U S S I O N

We used an intermodal association paradigm to investigate the de-
velopment of association for own- and other- race neutral faces with
happy versus sad music from 3 to 9 months of age. Specifically, we
relied on infant looking time to test whether infants associate own-
and other- race faces differentially with music of different emotional
valences. Two major findings were obtained.

First, infants from 3 to 6 months of age did not show any differ-
ences in looking time to the own- versus other- race faces when they
were paired with musical excerpts that conveyed happy or sad emo-
tions, supporting a ‘no association’ hypothesis. This outcome indicates
that infants initially did not associate face race with music emotional
valence, suggesting that infants are not biologically predisposed to
associate own- and other- race faces with music of differential emo-
tional valence. The finding that infants from 3 to 6 months did not
associate other- race faces with sad music differs from a prior result
that infants at 6 months associated other- race faces with non- native
speech (Uttley et al., 2013). The difference in outcomes might indicate
that the association beween face race and language emerges earlier
than that between face race and music emotional valence.

Our second major finding is that, unlike the younger infants, in-
fants at 9 months looked longer at own- race faces paired with happy
music, and at other- race faces paired with sad music. This age- related
change cannot be explained by the stimulus characteristics of face or
music alone because we used exactly the same faces and musical ex-
cerpts in the incongruent conditions. In the incongruent conditions,
infant attention to the same faces did not change with increased age
when the faces were presented with incongruent music (i.e. own- race
faces paired with sad music, and other- race faces paired with happy
music). This second major finding thus supports the hypothesis that
older infants associate face race with music emotional valence: they

TABLE 1 Number of participants and mean age in days for each age group and condition

Condition

3 months
(79–152 days)

6 months
(173–217 days)

9 months
(242–297 days)

N Mean SD N Mean SD N Mean SD

Own- race happy music 13 97.69 10.65 19 184.79 2.82 17 264.76 20.23

Own- race sad music 17 112.71 17.42 16 182.81 3.60 17 270.35 19.55

Other- race happy music 16 113.06 20.22 15 185.80 9.03 14 270.00 16.92

Other- race sad music 13 100.31 13.86 19 192.11 12.49 17 263.65 20.89

Total 59 106.76 17.37 69 186.57 8.71 65 267.06 19.35

     |  7 of 10XIAO et Al .

associate own- race faces with happy music and other- race faces with
sad music.

To our knowledge, the present study is the first to document the
development of associations of own- and other- race faces with music
of different emotional valences during the first year of life. This emerg-
ing association likely builds on the existing abilities of infants as young
as 5 to 6 months of age to decode face race and music emotional va-
lence information. As mentioned in the introduction, infants as young
as 6 months can readily extract race- specific information from the
faces they are viewing (Anzures et al., 2013; Quinn et al., 2016). The
face stimuli used in the present study were chosen to capitalize on
this early emerging ability in infants. Infant ability to process music
emotional valence has been revealed with the use of musical excerpts
differing in such important acoustic properties as tempo (fast vs. slow)
and scale (major vs. minor). In particular, it is well established that music
in a major scale with fast tempo universally conveys happy emotional
valence, whereas music in a minor scale with slow tempo conveys
sad emotional valence (Gabrielsson & Lindström, 2001; Pesic, 2014),
with a strong neural basis (e.g. Mitterschiffthaler, Fu, Dalton, Andrew,
& Williams, 2007). Evidence shows that, from as early as 5 months,
infants are able to discriminate happy and sad musical excerpts (Flom
et al., 2008; Flom & Pick, 2012). They also can match happy music with
happy facial expressions (Gentile, 1998; Nawrot, 2003). The musical
excerpts used in the present study thus took advantage of the ability
of infants to decode music emotional valence. Overall, then, the infant
findings suggest that infants as young as 5 to 6 months of age not only
can decode face race information, but also can detect emotional va-
lence in music. By relying on the existing abilities of infants to process
face race and music emotional valence information, here we were able
to reveal that 9- month- olds, but not younger infants, associated face
race with music emotional valence.

The reason that infants associated own- race neutral faces with
happy music may reflect the fact that infants primarily see own- race
faces (Rennels & Davis, 2008; Sugden et al., 2014), which mostly pose
positive expressions (Malatesta & Haviland, 1982) and deliver joyful
infant- direct speech (Kim & Johnson, 2014; Trainor et al., 2000). In ad-
dition, the survey results about music exposure of the infants in our
sample revealed that more were exposed to happy music than to sad
music. As a result, they may develop a specific association to perceive

own- race faces as emotionally positive entities, even if the faces re-
main expressively neutral.

We also found that 9- month- olds, but not 3- or 6- month- olds, asso-
ciated neutral other- race faces with sad musical excerpts. Because the
infants in the current study had no previous direct experience with other-
race individuals, the emergence of the negative emotional association
with other- race faces must not have arisen from direct negative expe-
rience with other- race individuals. One possible explanation is stranger
anxiety. Extensive studies have shown that human infants display neg-
ative affective reactions towards own- race strangers in the first year of
life (Bigelow et al., 1990; Feinman, 1980). For example, 9- month- old in-
fants show wariness to strangers (Bronson, 1972), and this stranger anx-
iety develops with age within the first year of life (Campos et al., 1975).
Given that other- race faces are more perceptually different than stranger
own- race faces (relative to familiar own-race faces), infants may perceive
the former as even more strange than the latter. As a result, infants may
associate negative emotional valence with other- race faces.

Thus, the developmental differences in face race and musical va-
lence association may reflect the asymmetrical experience of infants
with both face race and musical valence. In other words, this biased
association may be based on familiarity. Owing to their familiarity with
own- race faces and happy music, infants develop a specific associa-
tion to perceive own- race faces as emotionally positive entities, even
if the faces remain expressively neutral. In the same vein, owing to
their unfamiliarity with other- race faces and sad music, they associate
other- race faces with sad music. This experience- based cross- modal
association is consistent with a growing body of literature showing
that infant social cognition is shaped by experience (Waxman, 2012,
2013). For example, older infants exhibit increased toy acceptance
(Kinzler, Dupoux, & Spelke, 2007; Kinzler & Spelke, 2011), proso-
cial action (Cirelli, Einarson, & Trainor, 2014), and imitative behavior
(Buttelmann, Zmyj, Daum, & Carpenter, 2013) towards individuals
who share similar characteristics with the infant’s own experience,
such as speech accent and movement synchrony.

Alternative explanations for our findings should be entertained.
First, one possibility is that infants simply match the tempo of the
music with the speech tempo of the faces. However, as reported in the
Method section, the way that the face videos were created ensured that
there were no differences in the tempos of the own- and other- race

FIGURE 3 Means of total looking time
on the own- and other- race faces paired
with happy or sad music for each age
group. The asterisks indicate a significant
difference in face looking time when the
faces were paired with happy versus sad
music (independent sample t- test, p < .05). Each error bar represents a unit of standard error

8 of 10  |     XIAO et Al .

face stimuli. Second, as infants are known to be more experienced with
processing own- race faces, it is possible that they may process own-
race faces faster than other- race faces. As a result, they match the more
rapidly processed own- race faces to the faster tempo of happy music.
However, even though it is well established that infants at 9 months of
age discriminate own- race faces better than other- race faces, no evi-
dence suggests that they process the former faster than the latter. For
example, several studies have shown that infants habituate to own- race
faces no faster than to other- race faces (e.g. Kelly, Quinn et al., 2007),
and at least one study has reported the opposite effect whereby infants
show more rapid habituation to other- race faces relative to own- race
faces (Anzures et al., 2010). In addition, using ERP (event-related po-
tential) methodology, Balas, Westerlund, Hung, and Nelson (2011) have
shown that infants do not differ in their neural response latency in face-
relevant ERP components (i.e. N290 and P400). The existing evidence
thus suggests that infants do not have a speed- of- processing advan-
tage for own- race faces. Similarly, existing studies have not revealed
processing speed differences between happy and sad music in infants
(Flom et al., 2008; Flom & Pick, 2012).

Although we have reasoned that experience (i.e. familiarity) un-
derlies the development of the linkage between face race and music
emotional valence, future studies need to ascertain exactly how famil-
iarity engenders the linkage between face race and musical valence
in infancy. One possibility is that infants simply associate whatever
is visually familiar (or unfamiliar) with whatever is auditorially familiar
(or unfamiliar) regardless of the nature of the visual and auditory stim-
uli. A second possibility is that infants may associate own- race faces
with happy music because both types of familiar stimuli evoke posi-
tive responses, and associate other- race faces with sad music because
both types of unfamiliar stimuli evoke negative responses. To examine
these possibilities, following from the work of Heron- Delaney et al.
(2011) and Scott and Monesson (2009), one could longitudinally ex-
pose infants from 3 months of age to emotionally sad music and then
test whether the infants at 9 months would associate sad or happy
music with own- race faces. However, ethical considerations would
preclude such a manipulation. Alternatively, one could longitudinally
expose infants from 3 months of age to faces belonging to a race other
than their own to examine whether familiarity with the faces of this
race will cause them to associate these other- race faces with happy,
rather than sad, music at 9 months of age. In such studies, in addi-
tion to measuring visual attention, one needs also to measure infant
emotional responses using such methods as BabyFACS (Oster, 2004).
For example, one could use the infant visual attention and emotional
responses together to ascertain whether the association between face
race and music valence is established via emotional responses to the
musical excerpts, to the faces, or to both. Overall, studies and mea-
sures of this kind will help disambiguate among different possibilities
concerning how the linkage between face race and music emotional
valence emerges.

The present findings showing that infants associate face race and
music emotional valence is in accord with evidence from older children
and adults. Extensive research with adults has consistently shown that
adults perceive own- race individuals more positively than other- race

individuals and treat them more favorably (Dunham et al., 2013; Hardin
& Banaji, 2013; Pascoe & Richman, 2009). Recently, preschoolers have
been shown to have implicit racial biases (Baron & Banaji, 2006; Qian
et al., 2016). For example, when presented with a racially ambiguous
face displaying positive or negative emotion, preschoolers, like adults,
categorized the face with positive emotion as own- race, but the same
face with negative emotion as other- race (Dunham et al., 2013; Raabe
& Beelmann, 2011; Xiao et al., 2015). This race- based social categori-
zation is similar to what was observed in the current study with infants.

The similarity between the infant and child–adult findings suggests
that the associations that infants form between face race and music
emotional valence might be a precursor to the implicit racial biases of
children and adults (Baron & Banaji, 2006; Hugenberg & Bodenhausen,
2004). This possibility is supported by recent findings showing that per-
ceptual factors can influence implicit racial bias. In particular, studies have
reported that increasing perceptual experience with other- race faces can
significantly reduce implicit racial bias in children and adults (Lebrecht,
Pierce, Tarr, & Tanaka, 2009; Xiao et al., 2015). Thus, it is possible that
there is a connection between emotional associations with own- and
other- race faces in infancy and the emergence of racial biases in child-
hood. Future studies using a longitudinal design should test this intriguing
hypothesis. If the associations of infants are shown to be connected to
the pervasive racial biases in children and adults, then, considering their
negative consequences at individual and societal levels (e.g. Banaji &
Greenwald, 2013; Hardin & Banaji, 2013; Pascoe & Richman, 2009), early
intervention in infancy may help to reduce such biases, potentially fore-
stalling their emergence and related negative consequences later in life.

A C K N O W L E D G M E N T S

This research was supported by grants from the Natural Science and
Engineering Research Council of Canada, the National Institutes of
Health (R01 HD046526), the National Science Foundation of China
(31671146, 31070908, 31300860, and 31470993), and the Zhejiang
Provincial Natural Science Foundation of China (LY16C90006). We
thank two anonymous reviewers for their comments, and Jun Li,
Dandan Zhu, and Jing Bao for their assistance in data collection.

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How to cite this article: Xiao NG, Quinn PC, Liu S, Ge L, Pascalis
O, and Lee K. Older but not younger infants associate own- race
faces with happy music and other- race faces with sad music.
Dev Sci. 2018;21:e12537. https://doi.org/10.1111/desc.12537.

https://doi.org/10.1111/desc.12537

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Article

Places and Postures:
A Cross-Cultural Comparison of
Sitting in 5-Month-Olds

Lana B. Karasik1, Catherine S. Tamis-LeMonda2,
Karen E. Adolph2, and Marc H. Bornstein3

Abstract
Motor development—traditionally described in terms of age-related stages—is typically studied
in the laboratory with participants of Western European descent. Cross-cultural studies typically
focus on group differences in age-related stages relative to Western norms. We adopted a
less traditional approach: We observed 5-month-olds and their mothers from six cultural
groups around the world during 1 hr at home while they engaged in natural daily activities. We
examined group differences in infants’ sitting proficiency, everyday opportunities to practice
sitting, the surfaces on which sitting took place, and mothers’ proximity to sitting infants. Infants
had opportunities to practice sitting in varied contexts—including ground, infant chairs, and
raised surfaces. Proficiency varied considerably within and between cultural groups: 64% of the
sample sat only with support from mother or furniture and 36% sat independently. Some infants
sat unsupported for 20+ min, in some cases so securely that mothers moved beyond arms’
reach of their infants even while infants sat on raised surfaces. Our observations of infant sitting
across cultures provide new insights into the striking range of ability, varied opportunities for
practice, and contextual factors that influence the proficiency of infant motor skills.

Keywords
sitting, infants, motor development, cross-cultural

Motor development—perhaps more than any other area of developmental science—falls victim
to assumptions of universality (Adolph, Karasik, & Tamis-LeMonda, 2010a; Adolph & Robinson,
2015; Karasik, Adolph, Tamis-LeMonda, & Bornstein, 2010). Children are expected to display
postural, manual, and locomotor skills in an invariant sequence regardless of cultural or contex-
tual influences. This assumption can be traced to the standardization of motor skills in the 1930s
and 1940s. Based on observations from homogeneous samples of U.S. middle-class infants of
European descent, Shirley (1931), McGraw (1945), and Gesell (1946) identified a series of motor
accomplishments during infants’ first two postnatal years and established a corresponding set of

1College of Staten Island and Graduate Center, City University of New York, NY, USA
2New York University, New York City, NY, USA
3Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD, USA

Corresponding Author:
Lana B. Karasik, Department of Psychology, College of Staten Island, City University of New York, 2800 Victory Blvd.
4S-220, Staten Island, NY 10314, USA.
Email: lana.karasik@csi.cuny.edu

593803 JCCXXX10.1177/0022022115593803Journal of Cross-Cultural PsychologyKarasik et al.
research-article2015

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1024 Journal of Cross-Cultural Psychology 46(8)

developmental norms. These motor skills became standard items on screening tests, and the
norms provided the basis for developmental assessment tools, including the Bayley Scales of
Infant Development (1969, 1993), Alberta Infant Motor Scale (Piper & Darrah, 1994), and Denver
Developmental Screening Test (Frankenburg & Dodds, 1967; Frankenburg, Dodds, Archer,
Shapiro, & Bresnick, 1990). In fact, the classic motor milestone chart with accompanying onset
ages has become the gold standard of motor development and is prominently displayed in devel-
opmental textbooks, pediatrician’s offices, and parenting books. Infants from other cultures are
typically described as “precocious” or “delayed” relative to norms established with Western
infants (see Adolph & Robinson, 2015; Werner, 1972, for review).

Contemporary developmental science has come a long way since the standardization of motor
skills. Researchers today focus on the proficiency of infants’ skills at sitting, crawling, and walk-
ing, and the adaptability of their actions in response to local conditions. For example, infants’
postural sway and limit of stability reveal proficiency at keeping balance in a sitting position
(Harbourne & Stergiou, 2003; Woollacott, 1986), and gait characteristics reflect speed, ampli-
tude, and consistency of movements while crawling or walking (Hallemans, De Clercq, Otten, &
Aerts, 2005; Ivanenko, Dominici, Cappellini, & Lacquaniti, 2005; Patrick, Noah, & Yang, 2009).
Adaptability is assessed by infants’ ability to select and modify actions to navigate slopes, cliffs,
and other obstacles or to cope with changes in their bodies induced by carrying loads or wearing
platform or slippery-soled shoes (Adolph, 1997; Adolph & Avolio, 2000; Adolph, Karasik, &
Tamis-LeMonda, 2010b; Cole, Gill, Vereijken, & Adolph, 2014; Kretch & Adolph, 2013). This
work highlights the striking intra- and inter-individual variability that characterizes motor devel-
opment in infants of the same age, as first described by the early pioneers yet soon overshadowed
by the focus on developmental norms (Adolph, Cole, & Vereijken, 2015).

Across contemporary research studies (Adolph & Robinson, 2015), the primary predictor of
individual differences in infant motor skills is experience, defined as the number of days between
skill onset age and test date. Days of experience predict infants’ ability to control posture and to
make adaptive decisions for action in sitting, crawling, and walking (Adolph & Robinson, 2015).
But, experience so defined is not an explanatory mechanism: What is missing in studies of motor
development is a description of infants’ everyday opportunities to practice specific skills in natu-
ral contexts (Adolph et al., 2012; Adolph & Robinson, 2015).

Cross-Cultural Research on Sitting

Like most research on motor development, research on infant sitting falls prey to over-reliance
on estimates of onset ages and lack of focus on infants’ natural opportunities to practice sitting.
To establish onset ages, researchers rely on maternal reports or elicit sitting in the laboratory;
both methods use an arbitrary “pass/fail” criterion such as 5, 10, or 30 s of sitting with or without
support (Adolph, 2000; Fishkind & Haley, 1986; Wijnhoven et al., 2004). However, reliance on
onset ages obscures the day-to-day variability of infant skills in natural settings (Adolph,
Robinson, Young, & Gill-Alvarez, 2008), such as how long infants typically sit and under what
conditions. Moreover, the contextual opportunities for sitting are ignored.

Cross-cultural research offers a unique window into inter-individual variability in sitting skills
and the social contexts of infant sitting. Early cross-cultural studies documented variability in
sitting onset ages by assessing group differences relative to Western norms. Infants in some
African and Caribbean cultures showed accelerated onset ages relative to Western infants
(Brazelton, 1973; Capute, Shapiro, Palmer, Ross, & Wachtel, 1985; Hopkins & Westra, 1989,
1990; Iloeje, Obiekwe, & Kaine, 1991; Keefer, Tronick, Dixon, & Brazelton, 1982; Kilbride,
Robbins, & Kilbride, 1970; Leiderman, Babu, Kagia, Kraemer, & Leiderman, 1973; Lohaus
et al., 2011; Vierhaus et al., 2011). Whereas Western norms report that 25% of infants achieve
independent sitting by 5.5 months and 90% by 7 months (Frankenburg, Dodds, Archer, Shapiro,

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Karasik et al. 1025

& Bresnick, 1992), infants in Uganda sat independently at 4 months (Geber & Dean, 1957) and
infants from the West Indies sat at 5 months (Hopkins & Westra, 1989); sitting was delayed by
months for infants in Brazil (Lopes, de Lima, & Tudella, 2009), Taiwan (Wu et al., 2008), and
Japan (Ooki, 2006) relative to Western norms. A cross-cultural investigation by the World Health
Organization (WHO; Martorell et al., 2006) indicated that infants from India, Ghana, Norway,
Oman, and the United States sat, on average, at 5.9 months, but sitting onset ages ranged from
3.8 months (1st percentile) to 9.2 months (99th percentile).

In terms of social context, motor skills emerge in the natural settings of infants’ lives. For
example, cross-cultural differences in sitting onset ages are linked with differences in child-
rearing practices (e.g., Bril & Sabatier, 1986; Hopkins & Westra, 1990; Lohaus et al., 2011;
Super, 1976; Vierhaus et al., 2011). Augmentation of infants’ movements can facilitate the acqui-
sition of sitting. Jamaican infants whose mothers massaged and exercised their limbs and put
them into sitting positions sat at earlier ages than did Jamaican infants whose mothers did not
engage in these practices (Hopkins & Westra, 1990).

Striking variability in onset ages across different cultural groups begs for examination of the
range of proficiency in infant sitting skills and contextual factors that influence the development
of those skills. However, cross-cultural research continues to compare infants on onset ages or
against standardized Western norms and consequently describes infants as “precocious” or
“delayed” (see Adolph & Robinson, 2015; Werner, 1972, for review) despite the limited value of
standard methods of motor assessment for non-Western children (e.g., Lohaus et al., 2011;
Vierhaus et al., 2011). Naturalistic contexts of everyday life can determine the opportunities
infants have to practice specific motor skills, which, in turn, have implications for when skills
emerge and the proficiency of infants’ skills.

Current Study

Here, we move beyond onset ages and standardized norms to consider infants’ sitting skill and
practice with sitting in an everyday home setting. Sitting, one of the most important skills in early
infancy is associated with advanced forms of object exploration and facilitates infants’ percep-
tion and cognition (Kretch, Franchak, & Adolph, 2014; Soska, Adolph, & Johnson, 2010). Rather
than reforming developmental norms, which would require a large representative sample, this
demonstration study analyzed naturalistic observations from targeted samples. We considered
the everyday opportunities for infants to practice sitting, infants’ sitting proficiency, and the sur-
faces on which sitting takes place (e.g., strapped in a baby chair with postural support or on the
floor dealing with challenges of maintaining balance).

We had three aims. First, we describe and compare the relative prevalence and proficiency of
independent sitting in 5-month-olds from six cultural communities around the world during
everyday routines at home. Rather than limiting sitting skill to a dichotomous measure of absence/
presence, we report skill proficiency based on the duration of infants’ natural bouts of sitting. In
typical laboratory studies of proficiency, sitting bouts end when infant topple over, when an
experimenter repositions infants into another posture, or when infants spontaneously transition
from sitting into a prone posture. However, previous work cannot speak of how sitting bouts end
in the course of everyday life. Spontaneous transitions would suggest greater proficiency than
falling. Second, we characterize natural opportunities for sitting by calculating the time infants
spend in supported and unsupported sitting positions, thus moving beyond the laboratory stan-
dard of eliciting independent sitting with a 10- or 30-s criterion. In principle, prior to independent
sitting, infants can practice sitting for extended periods with various supports (e.g., in specialized
furniture, in mother’s arms, propped on their hands in a “tripod” position). Thus, our third aim
was to describe the context of sitting in terms of the various surfaces on which infants sat and
mothers’ location relative to their sitting infants.

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1026 Journal of Cross-Cultural Psychology 46(8)

We focused on 5-month-olds because, according to Western developmental norms, most
infants do not yet sit independently but begin to sit in the coming months. On the WHO standards
(Martorell et al., 2006), fewer than 25% of infants sit independently at 5 months. Because infants
are still unable to sit independently, their placement and postures largely depend on opportunities
provided by their caregivers.

Method

Participants and Procedure

Video records of 72 mother–infant pairs, 12 dyads from each of six countries (Argentina,
Cameroon, Italy, Kenya, South Korea, and the United States) were randomly selected from a
large archival data set (Bornstein, Putnick, Suwalsky, & Park, 2014). We aimed to maximize
inter-group variability by including families from urban and rural settings and industrialized and
developing nations. South Korean and U.S. families were recruited from metropolitan areas
(Seoul, Washington, D.C.). Argentinian families were from a rural indigenous (Mestizos) popula-
tion from the outskirts of Córdoba. Nso infants (the largest ethnic group in Cameroon) included
both rural and urban communities. The sample from South Italy was from a farming community.
Kenyan families from the Kamba tribe were from the Bantu region, from both rural and urban
areas.

All infants were firstborn, healthy, and born at term. Infants averaged 5 months (±1 week) at
the time of observation. Approximately equal numbers of girls and boys were recruited from each
country (33 boys and 39 girls). The average age of mothers was 25 years (SD = 4.79). Table 1
presents socio-demographic characteristics of infants and mothers in the six cultures.

A researcher local to the host culture video recorded mother–infant pairs for 1 hr in the natural
setting of their homes at a time most convenient for families. Mother–infant pairs were unre-
stricted in terms of where they could be in their homes. In fact, many dyads across the culture
groups spent time outside of their home (i.e., in the yard) during the observation hour. During
observations, the researcher remained in the background and interacted minimally with infants
and mothers. Mothers were told that the purpose of the study was to document infants’ daily
routines and were instructed to go about their normal activities. Mothers were unaware that
infants’ placement or postures would be the focus of study. After the observation, mothers

Table 1. Socio-Demographic Characteristics of Samples.

Infant Mother

Age (months) Gender (% girls) Age (years) Educationa

ARG 5.24 (0.33) 66.7 21.83 (2.52) 3.58 (1.08)
CAM 5.04 (0.14) 50 22.17 (1.64) 2.50 (1.09)
ITA 5.15 (0.20) 50 24.25 (6.55) 2.92 (1.31)
KEN 5.27 (0.42) 50 21.75 (3.14) 2.83 (1.70)
KOR 5.25 (0.16) 58.3 29.00 (2.41) 5.92 (0.79)
USA 5.33 (0.20) 50 30.25 (4.00) 6.17 (0.83)

Note. The numbers shown are means (with standard deviations in parentheses).
aHollingshead Index Education Scale (1 = less than 7th grade; 2 = 7th, 8th, and 9th grades; 3 = 10th and 11th grades;
4 = high school graduate/General Educational Development; 5 = partial college; 6 = college graduate; 7 = graduate/
professional. Differences in mothers’ age and education existed between U.S./South Korean mothers and mothers
from Argentina, Cameroon, Italy, and Kenya, F(5, 58) = 17.50, p < .01 and F(5, 66) = 23.20, p = .01, respectively. ARG = Argentina; CAM = Cameroon; ITA = Italy; KEN = Kenya; KOR = South Korea; USA = United States.

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Karasik et al. 1027

reported that they were comfortable during the observation and rated their behaviors and their
infants’ behaviors to be typical (Bornstein et al., 2014).

Coding Places and Postures

Behavioral data were coded from video files using a computerized video coding system, Datavyu
(www.Datavyu.org) that records the frequencies and durations of specific behaviors. A primary
coder scored every variable. A second coder scored 30% of the data to ensure inter-rater reliabil-
ity. Inter-rater reliability on categorical measures ranged from 95.1% to 99.5% and κs ranged
from .80 to .98 (ps < .001). The correlation between primary and reliability coders for durations was .96 (p < .001). Disagreements between coders were resolved through discussion.

Video files were coded in separate passes. In the first pass, coders accounted for every video
frame reflecting four types of places where mothers situated their sitting infants: ground (foot
area of a residence or outside space), adult furniture (furnishing that is several feet off the ground,
such as couch, bed, stool, table), child furniture (furnishing designed to support infants’ posture
and limit independent movement such as a belted highchair or stroller, or makeshift baby gear
such as a cardboard box lined with towels), or held in mothers’ arms (completely supporting
infants’ posture and limbs). Infants’ body contact with the surface of support (i.e., ground, furni-
ture, mother) denoted the onset; interrupted contact with the supporting surface for 1 s or more
signaled offset.

In a second pass, coders scored two types of infants’ sitting positions: sitting independently
(infants’ bottom resting on a flat surface with torso upright without external support) and sitting
with support (infants’ bottom resting on a flat surface with torso held upright with aid of external
support of adults’ arms or furniture). Coders also counted “tripod” sitting (infants’ back inclined
45° forward, balance supported on infants’ hands). By definition, child furniture and mothers’
arms fully support infants’ posture and limbs; thus, infants could not demonstrate independent
sitting when placed in child furniture or when held in mothers’ arms. When on the ground or on
adult furniture, infants could demonstrate independent sitting without support or sitting with sup-
port (e.g., sitting on the flat surface while resting against cushioning or supported by mothers’
hands). The onset of a sitting bout marked the video frame when infants were first placed into a
sitting position. The offset of a sitting bout marked the video frame when infants began transi-
tioning out of sitting. To count as a separate sitting bout, infants had to maintain the sitting pos-
ture for at least 1 s. Figure 1 illustrates infant sitting across the four places found around the
home. The coders also noted how sitting bouts ended: fall (loss of balance forward, backward or
sideways with torso contacting the floor or mothers’ rescuing arms), transition (controlled move-
ment from a sitting posture to prone), or mother (mothers repositioned infants).

In a third pass, coders examined whether sitting infants were out of their mothers’ reach and
for how long. We coded the duration of time mothers were proximal (within arms’ reach of
infants) and distal (out of reach) while infants were in supported and independent sitting
positions.

Infant Sitting

Although laboratory assessments and standardized tests suggested that tripod sitting would be
prevalent, tripod sitting constituted only 0.9% of all postural bouts in the data set, with most
bouts limited to one U.S. infant, who leaned onto his or her hands to play with toys and who also
demonstrated multiple bouts of independent sitting. Thus, it appears that mothers across our
sample did not put their pre-sitting infants into a sitting position without external supports for
balance. None of the infants independently transitioned into a sitting position from a prone or
supine position, so mothers decided when infants should sit up. None of the infants demonstrated

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1028 Journal of Cross-Cultural Psychology 46(8)

independent mobility (e.g., crawling, cruising), so their experience with surfaces depended on
mothers’ decisions about placements. Because of its low frequency, tripod sitting was not consid-
ered in the subsequent analyses of independent and supported sitting.

Infants were classified as sitters if they demonstrated independent sitting for at least 1 s at
least once during the 1-hr observation. Frequencies of both supported and independent sitting
bouts were tallied to obtain an accumulated number of sit bouts over the session. Accumulated
time sitting with support and sitting independently indicated the total amount of time infants
spent sitting upright over the entire session. Proficiency of independent sitting was computed by
considering the longest bout of independent sitting. We differentiated the longest single bout of
independent sitting from accumulated sitting time to establish the extent of infants’ sitting profi-
ciency. Accumulated time in sitting due to shorter sitting bouts (e.g., 10 bouts of 30 s would yield
5 min of accumulated sitting time) is not the same as a protracted period of sitting (e.g., 1 bout of
5 min).

Results

Moving Beyond Onset Ages: Sitting at 5 months

Independent sitting. In the context of everyday naturalistic interactions, mothers placed infants in
a sitting position and infants sometimes sat independently. In fact, 36% of infants (n = 26) dem-
onstrated independent sitting at least once during the observation.

(c) (d)

(a) (b)

Figure 1. Line drawings from video files illustrating four types of places where mothers situated their
infants for sitting: (a) infant sitting on the ground or floor of residence; (b) infant sitting on adult furniture
several feet from the floor; (c) infant sitting in child furniture, which supports the body and posture; and
(d) infant sitting supported in mother’s arms.

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Karasik et al. 1029

The number of independent sitters varied across the six culture groups, χ2(5) = 32.27, p < .001 (Figure 2). Only 2 (17%) U.S. infants, 2 (17%) South Korean infants, and 3 (25%) Argentinian infants demonstrated independent sitting. None of the Italian infants displayed independent sit- ting. In contrast, 8 (67%) Kenyan infants and 11 Cameroonian infants (92% of Cameroon sam- ple) demonstrated independent sitting (Table 2).

Proficiency of independent sitting. Sitting proficiency—the longest bout of independent sitting—
ranged from 2.4 s to 28 min (M = 7.72 min, SD = 8.32). All but one infant labeled as an indepen-
dent sitter demonstrated sitting bouts of 5 s or more, aligning with lab-based definitions of sitting.
Figure 2 shows the enormous variation in sitting proficiency within and across cultural groups.
Although only two U.S. infants demonstrated independent sitting, one infant sat for about 1 min
(57 s) and one infant sat for almost 5 min. Kenyan and Cameroonian infants showed the most
variability. One Kenyan infant exhibited one of the shortest bouts of independent sitting (5.40 s)
of all 26 independent sitters; another Kenyan infant exhibited one of the longest bouts in the
sample (25.37 min). Cameroonian infants matched Kenyan infants in sitting proficiency and
included the infant whose sitting bout approached half of the observation period (27.79 min).

How bouts ended. Infants rarely fell while in a supported sitting position. Most supported bouts
ended with mothers changing infants’ position (96%). Independent sitting bouts had more hetero-
geneous endings: 55% ended when mothers lifted infants into a new position, 34% ended when
infants fell, and 10% ended when infants spontaneously transitioned from sitting to prone.

Opportunities for Sitting

Accumulated time. All infants had experience sitting upright. Over the observation hour, infants
spent about one third of their time in a sitting posture (M = 19.50 min, SD = 15.37), and most of
that time was spent in a supported sitting posture (M = 13.28 min, SD = 10.87). Supported sitting
time did not differ for sitters and non-sitters. However, the 26 infants who displayed independent
sitting averaged an additional 17.22 min of independent sitting (SD = 15.64) accumulated over
the session. Therefore, overall accumulated sitting time was longer for sitters (M = 28.54 min, SD
= 16.09) compared with non-sitters (M = 14.39 min, SD = 12.56), t(70) = 4.16, p < .001.

Opportunities for sitting varied widely across the sample. Accumulated sitting duration (with
and without support) ranged from 30 s for one infant to 52 min—nearly the entire session—for

CAMKENUSAKORARGITA
0

10

20

30

In
de

pe
nd

en
t S

it
(m

in
)

Figure 2. Proficiency of independent sitting as measured by the longest single bout of sitting (in
minutes) for infants in ITA, ARG, KOR, USA, KEN, and CAM.
Note. Symbols represent individual infants who demonstrated independent sitting during the session. Broken y-axis
highlights the infants at 0 who never sat independently. ITA = Italy; ARG = Argentina; KOR = South Korea; USA =
United States; KEN = Kenya; CAM = Cameroon.

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1030 Journal of Cross-Cultural Psychology 46(8)

another infant. Accumulated duration of independent sitting ranged from approximately 30 s
(four infants) to more than 30 min (four infants) paralleling the findings above on sitting profi-
ciency. The time that infants were not in a sitting position was spent lying, usually on their backs.

Time spent in accumulated sitting differed by culture group. Italian infants spent the least
amount of time sitting upright (M = 7.68 min, SD = 4.71), whereas Kenyan and Cameroonian
infants spent the most amount of time in an upright posture (Ms = 25.19, 33.45 min and
SDs = 19.21, 12.80, respectively). Infants from the United States, South Korea, and Argentina
were comparable on their accumulated sitting duration (Ms = 17.06, 13.73, 19.89 min and
SDs = 10.16, 11.41, 17.16, respectively).

U.S., South Korean, Argentinian, and Italian infants spent more time in supported sitting
(Ms = 15.23, 11.92, 19.72, 7.68 min and SDs = 7.88, 10.58, 17.02, 4.71, respectively) than unsup-
ported sitting (Ms = 1.82, 1.81, 0.17, 0 min and SDs = 5.97, 5.28, 0.48, 0, respectively), whereas
Kenyan and Cameroonian infants spent equivalent times in supported (Ms = 12.50, 12.63 min
and SDs = 6.92, 11.93, respectively) and unsupported sitting (Ms = 12.69, 20.82 min and SDs =
18.31, 14.25, respectively). A 6 (Group) × 2 (Sit type: Independent and supported) mixed-mea-
sures ANOVA on duration of sitting confirmed the main effect for sitting duration, F(5, 66) =
5.40, p < .001, partial η2 = .29; sitting type, F(1, 66) = 14.62, p < .01, partial η2 = .18; and Group by Sit type interaction, F(5, 66) = 4.80, p < .01, partial η2 = .27. Post hoc, Sidak-corrected pair- wise comparisons confirmed these differences, ps < .05.

Table 2. Descriptive Statistics.

Sit prof
(min)

Supp sit
(min)

Unsupp
sit (min)

Unsupp and
supp sit bouts

(freq)
Grnd sit

(min)
Adt furn
sit (min)

Chi furn
sit (min)

Arms
sit

(min)
Accumul
sit (min)

ARG
M 0.53 19.72 0.17 11.58 0.88 2.47 14.45 2.09 19.89
SD 0.78 17.02 0.48 9.81 1.9 4.7 16.01 2.67 17.16
CAM
M 11.26 12.63 20.82 19.33 8.53 13.14 3.58 8.2 33.45
SD 7.85 11.93 14.25 13.39 15.55 14.66 9.74 4.47 12.8
ITA
M 0 7.68 0 7.83 0 1.92 0 5.76 7.68
SD 0 4.71 0 4.64 0 2.9 0 3.7 4.71
KEN
M 8.1 12.5 12.69 27.42 12.16 4.77 0.94 7.32 25.19
SD 10.05 6.92 18.31 14.49 16.11 7.65 1.41 3.98 19.21
KOR
M 2.31 11.92 1.81 12.92 3.44 0.14 3.54 6.61 13.73
SD 1.02 10.58 5.28 14.16 7.46 0.26 8.86 5.2 11.41
USA
M 2.89 15.23 1.82 11.33 2.53 0.28 9.77 4.48 17.06
SD 2.74 7.88 5.97 8.4 5.96 0.46 7.6 2.61 10.16

Note. Sitting proficiency averages (in minutes) are shown for independent sitters. Supported plus unsupported sitting
(in minutes) equal to accumulated sitting (in minutes) across the four places (ground, adult and child furniture, and
mother’s arms). Frequency of supported and unsupported sitting bouts were distributed over the hour with sitters
accumulating more sitting bouts overall than non-sitters. Maternal age and education did not predict duration of
sitting in the four places. Places where mothers situated infants related to infant sitting proficiency after controlling
for maternal age and education. Sit prof = sitting proficiency; Supp sit = supported sitting; Unsupp sit = unsupported
sitting; Grnd = ground/floor; Adt furn = adult furniture; Chi furn = child furniture; Arms = mothers’ arms/lap;
Accumul sit = accumulated time sitting; ARG = Argentina; CAM = Cameroon; ITA = Italy; KEN = Kenya; KOR =
South Korea; USA = United States.

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Karasik et al. 1031

Sitting bouts. Sitting episodes were brief and distributed over time. The frequency of bouts of
supported and independent sitting ranged from 2 to 62 (M = 15.07 bouts, SD = 12.79).

Not surprising, independent sitters had more sitting bouts overall (M = 25.31 bouts,
SD = 15.40) than did non-sitters (M = 9.28, SD = 5.60), t(70) = 6.38, p < .001, even when compar- ing only supported sitting bouts (Ms = 18.42 and 9.28, SDs = 11.76 and 5.60, for sitters and non- sitters, respectively), t(70) = 4.47, p < .001. All culture groups were comparable on the number of sitting bouts except for Kenya. Kenyan infants accumulated 27.42 (SD = 14.49) bouts of independent and supported sitting, which is double that of the other groups (Ms = 11.33, 12.92, 11.58, 7.83, 19.33 and SDs = 8.40, 14.16, 9.81, 4.64, 13.39, for the United States, South Korea, Argentina, Italy, and Cameroon, respectively), F(5, 66) = 4.69, p < .01.

Most supported sitting bouts were short: 77% of supported sitting bouts lasted less than 1 min,
with no differences between sitters and non-sitters. In contrast, 40% of independent sitting bouts
were 1 min or longer and 10% of independent sitting bouts were more than 7 min. Although non-
sitters had opportunities to sit while supported, their mothers left them in a supported sitting
position for brief periods; therefore, the bouts of sitting seen in non-sitters never reached the
durations seen for independent sitters.

Contexts of Sitting

Although infants had opportunities to spend time in all four places, only 17% of infants spent
time on the ground, adult and child furniture, and in mothers’ arms. Of their observation hour,
approximately one third was spent in mothers’ arms (M = 22.63 min, SD = 10.68; ranging from
M = 15.21 min for Argentinians to M = 28.51 min for Italians).

Places infants sit. Infants sat on many surfaces, enabling them to practice postural control across
different contexts. Where mothers situated their infants for sitting differed by group (Figure 3).
Infants from the United States, Argentina, South Korea, and Italy spent most of their sitting time
in places that offered postural support: child furniture for U.S. (M = 9.77 min, SD = 7.60) and
Argentinian infants (M = 14.45 min, SD = 16.01); and mothers’ arms for South Korean (M = 6.61

CAMKENUSAKORARGITA
0
10
20
30

D
ur

at
io

n
(m

in
)

Ground, floor
Adult furniture
Child furniture
Mother s arms

Figure 3. Sitting across four places represented as duration in minutes: ground/floor, adult furniture,
child furniture, and mother’s arms.
Note. ITA = Italy; ARG = Argentina; KOR = South Korea; USA = United States; KEN = Kenya; CAM = Cameroon.

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1032 Journal of Cross-Cultural Psychology 46(8)

min in arms, SD = 5.20) and Italian infants (M = 5.76 min in arms, SD = 3.70). In contrast, infants
from Kenya and Cameroon spent most of their sitting time in places that offered little postural
support, requiring infants to manage the challenges of gravity to stay upright. Kenyan infants
spent most of their sitting time on the ground (M = 12.16 min, SD = 16.11) and Cameroonian
infants spent most of their sitting time on adult furniture (M = 13.14 min, SD = 14.66). These
differences were confirmed by a Group × Place interaction, F(15, 198) = 3.72, p < .001.

Places and types of sitting. Infants across the six groups differed in where they sat when supported
and unsupported, as revealed in the three-way interaction, F(15,198) = 3.94 p < .001. Of the 26 sitters, infants from the United States, South Korea, and Kenya sat unsupported on the floor (Ms = 10.98, 10.87, and 16.18 min, SDs = 13.82, 10.46, 17.34) rather than on adult furniture (Ms = 0, 0, and 2.81 min, for the United States, South Korea, and Kenya, respectively). Argentin- ian and Cameroonian infants divided their independent sitting time between the ground and adult furniture. The three sitters from Argentina, on average, spent 0.13 min (SD = 0.23) sitting on the ground and 0.56 min (SD = 0.94) sitting on adult furniture. In comparison, the 11 Cameroonian independent sitters, on average, spent 9.29 min (SD = 16.05) sitting on the ground and 13.17 min (SD = 14.0) sitting on adult furniture. Compared with independent sitting on the ground, sitting on adult furniture is potentially more challenging and the consequences of falling are more severe.

The places where mothers situated their infants were related to infants’ sitting proficiency,
controlling for maternal age and education. Mothers who placed their infants on the ground,
floor, or adult furniture had infants who demonstrated the longest bouts of independent sitting,
r(23) = .86, p < .001.

Mothers’ location. Mothers’ willingness to leave their sitting infants on adult furniture was related
to infants’ sitting skill. For the 26 sitters, the more proficient the sitter, the longer mothers tended
to stay out of reach of their sitting infants, r(26) = .34, p = .05. These results were not carried by
one or two mothers; 10 of 26 mothers (38%) of sitters spent time out of their infants’ reach while
infants sat independently on adult furniture.

The differences in mothers’ location were most pronounced for infants in Cameroon and
Kenya. When Cameroonian infants were sitting independently on high adult furniture, their
mothers were just as likely to be near their infants (51% of time sitting independently on adult
furniture) as out of reach of their infants (49% of time).

Kenyan mothers maintained comparable distances from their infants: When their infants sat
independently on adult furniture, mothers spent 38% of the time away and 62% of the time near
their infants. In fact, one Kenyan mother spent a stretch of 13 min away from her infant as he sat
independently on adult furniture: This infant was one of the more proficient sitters (17.4 min of
sitting in a single bout). In contrast, when infants of other cultural communities were placed sit-
ting independently or supported on adult furniture, mothers hovered near their infants (100%,
100%, 91%, and 78% of sitting time for the United States, South Korea, Argentina, and Italy,
respectively).

Discussion

The study of motor development has been limited in terms of how motor skills are depicted,
where motor development is studied, and who is studied. Previous work has been confined
largely to the study of Western, White, middle-class populations in laboratory settings. Based on
laboratory research on sitting proficiency, we would expect infants to sit for short periods, with
bouts ending in falls or transitions to prone. Cross-cultural research—studies involving the
other 95% of the population (Henrich, Heine, & Norenzayan, 2010)—is limited primarily to

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Karasik et al. 1033

comparisons of milestone onset ages with Western norms. The implementation of these limited
methods has led to a gross misrepresentation of motor development (Adolph et al., 2010a;
Adolph & Robinson, 2015).

How: Conceptualizing Sitting Skill

Here, rather than focusing on onset ages and imposing arbitrary criteria for success, we focused
on variability in infants’ sitting proficiency. At 5 months, approximately one third of infants sat
independently, with 92% of infants in Cameroon and 67% of infants in Kenya being independent
sitters. These findings align with the accelerated sitting onset ages observed in some African and
Caribbean cultures (e.g., see Adolph et al., 2010a, for review; Hopkins & Westra, 1990). However,
unlike other researchers (e.g., Carra, Lavelli, Keller, & Kartner, 2013; Keller, Yovsi, & Voelker,
2002; Lamm, Keller, Yovsi, & Chaudhary, 2008), we did not collect data on parental expectations
or specific child-rearing practices outside the observation hour.

We also found considerable overlap in sitting proficiency across the six cultures: Approximately
half of the independent sitting bouts in each sample were less than 10 min. Ranges of sitting were
most pronounced in the Kenyan and Cameroonian samples. Infants’ sitting bouts ranged from a
few seconds to half of the observation period. Some U.S. infants sat longer than some of the
Kenyan and Cameroonian infants. These ranges highlight a frequent misattribution in compara-
tive studies. Cultures cannot be characterized as uniformly “advanced” or “delayed;” rather,
within-group variability nearly always surpasses between-group differences. In addition to the
between-group differences, variability within-groups was striking.

The upper range in the duration of single sitting bouts is particularly remarkable because in
the laboratory when researchers attempt to elicit sitting, they typically adopt a 5-s, 10-s, or 30-s
criterion to demonstrate sitting ability (Fishkind & Haley, 1986; Martorell et al., 2006; McGraw,
1945). At home, in the context of spontaneous activity, one infant sat for almost half an hour in a
single episode of uninterrupted independent sitting.

Sitting for extended periods might have far-reaching implications for developing skills in
other domains. While sitting upright, the infants’ world comes into view (Kretch et al., 2014),
allowing them to visually scan interesting objects and people. While sitting independently,
infants’ hands are freed from supportive functions to explore objects and interact with caregivers.
Sitting for prolonged periods provides ample opportunity to explore and learn about objects. In
fact, independent sitters are more likely to demonstrate more advanced object manipulation skills
and better performance on a 3D object completion task compared with non-sitters (Soska et al.,
2010). Long-term effects, beyond infancy, have been documented: Motor-exploratory behaviors
in infancy predicted cognitive function in childhood and academic achievement in adolescence
(Bornstein, Hahn, & Suwalsky, 2013).

Where: Sitting in Natural Settings

The study of motor development is typically confined to the laboratory. In contrast, we observed
infants’ spontaneous real-time experiences with sitting in the home. Cultural routines and expec-
tations about the ages at which infants should display various skills guide caregivers’ child-
rearing practices including when and how to allow infants to practice skills, and what is safe and
appropriate for infants to do (Carra, Lavelli, & Keller, 2014; Carra et al., 2013). Caregivers
determine opportunities for sitting; they situate infants in certain places (stroller or dirt floor) and
place them in particular postures (lying or sitting), thereby restricting or broadening infants’
opportunities to practice sitting. Caregivers rarely leave pre-sitters in a tripod position, and
they—not infants—most frequently decide when sitting bouts should end.

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1034 Journal of Cross-Cultural Psychology 46(8)

Infants had extensive experiences with sitting across a variety of places—floor, infant and
adult furniture, and mothers’ arms. These surfaces provided different constraints on balance and
offered different opportunities for learning. For example, although independent sitting occurred
on the ground or floor and adult furniture, the consequences of keeping balance on these two
surfaces differ. When sitting independently, there is a possibility of falling, but falling from high
adult furniture has potentially dire consequences. Thus, sitting independently or while supported
on adult furniture provides a more demanding learning context than sitting on the floor, strapped
into infant furniture, or in mothers’ arms.

We found no group differences in infants spending time in mothers’ arms, although others
have shown that mothers from West Africa spend more time in body contact with their infants
than do mothers from Italy (e.g., Carra et al., 2014; Carra et al., 2013). Infants across the six
cultures, on average, spent one third of the observation hour held in mothers’ arms. It is possible
that while engaging in typical daily activities in mothers’ arms (i.e., face-to-face interactions,
grooming, feeding, carrying), infants experience forms of handling that may emphasize different
postural positions (Bril & Sabatier, 1986; Lamm et al., 2008) and may in turn affect development
of various skills. For example, when in body contact, West African mothers showed longer dura-
tions of rhythmic motor behaviors by repeatedly shaking or moving infants’ bodies than Italian
mothers (Carra et al., 2014). Future investigations of the different postural positions and activi-
ties that mothers engage in while holding their infants would shed light on whether and how
patterns of holding relate to infant sitting.

These findings challenge current definitions of sitting. Why is sitting on the floor with legs
outstretched (termed “long sit” or “v-sit”) considered the benchmark of independent sitting?
Infants have opportunities to practice sitting on many surfaces under varying balance constraints.
Yet, sitting on a high surface, which poses more risk and potentially requires more balance con-
trol, is not assessed on standard developmental screening tests. Similarly, the “short sit,” with
legs bent over the edge of a chair or bench, “w-sitting” with legs bent backward at the knee, deep
crouching with buttocks near heels, and other forms of sitting that are prevalent in many cultures
(Hewes, 1955) are missing from most assessment tests. Indeed, the short sit is the most prevalent
form of sitting among Western children and adults, and many older children and adults cannot
perform the “long sit” that typifies sitting on Western assessment instruments for infants.

Who: Sitting Across Cultures

What is known about motor development, similar to other areas of psychology, is predominantly
based on infants from Western countries, which precludes a full appreciation of social and cul-
tural influences (Bornstein, 2010; Bornstein et al., 2014; Tomlinson, Bornstein, Marlow, &
Swartz, 2014). The few cross-cultural studies of infant motor development are limited to group
comparisons of onset ages (e.g., Hopkins & Westra, 1990). Cross-cultural studies of natural,
everyday experiences with motor action are rare.

Our observations of infant sitting across six cultural groups uncovered possibilities in human
development previously unimagined. In terms of sitting proficiency, half-hour sitting bouts could
only be documented with an eye toward cultural variability. In terms of where infants sit, the
common mandate is for 5-month-olds to be strapped into infant seats or held in mothers’ arms.
Most U.S. parents, pediatricians, and even researchers could not imagine leaving an infant seated
unattended on a high bed or bench. Our culture promotes implicit expectations that mothers
should be nearby when infants are sitting independently. This was indeed the case for infants
from the United States, South Korea, Argentina, and Italy. However, mothers from Kenya and
Cameroon spent substantial time out of the vicinity of their sitting infants. One of the most pro-
ficient sitters in the Cameroonian sample demonstrated a bout of independent sitting that lasted

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Karasik et al. 1035

28 min. At the start of the visit, her mother sat on the bench nearby and periodically glanced over
and smiled/vocalized to her infant. On several occasions, she left the room for minutes at a time.
Upon her return, she casually checked in with her infant and continued her work. The routine of
mother leaving and reuniting with her infant lasted the entire half an hour; all the while the infant
contentedly remained seated without falling out of her sitting posture. This finding was not due
to lack of care for infants’ safety. In fact, none of the infants who sat independently on adult fur-
niture experienced a fall.

Conclusions

Conclusions about the bounds of infant motor development are the product of our methods—
whom we study, where we conduct studies, and how we assess developmental changes in skills.
Had we not looked beyond onset ages, ventured outside the laboratory, and studied samples of
infants from six cultures across the globe, we would never have known that at 5 months, some
infants can safely sit on high benches for extended periods without the support of adults nearby.
The sort of phenomena we observed could only be revealed through the lens of cross-cultural
inquiry and the use of ecologically valid methods and measures.

Authors’ Note

Portions of this work were presented at the 2010 meeting of the International Society for Developmental
Psychobiology, San Diego, California; at the 2010 meeting of the Society for Cross-Cultural Research,
Albuquerque, New Mexico; and at the 2011 meeting of the Society for Research on Child Development,
Montreal, Canada.

Acknowledgment

We thank Joan Suwalsky, Alyssa Zuckerman, Laurel Bunse, and Loye Tucker for their assistance, and
Shashi Bali, Eleanor Berti, Celia de Zingman Galperin, Margaret Kabiru, Keumjoo Kwak, A. Bame
Nsamenang, and Paola Venuti for help in data collection. We gratefully acknowledge the contributions of
the infants and parents who participated in this study.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or
publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publi-
cation of this article: This research was supported by National Institute of Child Health and Human
Develppment Grant R37-HD33486 to Karen E. Adolph, National Institute of Child Health and Human
Development Grant R01-HD42697 to Karen E. Adolph and Catherine S. Tamis-LeMonda, and by the
Intramural Research Program of the National Institutes of Health, National Institute of Child Health and
Human Development.

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PAPER

Go naked: diapers affect infant walking

Whitney G. Cole, Jesse M. Lingeman and Karen E. Adolph

Department of Psychology, New York University, USA

Abstract

In light of cross-cultural and experimental research highlighting effects of childrearing practices on infant motor skill, we asked
whether wearing diapers, a seemingly innocuous childrearing practice, affects infant walking. Diapers introduce bulk between the
legs, potentially exacerbating infants’ poor balance and wide stance. We show that walking is adversely affected by old-fashioned
cloth diapers, and that even modern disposable diapers – habitually worn by most infants in the sample – incur a cost relative to
walking naked. Infants displayed less mature gait patterns and more missteps and falls while wearing diapers. Thus, infants’ own
diapers constitute an ongoing biomechanical perturbation while learning to walk. Furthermore, shifts in diapering practices may
have contributed to historical and cross-cultural differences in infant walking.

Introduction

Childrearing practices affect motor development. Cul-
tural and historical differences in how caregivers handle,
dress, and toilet their infants can have profound effects
on whether infants acquire certain motor skills, the age at
which skills are acquired, and the subsequent develop-
mental trajectory (Adolph, Karasik & Tamis-LeMonda,
2010; Adolph & Robinson, in press). For example, in
some African and Caribbean cultures, caregivers use
special handling and exercise routines to facilitate the
onset of sitting and walking – propping infants into
sitting postures, practicing upright stepping, stretching
infants’ limbs, and suspending infants by ankles or wrists
(Bril & Sabatier, 1986; Hopkins & Westra, 1988; Rabain-
Jamin & Wornham, 1993). Such daily exercise results in
earlier onset of sitting and walking relative to Western
norms (Hopkins & Westra, 1989, 1990). Crawling, a skill
not exercised or encouraged, may be delayed or skipped
altogether.

Historical changes in handling practices within a cul-
ture show similar effects. Within a decade, the ‘Back to
Sleep’ campaign instituted by the American Academy of
Pediatrics reversed the long-time practice of putting
infants to sleep on their bellies to putting infants to sleep
on their backs (Willinger, Ko, Hoffman, Kessler &
Corwin, 2000). Although successful in reducing the
incidence of Sudden Infant Death Syndrome, the change
in handling practices had the unintended effect of
delaying prone skills such as crawling and rolling (Davis,
Moon, Sachs & Ottolini, 1998). A follow-up ‘Tummy
Time’ campaign urged mothers to compensate for the
lost prone experience by giving infants playtime on their

stomachs. Subsequent research demonstrated a dose–
response relation between awake time in a prone position
and the onset age of prone skills (Majnemer & Barr,
2005).

Experimental evidence supports the facilitative effects
of infant exercise. A few minutes of daily practice can
alter the course of motor development (Clark, Kreutz-
berg & Chee, 1977; Lagerspetz, Nygard & Strandvik,
1971). For example, with no intervention, infant stepping
has a U-shaped trajectory: Newborns supported in an
upright position exhibit stepping movements, but step-
ping disappears between 2 and 8 months, and reappears
when infants begin learning to walk (McGraw, 1932;
Thelen, Fisher & Ridley-Johnson, 1984). However, just
12 minutes of daily practice executing stepping move-
ments in an upright position increases the frequency of
newborn stepping, maintains stepping during the dor-
mant period when stepping normally disappears, and
accelerates the onset of independent walking compared
to infants who receive only passive exercise (Zelazo,
Zelazo & Kolb, 1972). Similarly, 15 minutes of daily
practice fighting gravity in prone, sitting, and upright
positions between 2 and 3 months of age results in earlier
onset ages for crawling, sitting, and walking compared to
infants who receive comparable amounts of time engaged
only in social interactions (Lobo & Galloway, in press).

Various historical and cultural differences in dress also
affect motor development. In the 19th century, 40% of
American infants skipped crawling, possibly because
their long flowing gowns impeded movement on hands
and knees (Trettien, 1900). More recently, infants who
wear thick winter clothes or sleep under heavy blankets
show delays in prone skills such as crawling (Bensen,

Address for correspondence: Karen E. Adolph, Department of Psychology, New York University, 6 Washington Place, New York, NY 10003, USA;
e-mail: karen.adolph@nyu.edu

� 2012 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.

Developmental Science 15:6 (2012), pp 783–790 DOI: 10.1111/j.1467-7687.2012.01169.x

1993; Hayashi, 1992), and tight leggings reduce the fre-
quency of upright stepping movements in 2- to 4-month-
olds (Groenen, Kruijsen, Mulvey & Ulrich, 2010).

Toileting practices can also have dramatic effects on
motor development. In parts of Northern China where
water is scarce, caregivers lay infants on their backs inside
bags filled with fine sand for most of each day. The sand-
bags effectively absorb waste and keep infants clean, but
severely restrict infants’ movements and lead to sub-
stantial delays in sitting and walking compared to children
from comparable areas who were not sandbagged (Mei,
1994; Xie & Young, 1999). Here we ask whether a less
dramatic solution to toileting – wearing diapers – might
also affect infant motor development. Specifically, we
asked whether diapers affect the proficiency of early
walking. Because diapers introduce bulk between the legs
and may constrain infants’ leg movements, diapers may
exacerbate infants’ already immature gait.

In the current study, we compared infants’ walking
while naked, wearing a modern, thin disposable diaper,
and wearing an old-fashioned, thick, cloth diaper. The
three conditions provided a crude gradation in overall
bulk and were designed to reflect historical and cultural
differences in diapering. We collected standard measures
of infant walking skill to assess effects of diapers on the
maturity of infants’ gait. For nearly 100 years,
researchers have characterized the maturity of infant gait
in terms of step width and step length: A narrower side-
to-side distance between the feet and a longer front-to-
back distance between feet are indicative of more mature
gait patterns (Bril & Breniere, 1989; Shirley, 1931). In
addition, we measured functional outcomes – whether
infants misstepped or fell – to assess whether diapers
make it more difficult to walk.

To test the differential effects of diapers on novice and
experienced infant walkers, we observed 13-month-olds,
an age when most infants have just begun walking, and
19-month-olds, an age when improvements in walking
skill have begun to reach asymptote (Adolph, Vereijken
& Shrout, 2003; Bril & Breniere, 1989; Hallemans, De
Clercq & Aerts, 2006). For novice walkers, falling is
common – 100 times a day – and gait patterns are
notoriously immature; the side-to-side distance between
infants’ feet may be larger than the front-to-back dis-
tance (Adolph, Cole, Komati, Garciaguirre, Badaly,
Lingeman, Chan & Sotsky, in press). Walking in novices
is more adversely affected by load carrying (weights
strapped to their waists or carried in shoulderpacks) and
variations in the ground surface (slopes, cliffs, and so on)
compared with more experienced walkers (Adolph, 1997;
Garciaguirre, Adolph & Shrout, 2007; Kretch & Adolph,
in press; Vereijken, Pedersen & Storksen, 2009). Thus,
walking may be more disrupted by diapers in the
13-month-olds because a small perturbation could
exacerbate their already precarious walking skill. Alter-
natively, because novice walkers already take wide,
immature steps, they may be less susceptible to the bulk
of diapers than more experienced infants. Finally, to

separate effects of bulk from effects of novelty, mothers
reported their normal diapering practices and how much
time infants were allowed to walk naked.

Method

Participants

We tested 30 13-month-olds and 30 19-month-olds.
Infants were predominantly white and middle class. An
additional three 19-month-olds did not complete testing
due to fussiness. Mothers reported in a structured
interview the first day they saw their infants walk at least
10 feet continuously – our definition of walking onset.
Walking experience data from three 13-month-olds were
not available. As shown in Figure 1, the range in walking
experience within age groups was considerable, and the
overlap between the two age groups was minimal. The
13-month-olds had 8 to 97 days of walking experience
(M = 45.25 days); the 19-month-olds had 58 to 289 days
(M = 192.07 days); overall, the older group was more
experienced than the younger group, t(55) = 12.44,
p < .001.

Outside the laboratory, most infants normally wore
disposable diapers (90% of 13-month-olds and 93.3% of
19-month-olds) identical or similar to the brand we used
for testing. Only one 13-month-old and one 19-month-
old normally wore cloth diapers. Based on mothers’
reports, infants were allowed to walk naked M = 41 min
a week; 73% had some experience walking naked and
27% never walked naked.

Apparatus and procedure

Infants walked repeatedly (M = 7.31 trials per condition,
SD = 1.53) over a 5.73-m long · 0.92-m wide pressure-
sensitive gait carpet (http://www.gaitrite.com) while
wearing each type of diaper (Figure 2A). The carpet had
a spatial resolution of 1.27 cm. If infants veered off the
carpet, stopped immediately, or fell, we repeated the trial,
aiming for at least six trials per diaper condition. The
order of diaper conditions was counterbalanced.

Figure 1 Infants’ walking experience in 13-month-olds and
19-month-olds. Each circle represents data from one infant.
The horizontal lines represent group means.

784 Whitney G. Cole et al.

� 2012 Blackwell Publishing Ltd.

The disposable diaper used in testing was a common
commercially available brand in sizes 3–5, weighing
between 32 and 41 g depending on size. Infants were tested
in the size diaper they typically wore. Measured flat on a
table, all three sizes of disposable diaper were 7.5 cm
across by 1.1 cm thick at the crotch. The cloth diaper
weighed 170 g and was folded for nighttime use, making
the crotch 12.3 cm across and 2.8 cm thick. Infants’ dia-
pers were changed if they became soiled during testing.

At the end of the session, an experimenter measured
each infant’s leg lengths (from hip to ankle) and
recumbent height (crown to heel). Due to fussiness and
experimenter error, leg length data were missing from
nine infants and height data were missing from eight
infants.

Data coding and processing

Using the video coding software OpenShapa (http://
www.openshapa.org), we identified trials with at least five
consecutive steps on the carpet. These trials were then
scored for disruptions of alternating gait: falls (when the
body dropped to the floor unsupported) and missteps
(trips when the swinging foot failed to clear the ground,
double steps when the same foot stepped twice, back steps
when the leading leg moved backward behind the trailing
leg, and lag steps when the swinging leg moved forward
but failed to move ahead of the stance leg).

We calculated gait parameters based only on instances
where infants took several consecutive steps at a relatively
steady state velocity, as is customary (Bril & Breniere,

1989). Thus, we removed portions of trials that included
falls ⁄ missteps or gait initiation (the first two steps on the
gait carpet) and used only the trials with at least five
consecutive steps remaining (M = 9.42 steps). Gait data
from three infants were unavailable due to veering off the
carpet and gait disruptions. Figure 2B shows the calcu-
lation of gait parameters. Using the raw x-y coordinates
generated by the gait carpet, a customized software pro-
gram calculated step width (distance from the heel of the
current step to the line of progression formed by the
opposite stride), step length (distance along the line of
progression from the heel of the previous step to the heel
of the current step), dynamic base of support (angle
between the heel points of three consecutive steps), and
walking speed (distance between the first to last step
divided by time). Because previous work showed that
infants’ walking speed is highly correlated with other gait
parameters and generally reflects infants’ highest level of
walking skill (Garciaguirre et al., 2007), we analyzed each
infant’s two fastest trials in each condition.

Results

Gait disruptions

Walking in diapers had a functional cost, especially in
the 13-month-old novice walkers. When walking naked,
10 of the 30 13-month-olds fell or misstepped at least
once. While wearing the cloth diaper, 21 of them fell or
misstepped. In contrast, 19-month-olds rarely fell or

Gait
Parameters

Step width

Step length

Dynamic
base

Naked Disposable Cloth

(A) (B)

Figure 2 (a) Sample footprint paths from one typical infant walking while naked, wearing a disposable diaper, and wearing a cloth
diaper. Infant is walking from top to bottom. Marks represent the pressure points of each footfall recorded by the gait carpet. (b) Gait
parameters illustrated with footfalls recorded by the gait carpet as infant walked from top to bottom. Top: Step width is the side-to-
side distance between feet. Middle: Step length is the front-to-back distance between consecutive footfalls. Bottom: Dynamic base is
the angle between three consecutive steps.

Diaper walking 785

� 2012 Blackwell Publishing Ltd.

misstepped, and 17 walked free of disruptions across all
conditions. But when 19-month-olds did display gait
disruptions, they usually did so while wearing a cloth
diaper: Only four of the experienced infants had a gait
disruption walking naked, whereas eight did so in the
cloth diaper. In the 13-month-olds, the frequency of
disruptions across trials decreased with days of walking
experience, r(28) = ).39, p = .04. Thirteen-month-olds
fell or misstepped on M = 17% of trials while wearing
the cloth diaper, 15% while wearing the disposable and
9% while walking naked. Nineteen-month-olds fell less
frequently: M = 5% in cloth, 2% in disposable, and 2%
while naked. Table 1 shows the prevalence of gait dis-
ruptions in terms of the number of infants who fell or
misstepped at least once in each condition (top) and in
terms of the proportion of trials that were disrupted
(bottom).

Because disruption data were not normally distributed,
we analyzed the number of infants displaying at least one
gait disruption using a Generalized Estimating Equation
(GEE) model with a binomial probit function (Hardin &
Hilbe, 2003). The GEE confirmed a main effect of diaper
condition, Wald V2(2, N = 60) = 8.62, p = .01. Sidak-
corrected pairwise comparisons showed that more in-
fants had a gait disruption when walking in the cloth
diaper compared to walking naked, p = .007. The num-
ber of infants with disrupted gait in the disposable diaper
was intermediary and not significantly different from
either the naked or cloth diaper conditions. The GEE
also confirmed a main effect of age group, Wald V2(1,
N = 60) = 22.89, p < .001. The interaction between age and diaper condition was not significant, Wald V2(2, N = 60) = 1.80, p = .41. A GEE on the proportion of trials with gait disruptions revealed comparable effects; Wald V2(1, N = 60) = 19.98, p < .001 for age group, Wald V2(2, N = 60) = 6.89, p = .03 for diaper condition. Replacing age group with infants’ individual walking experience as a predictor yielded parallel findings: The GEE on the number of infants who experienced at least one gait disruption showed main effects of walking experience, Wald V2(1, N = 60) = 23.43, p < .001, and diaper condition, Wald V2(2, N = 60) = 7.83, p = .02, but no interaction, Wald V2(2, N = 60) = 2.85, p = .24.

Gait parameters

In addition to incurring functional consequences, diapers
reduced the proficiency of infants’ gait. Diapers induced

large enough changes in infants’ walking to make the
condition effect visible to the naked eye. Figure 2A
shows footfall patterns from three trials in a typical 19-
month-old: Naked steps were straight and narrow; diaper
steps were noticeably wider and less mature. Figure 3
shows the diaper effect for the calculated gait parameters.
Nineteen-month-olds walked better than 13-month-olds.
But while wearing diapers, infants in both age groups
took wider, shorter steps and had smaller dynamic base
angles – all characteristics of less mature walking – and
both age groups were equally affected. Although the cost
of wearing a cloth diaper was most severe, even the dis-
posable diaper – worn daily by 92% of the infants –
increased step width and decreased dynamic base angles.

All gait parameters were entered into a 2 · 3 repeated-
measures multivariate analysis of variance. The MA-
NOVA confirmed main effects of age, F(4, 52) = 20.29,
p < .001, partial g2 = .61, and diaper condition, F(8, 48) = 11.85, p < .001, partial g2 = .66. The interaction between age and diaper condition was not significant, so

Table 1 Prevalence of gait disruptions in terms of the number
of infants disrupted and the proportion of trials disrupted

Naked Disposable Cloth

Number of infants disrupted
13-month-olds 10 17 21
19-month-olds 4 4 8

Proportion of trials disrupted
13-month-olds .09 .15 .17
19-month-olds .02 .02 .05

(a)

(b)

(c)

Figure 3 Average results for each age group in each condi-
tion illustrating the main effects of age and diaper condition on
(a) step width, (b) step length, and (c) dynamic base. Error bars
represent the standard error.

786 Whitney G. Cole et al.

� 2012 Blackwell Publishing Ltd.

data were collapsed across ages for follow-up univariate
ANOVAs and Sidak-corrected pair-wise comparisons of
diaper conditions. The ANOVA on step width confirmed
a main effect of diaper condition, F(2, 110) = 32.57,
p < .001, partial g2 = .37. As shown in Figure 3A, infants took wider (less mature) steps in disposable dia- pers compared with naked and still wider steps in cloth diapers compared with disposables, ps < .001. The ANOVA on step length revealed a main effect for diaper condition, F(2, 110) = 9.23, p < .001, partial g2 = .14. As shown in Figure 3B, infants took shorter (less mature) steps in cloth diapers compared with naked and disposables, ps < .02. The ANOVA on dynamic base angle confirmed a diaper effect, F(2, 110) = 32.48, p < .001, partial g2 = .37. As shown in Figure 3C, infants had smaller (less mature) base angles in dispos- able diapers compared with naked and smaller yet in cloth diapers compared with disposables, ps < .001.

Using infants’ walking experience as a predictor
instead of age group yielded parallel results, with main
effects of walking experience, F(4, 51) = 19.00, p < .001, and diaper condition, F(8, 212) = 2.74, p = .007, and no interaction between walking experience and diaper condition, F(8, 212) = 1.73, p = .09. Follow-up univar- iate ANOVAs yielded main effects of diaper condition only for step width, F(2,108) = 8.55, p < .001, and dynamic base, F(2, 108) = 9.21, p < .001. The main effect of diaper condition on step length was no longer significant when using walking experience as a predic- tor, but none of the univariate tests revealed an inter- action.

As in previous work (Adolph et al., 2003; Garciaguirre
et al., 2007), leg length and height were not correlated
with gait parameters after controlling for infants’ age,
partial rs(44) from ).11 to .04, ps > .47. Nevertheless,
19-month-olds had longer legs (M = 36.67) than
13-month-olds (M = 33.70), t(49) = 8.44, p < .001, and 19-month-olds were taller (M = 82.63) than 13-month- olds (M = 76.68), t(50) = 8.17, p < .001. Thus, as a precaution we reran analyses on step length after nor- malizing infants’ step lengths to their leg lengths. Adjusting for the larger body dimensions of the older infants did not alter the findings: The ANOVA on step length yielded main effects of age group, F(1, 51) = 33.03, p < .001, and diaper condition, F(2, 102) = 8.05, p = .001; the interaction was not significant.

As expected from previous work (Garciaguirre et al.,
2007), walking speed was correlated with step width,
r(56) = ).74, p < .001, step length, r(56) = .95, p < .001, and dynamic base, r(56) = .86, p < .001. However, there was no main effect of diaper condition on walking speed, F(2, 110) = 2.96, p = .06, partial g2 = .05, and the detriment to each gait parameter remained after statis- tically adjusting for speed, suggesting that changes in speed did not drive the results: step width, Wald V2(2, N = 57) = 53.97, p < .001; step length, Wald V2(2, N = 57) = 19.77, p < .001; dynamic base, Wald V2(2, N = 57) = 47.78, p < .001.

Although the effects of the diaper are statistically
significant, inspection of the y-axes in Figure 3 indicates
that the detriments to walking proficiency were relatively
small. For example, the average step width increased
from 9.71 cm when walking naked to 11.05 cm in the
disposable diaper and 12.24 cm in the cloth diaper. How
substantial is a M = 2.5 cm increase in step width? We
addressed this question by modeling the relation between
walking skill and walking experience using a nonlinear
mixed model with an exponential decay function (Burke,
Shrout & Bolger, 2007). As illustrated in Figure 4, for an
infant with the median walking experience of 97 days, a
2.5 cm change in step width represents the culmination
of 7.5 weeks of walking experience. That is, the 2.5 cm
increase caused by a cloth diaper makes infants’ walking
as immature as it had been nearly eight weeks earlier
when walking naked. Similarly, the deficit to step width
caused by a disposable diaper is equivalent to losing
4.7 weeks of walking experience.

Discussion

The current results show that diapers reliably alter infant
walking, in terms of both function (causing more falls
and missteps) and proficiency (inducing less mature
walking patterns). Impairments were equally strong for
13-month-old novice walkers and 19-month-old experi-
enced walkers. However, we only documented real-time
impairments due to diapers: As soon as infants were
naked, they walked better.

Figure 4 Infants’ step width as a function of walking experi-
ence. The curve represents the step width predicted by the
exponential decay model. The solid vertical line shows the
median walking experience. The dotted vertical line intersects
the fit line at a step width 1.2 cm larger (the average increase
caused by wearing a disposable diaper). The dashed line
intersects the fit line at a step width 2.5 cm larger (the average
increase caused by wearing a cloth diaper). The distance from
the solid line to the dashed line represents the cost to infants’
walking skill from wearing a cloth diaper in terms of the
amount of walking experience needed to accomplish an
equivalent change.

Diaper walking 787

� 2012 Blackwell Publishing Ltd.

Real-time effects

While wearing a diaper, infants’ steps were wider, shorter,
and had smaller dynamic base angles – all signatures of
less mature walking – compared with walking naked.
Albeit statistically significant, are a few centimeters in
step width and a few degrees in base angle functionally
significant? Simply put: Yes. Infants walked as poorly
while wearing a diaper as they would have done several
weeks earlier had they been walking naked. That is, in
terms of gait maturity, wearing a diaper immediately
costs infants several weeks of walking experience. In fact
when walking naked, more than half of the 19-month-
olds displayed dynamic base angles similar to those of
5- to 6-year-olds (Adolph et al., 2003); only two infants –
neither of whom habitually wore cloth diapers – dis-
played such mature walking while wearing a cloth diaper.
Moreover, diapers impair infants’ ability to walk from
one place to another. Three times as many infants fell or
misstepped while wearing a diaper and gait disruptions
were three times more likely in the cloth diaper compared
with walking naked.

Why might diapers impair walking? One potential
explanation concerning the novelty of our experimental
manipulation can be ruled out. Although the cloth dia-
per was novel for most infants, so was walking naked. On
average, infants accumulated only 41 minutes per week
of naked walking and nearly one-third had never walked
naked. Nonetheless, infants walked best while naked.
Most infants habitually wore the same or an equivalent
disposable diaper as the model we used for testing.
Nonetheless, their gait was impaired relative to walking
naked. Moreover, we found no interaction between dia-
per condition and age or walking experience. Although
the 19-month-olds had been walking in a disposable
diaper for several months, they were equally affected as
the 13-month-olds.

A second potential explanation is biomechanical. Even
modern disposables that are designed to be thin, light,
and comfortable introduce bulk between infants’ legs.
Walking in dirty diapers – a common occurrence in
everyday life – would further increase the bulk between
infants’ legs. By pushing infants’ legs apart, step width
increases. As step width grows, the dynamic base angle
and step length shrink. In addition, diapers may con-
strain forward movement due to the material wrapped
around infants’ legs and thereby contribute to deficits in
step length and dynamic base. Alterations to the base of
support are likely to adversely affect balance and lead to
gait disruptions. In addition, wet diapers would increase
the weight of the load. Previous work shows that load
carriage increases gait disruptions and decreases infants’
walking proficiency (Garciaguirre et al., 2007; Schmuc-
kler, 1993; Vereijken et al., 2009). Given that diapers
interfere with alternating gait and foot placement, kine-
matics such as joint angles and limb trajectories and
dynamics such as forces and muscle actions are likely to
be adversely affected as well.

Taken together, our results suggest that infants learn to
walk in the context of an ongoing biomechanical per-
turbation to their gait in the form of their own diaper.
But the immediate improvement in infants’ walking when
the diaper is removed tells us something more: Infants
can exhibit more mature gait patterns when the condi-
tions allow, despite the fact that they do not produce and
experience these patterns in daily life when they walk
habitually in a diaper.

Developmental effects

Although we found that diapers cause immediate
decrements to infant walking, the current work cannot
address whether these real-time changes have more last-
ing developmental implications. Cross-cultural data raise
the provocative suggestion that childrearing practices
such as how infants are dressed can alter the course of
development. Everyday factors such as wearing heavy
clothing or being placed in a constricted posture can
delay motor development if spontaneous movement is
impeded (Adolph et al., 2010; Adolph & Robinson, in
press). Possibly, infants who learn to walk while naked –
without the additional challenge posed by a diaper –
might show more rapid gains in posture and coordination,
facilitating earlier onset ages and faster improvements.
This would be consistent with reported historical chan-
ges in infant walking: Infants today walk sooner and
better than those of previous generations, when all
infants wore cloth diapers (Shirley, 1931).

However, the opposite effect is equally plausible.
Cross-cultural practices such as enhanced handling
routines and experimental manipulations that encourage
infants to fight gravity show us that factors which chal-
lenge developing motor skills lead to accelerated onset
ages and a faster course of improvements for skills such
as sitting and walking (Adolph et al., 2010; Adolph &
Robinson, in press). In the same way, being forced to
compensate for the perturbation of the diaper might
actually accelerate skill acquisition by actively challeng-
ing infants’ developing motor skills.

By analogy, many children learn to do homework in
front of the television – in the midst of a perceptual and
cognitive perturbation. The real-time consequences may
be higher levels of distraction, thereby leading to sloppier
and less skillful performance. In the long term, children
who learn to do their homework in this context may
remain at a deficit relative to those who learn in a quiet
environment. Alternatively, learning to do homework in
the midst of this perceptual-cognitive perturbation may
make attention more flexible and focused in the long
term, and thereby lead to greater benefits. In the same
way, the challenge posed by walking in a diaper could
either hinder or facilitate motor development. An
experimental study comparing infants reared naked
throughout the first two years to infants reared in diapers
could help to clarify whether diapers play a facilitative or
hindering role in the development of walking.

788 Whitney G. Cole et al.

� 2012 Blackwell Publishing Ltd.

Concluding thoughts

The current study provides a cautionary note for
researchers because many have not reported what in-
fants were wearing (Bril & Breniere, 1989; Shirley,
1931). Clothes, shoes, and recording devices can affect
infants’ movements: Pre-walking 2- to 4-month-olds
showed equal frequency of alternating upright steps
while naked or wearing a diaper, but tight leggings of
the sort typically worn to facilitate high-speed motion
tracking impeded their movements (Groenen et al.,
2010). Lack of information about infants’ diapers and
other garb is particularly worrisome when attempting
to interpret historical changes and cross-cultural dif-
ferences in walking skill. Historical improvements in
infant walking and precocity in non-industrialized
societies are confounded with diapering practices.
Much of the previous work on motor development has
tested infants while wearing their habitual diaper
(Adolph et al., 2003; Bril & Breniere, 1989; Hallemans
et al., 2006; Ivanenko, Dominici, Cappellini & Lac-
quaniti, 2005; Sutherland, Olshen, Cooper & Woo,
1980). Our findings suggest that this practice may have
led researchers to underestimate infants’ abilities: Dia-
pers disrupt the very measures used to index the
growing skill that comes with walking experience. How
this has impacted our understanding of the underlying
developmental trajectory of walking is unknown. Dia-
pers may consistently decrease measures of skill by
shifting the learning curve to a later period of devel-
opment or alter the slope of the developmental tra-
jectory.

It seems that in the search for a pure, context-free
description of developing motor skills, it did not occur to
researchers that something as non-biological and cul-
turally dictated as diapers might influence locomotion.
Whereas biomechanics are the domain of the movement
scientist, exotic clothing and toileting practices are con-
sidered the realm of anthropologists. The reality, of
course, is not that simple. There is no context-free
description of movement and no context-free description
of development. Locomotion always occurs within an
environment; a developing child within a culture.

Acknowledgements

The project described was supported by Award Number
R37HD033486 from NICHD and by Procter and
Gamble International Relations. The content is solely the
responsibility of the authors and does not necessarily
represent the official views of the NICHD or P&G. We
thank Patrick Shrout for his advice on statistical analyses
and Judy DeLoache for helpful comments. We would
also like to thank Gladys Chan for her help preparing
figures and Meghana Komati for her assistance in data
management. We gratefully acknowledge the infants and
parents who participated in the studies.

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790 Whitney G. Cole et al.

� 2012 Blackwell Publishing Ltd.

Feeding Imprinting: The Extreme Test Case of Premature Infants Born With
Very Low Birth Weight

Moriya Suberi*
Bar Ilan University

Iris Morag* and Tzipora Strauss
Sheba Medical Center

Ronny Geva
Bar Ilan University

Feeding imprinting, considered a survival-enabling process, is not well understood. Infants born very preterm,
who first feed passively, are an effective model for studying feeding imprinting. Retrospective analysis of
neonatal intensive care unit (NICU) records of 255 infants (Mgestational age = 29.98 � 1.64) enabled exploring
the notion that direct breastfeeding (DBF) during NICU stay leads to consumption of more mother’s milk and
earlier NICU discharge. Results showed that DBF before the first bottle feeding is related to shorter transition
into oral feeding, a younger age of full oral feeding accomplishment and earlier discharge. Furthermore, the
number of DBF meals before first bottle feeding predicts more maternal milk consumption and improved
NICU outcomes. Improved performance in response to initial exposure to DBF at the age of budding feeding
abilities supports a feeding imprinting hypothesis.

Infants’ thriving is dependent on their nurturance
(Ehrenkranz et al., 2006; Hay & Lucas, 1999), both
in the physical sense and in the psychological sense
(Silberstein, Feldman, et al., 2009). It has been well
established that mother’s milk (MM) is the pre-
ferred nutritional composition for premature infants
(Academy of Nutrition and Dietetics, 2015; Eidel-
man & Schanier, 2012; Lessen & Kavanagh, 2015).
Mother’s milk provides many benefits, including
improved composition of intestinal microbiota (Sela
& Mills, 2010), lower rates of sepsis (Furman,
Taylor, Minich, Hack, & Chb, 2003) and necrotizing
enterocolitis (Cristofalo et al., 2013; Schanler,
Shulman, & Lau, 1999; Sullivan et al., 2010), lower
long-term growth failure (Hintz, 2005), fewer hospi-
tal readmissions for illness in the 2 years after
discharge (Vohr et al., 2007), and improved neu-
rodevelopmental outcomes examined at 3 months
through 15 years of age (Blaymore Bier, Oliver, Fer-
guson, & Vohr, 2002; Gibertoni et al., 2015; Isaacs,
Fischl, Quinn, Chong, & Gadian, 2010; Vohr et al.,

2007). Infants born at term typically receive MM
through oral feeding. In order to be able to orally
feed, an infant must be capable of complex integra-
tion of controlled and regulated activity of multiple
anatomic structures including the lips, jaw, cheeks,
tongue, palate, pharynx, and larynx. In addition,
coordinated rhythmic sequences of sucking, swal-
lowing, and breathing are required, as well as the
ability to sustain an alert behavioral state (Amaizu,
Shulman, Schanler, & Lau, 2008; Delaney & Arved-
son, 2008). This complex process, which requires
neurological (Silberstein, Geva, et al., 2009) and
physiological maturation of the relevant organs
(Delaney & Arvedson, 2008), begins to be develop-
mentally possible at approximately 33 weeks gesta-
tional age (GA; Bache, Pizon, Jacobs, Vaillant, &
Lecomte, 2014) or earlier (Amaizu et al., 2008).

Infants born preterm have limited and altered
experiences in their path toward achieving normal
feeding. They are challenged by the need to man-
age oral motor coordination at an earlier age than

*Moriya Suberi and Iris Morag contributed equally.
We thank the participating families as well as the teams at the

Sheba Medical Center obstetric department and NICU and at the
Developmental Neuropsychology laboratory at the Gonda Brain
Research Center.

Correspondence concerning this article should be addressed
Ronny Geva, The Department of Psychology, Gonda Brain
Research Center, Bar Ilan University, Ramat Gan Israel, 5290002.
Electronic mail may be sent to ronny.geva@biu.ac.il.

© 2017 The Authors
Child Development published by Wiley Periodicals, Inc. on behalf of Society
for Research in Child Development.
This is an open access article under the terms of the Creative Commons
Attribution-NonCommercial License, which permits use, distribution and
reproduction in any medium, provided the original work is properly cited
and is not used for commercial purposes.
0009-3920/2017/xxxx-xxxx
DOI: 10.1111/cdev.12923

Child Development, xxxx 2017, Volume 00, Number 0, Pages 1–14

http://creativecommons.org/licenses/by-nc/4.0/

http://creativecommons.org/licenses/by-nc/4.0/

infants born at term (Bu’Lock, Woolridge, & Baum,
1990), and they often lack the ability to coordinate
the sucking–swallowing–breathing cycle during
feeding (Lau, Alagugurusamy, Schanler, Smith, &
Shulman, 2000). Additional challenges in feeding
preterm infants may include difficulties in feeding
tolerance (Dollberg, Kuint, Mazkereth, & Mimouni,
2000) and the need to fortify MM in order to meet
the special nutritional needs of premature infants
(Cohen & McCallie, 2012). Neonatal intensive care
unit (NICU) staff and parents seek more accurate
protocols in order to facilitate the transition to oral
feeding in infants born preterm.

Infants born prematurely are less likely to receive
MM than infants born at term age (Donath & Amir,
2008; Flacking, Nyqvist, & Ewald, 2007). Providing
MM for the premature infant is a challenging task
for mothers due to various reasons, one of them
being the delay or lack of direct breastfeeding
(DBF; feeding directly at the breast; distinguished
from feeding expressed breast milk by bottle or
other means), owing to the complexity and diffi-
culty involved in the process of oral feeding. This
delay brings to more challenges, including reliance
on breast pumps and diminished milk supply, in
addition to a stressful environment in the NICU
(Callen & Pinelli, 2005). However, there are no defi-
nite criteria that signal infant readiness to feed
orally (Ross & Browne, 2002), and as studies exam-
ining the main predictors of the transition process
from gavage to oral feeding show inconsistent find-
ings (Jackson, Kelly, Mccann, & Purdy, 2015), the
process of oral feeding initiation and progression is
extremely challenging and somewhat unclear.

Transitioning from gavage to full oral feeding is
indeed one of the most important tasks infants
must accomplish in the NICU. It is a criterion for
discharge (American Academy of Pediatrics, 2008),
and is a demanding undertaking for many preterm
infants (Silberstein, Geva, et al., 2009), often causing
a delay in attaining full oral feeding skills and a
prolonged hospitalization in the NICU (Bakewell-
Sachs et al., 2009). Feeding difficulties frequently
linger after discharge and often elicit secondary
issues, compromising the feeding dyad relationship
(Silberstein, Feldman, et al., 2009).

Bottle feeding is considered less effortful than
DBF for infants (Ahluwalia, Morrow, & Hsia, 2005;
Lagan, Symon, Dalzell, & Whitford, 2014) and par-
ticularly for infants born preterm (Briere, 2015).
Consequently, mothers report that bottle feeding
with expressed MM is often encouraged by NICU
staff, with the implication that DBF is an additional
step forward, which will take place following

discharge (Niela-Vil�en, Axelin, Melender, & Sal-
anter€a, 2014). Moreover, bottle feeding is encour-
aged with a promise of a faster discharge, despite
the lack of direct evidence to support this claim
(Briere, 2015). Once at home, with no guidance,
mothers often find it difficult to establish

DBF

(Niela-Vil�en et al., 2014). Nevertheless, because
most studies examining the benefits of MM for pre-
term infants do not distinguish between the nutri-
tional benefits of MM provision and the additional
benefits of its “mode of administration” through
DBF (Eidelman & Schanier, 2012; Furman et al.,
2003; Gibertoni et al., 2015; Isaacs et al., 2010), it is
still unknown if indeed bottle feeding with MM
results in better NICU outcomes than DBF.

Furthermore, there is a need for research focus-
ing on the first steps of feeding, as it may be that
the first feeding phase may comprise a feeding
imprinting process and may be hyperpotent in
establishing a preferred feeding mode. As oral feed-
ing abilities become developmentally possible at
approximately 33 weeks GA (Bache et al., 2014),
infants born earlier than that may serve as an effec-
tive test case to explore the notion of feeding
imprinting. Infants born preterm experience feeding
as a major challenge. This may suggest a more pro-
nounced sensitivity to the imprinting process rela-
tive to infants born at term, who manage the
feeding process more easily, regardless of mode of
initiation. Second, infants born very preterm may
be studied at ages that precede initiation of oral
feeding, as well as during a more prolonged phase
of acquiring effective oral feeding ability, thereby
offering an effective model to study this process
effectively in human infants.

Lorenz’s imprinting term describes the process
by which newly hatched goslings identify and bond
to the first object they see as their mother (Lorenz,
1937). This primary input alters the infant’s brain,
affecting the density of postsynaptic density of
axospinous synapses in the left hyperstriatum ven-
tral, thought to form the neural basis for recogni-
tion memory (McCabe & Horn, 1988). Full-term
human infants also go through a behavioral
imprinting process in the early hours of life, medi-
ated by oral tactile sensory stimuli, normally fixat-
ing to the mother’s nipple (Mobbs, 1989). Mobbs,
Mobbs, and Mobbs (2016) recently proposed that
the oral tactile imprint to the breast serves as the
foundation for optimal breastfeeding and latching,
thereby serving the first stage of emotional develop-
ment, preceding attachment, and suggesting feed-
ing imprinting as a relevant construct in exploring
human newborns.

2 Suberi, Morag, Strauss, and Geva

This process of latching to the breast does not
typically occur in the first hours in the lives of
infants born very prematurely, as the ability to
safely feed orally develops at approximately
33 weeks GA (Bache et al., 2014; Delaney & Arved-
son, 2008). Hence, once oral feeding does begin,
feeding imprinting may still occur and serve an
important role in establishing DBF and in support-
ing its potential impact. Imprinting is also thought
to strengthen as exposure dose increases (McCabe
& Horn, 1988). Indeed, Pineda (2011a) found that
mothers who employed DBF in the NICU were
more likely to provide MM at discharge and that
the duration of MM feeding in the NICU was asso-
ciated with DBF. Importantly, age at first DBF
attempt and whether the first oral feeding attempt
was at the breast were found as potential factors in
the duration of MM feeding in the NICU (Pineda,
2011a). These findings suggest that whether the first
oral feeding is through DBF or with a bottle may
make a difference in infants born very preterm.

Some of the variables shown to be significant
predictors of the transition process from gavage to
oral feeding include GA (Dodrill, Donovan, Cleg-
horn, McMahon, & Davies, 2008), birth weight
(Jackson et al., 2015), number of oral feeding
attempts (Pickler, Best, & Crosson, 2009), behavioral
state (Kirk, Alder, & King, 2007), and medical con-
ditions (Jackson et al., 2015). Yet, to date, the nature
of the first exposure to oral feeding, namely,
whether the first oral feeding is done using a bottle
or at the breast, and its relationship with the length
of the transition period, has not been explored.
Given that the first exposure may serve a pivotal
role in facilitating the vital transition to oral feeding
in infants born very preterm, such a study may
serve to validate the notion of feeding imprinting
and offer factors affecting it in human infants.

Method

Study Design and Setting

This retrospective analysis study took place in a
Level III, 40-bed NICU at Sheba Medical Center,
Ramat Gan, Israel. The study was approved by the
human subjects committee at the study site.
Informed consent was waived because the data
were retrieved using chart review of information
which was not deemed to be sensitive. The philoso-
phy of the Newborn Individualized Developmental
Care and Assessment Program (Als, 1986) was
gradually introduced at the study site at the begin-
ning of the study period. Parents were encouraged

to actively participate in infant care at all hours.
Skin-to-skin care was promoted, as well as MM
pumping and non-nutritive sucking. DBF was pro-
moted starting at 33 weeks postmenstrual age
(PMA), aided by a lactation consultant, yet exclu-
sive DBF was nonexistent, and all oral supplemen-
tation was conducted via bottle. For purposes of
the current study, all selected cases were fed a pre-
determined volume every 3 hr. Based on previous
feeding interventions with premature infants (Yildiz
& Arikan, 2012), the minimal sample size required
for the detection of differences between the two
groups is 33 participants in each cell (Cohen, 1988).
We therefore collected data from a large cohort
(N = 340) to enable the exploration of varying attri-
butes that occur at a minimal rate of 10% of the
sample.

Data Extraction

Based on a protocol for retrospective studies
(Gearing, Mian, Barber, & Ickowicz, 2006), type, vol-
ume, and mode of infant feeding were documented
by the staff at the study site, using a patient data
management system (iMDsoft MetaVision�, Tel
Aviv, Israel). Proper data extraction was supervised
by the hospital’s information technology advisor and
directly transferred to Microsoft Excel (Version
14.0.7177.5000; Microsoft Office Professional Plus
2010), limiting manual processing.

Data Analysis

The cohort was divided according to the criterion
of having DBF exposure or not having such expo-
sure. To enable the exploration of group differences,
a multivariate analysis of variance (MANOVA) was
conducted. Exploration of the relations between
in vitro fertilization (IVF), twinhood, and the incli-
nation to DBF was conducted using a logistic
regression. Exploration of the relation between GA
and the inclination to DBF was conducted using a
chi-square analysis. A multivariate analysis of
covariance (MANCOVA) was conducted to deter-
mine differences between the DBF groups in NICU
outcomes using IVF and twinhood measures as
covariates. Feeding imprinting hypothesis was
explored by dividing the portion of the cohort that
did have DBF exposure in the NICU according to
the criterion of having exposure to DBF prior to
bottle feeding or not having such exposure. In
order to determine differences between the groups,
a MANOVA was conducted. Exploration of differ-
ences between the groups in NICU outcomes was

Feeding Imprinting 3

conducted using a MANCOVA, with intrauterine
growth restriction (IUGR), birth weight, and Clini-
cal Risk Index for Babies II (CRIB) II score as
covariates.

In order to explore the factors involved in feed-
ing imprinting, stepwise multiple regressions were
conducted predicting length of transition period,
age at full oral feeding accomplishment, and age at
discharge using weight at birth, GA, sex, CRIB II
score, Apgar 1, Apgar 5, singleton or twin, IVF,
IUGR, maternal age, primiparous or multiparous,
age at first bottle feeding, age at first DBF, number
of DBF meals prior to first bottle feeding, and per-
centage of MM consumed as possible predictors. A
similar stepwise regression was conducted to
explore predictors of age at first bottle feeding. In
order to explore the relations between maternal
age, parity, and the inclination to DBF, a MANOVA
was conducted. All analyses were conducted using
SPSS (Version 20.0; IBM� SPSS� Statistics, Armonk,
NY. USA).

Participants

Participants included 340 infants who were
admitted to the NICU at Sheba Medical Center
between January 1, 2012 and April 30, 2015 and
were born earlier than 32 weeks GA, excluding
infants who presented congenital malformations
(n = 18), intraventricular hemorrhages Grades III or
IV (n = 11), necrotizing enterocolitis (n = 10),
infants that died during hospitalization (n = 46),
and infants receiving different feeding protocols
(n = 13), resulting in a final sample of 255 infants.
Demographic characteristics are presented in
Table 1. The Sheba Medical Center is the largest
public hospital in Israel, with a Level III NICU unit,
catering to the greater municipal area of central
Israel. The mean education level of mothers repre-
sents attaining a degree at the undergraduate level.
According to the Central Bureau of Statistics (Yafe,
2013), this level of education is characteristic of 57%
of women at this age range in Israel. Based on the
above needed sample size calculation, this sample
size was designed to enable sufficient power to
explore moderating factors such as maternal age,
parity, and IVF.

Measures

Seven dependent measures were collected: first
nutritive DBF, defined as the first time an infant
suckled directly at the breast and some milk was
transferred. Infants feeding directly at the breast

were weighed before and after breastfeeding to
assess milk intake; the number of DBF meals prior to
the first bottle feeding was noted; first bottle feeding,
defined as the first time an infant was fed with a
bottle, irrespective of whether the bottle contained
MM or formula; transition period calculated from the
day at which an infant was first fed with a bottle,
until the day in which full oral feeding was accom-
plished; percent nutritive DBF in NICU was calcu-
lated as the percent of meals in which nutritive
DBF occurred of all feedings from the first DBF
attempt until discharge. Every nutritive DBF
attempt was counted, even when supplementation
via bottle or enteral feeds was necessary; percent
MM consumed in NICU was calculated out of the
total amount of milk consumed by an infant from
the time of admission until discharge; MM provision
at discharge was noted if the infant received MM
during the last day in the NICU, whether by bottle
or at the breast; nutritive DBF at discharge was noted
if the infant was directly breastfed during the last
2 days in the NICU; finally, infant medical risk was
measured by the CRIB II (Parry, Tucker, & Tarnow-
Mordi, 2003; Figure 1).

Results

Sixty-six percent (n = 169) of infants were directly
breastfed at least once during their NICU stay. A

Table 1
Demographic Characteristics of the Cohort

M SD Range

Birth weight (g) 1,286.96 311.22 478–2,023
GA (weeks) birth 29.98 1.64 24.6–31.6
CRIB II 6.28 2.98 1–19
Apgar 1 7.50 2.09 0–1

0

Apgar 5 9.09 1.25 4–

10

Maternal age (year) 31.92 5.72 20–51
Maternal education (year) 15.37 3.01 12–

30

Paternal age (year) 34.26 6.01 21–52
Paternal education (year) 14.55 2.94 8–29
No partner 7.8%
Male/female 49.4%/50.6%
Singleton/twin 43.1%/56.9%
Twin death 2.35%
Primipara/multipara 45.5%/54.5%
IUGR 10.2%
IVF 43.14%

Note. GA = gestational age; CRIB = Clinical Risk Index for
Babies; IUGR = intrauterine growth restriction; IVF = in vitro fer-
tilization.

4 Suberi, Morag, Strauss, and Geva

MANOVA and a chi-square analysis were con-
ducted to determine differences in perinatal mea-
sures between infants who were DBF at least once

during their NICU stay (DBF group) and those
who were not (no DBF group), exploring the notion
that these characteristics possibly affect the

Figure 1. Research paradigm: Timeline of data collection and dependent measures. NICU = neonatal intensive care unit; DBF = direct
breastfeeding; MM = mother’s milk.

Table 2
Demographic Characteristics DBF Versus No DBF Groups

DBF group (n = 168) No DBF group (n = 87)

pM SD M SD

Birth weight (g) 1,299.09 315.94 1,263.53 302.31 .388
GA (weeks) birth 29.96 1.61 30.02 1.72 .772
CRIB II (score) 6.26 2.93 6.31 3.09 .887
Apgar 1 min 7.42 2.07 7.65 2.13 .403
Apgar 5 min 9.06 1.18 9.14 1.37 .628
Maternal age (year) 31.63 5.57 32.49 5.99 .264
Maternal education (year) 15.62 3.04 14.85 2.89 .073
Paternal age (year) 34.27 5.81 35.11 5.16 .318
Paternal education (year) 14.71 2.82 14.19 3.18 .247
No partner 5.96% 9.12% .327
Male/female 54.8/45.2% 42.5/57.5% .064
Singleton/twin 49.4/50.6% 31/69% .005

**

Twin death 2.98% 1.15% .364
Primipara/multipara 45.2/54.8% 46/54% .908
IUGR 8.93% 12.64% .355
IVF 33.93% 50.57% .010**

Note. DBF = direct breastfeeding; GA = gestational age; CRIB = Clinical Risk Index for Babies; IUGR = intrauterine growth restriction;
IVF = in vitro fertilization.
**p < .01.

Feeding Imprinting 5

inclination to DBF (see Table 2). The no DBF group
was found to have a higher percentage of twins
(68.97%) compared to the DBF group (50.56%;
p < .005), as well as a higher percentage of infants conceived via IVF (50.57%) compared to the DBF group (33.93%; p < .01). Due to the high percentage of twins among infants born to mothers who con- ceived via IVF (75.76%) compared to mothers who conceived spontaneously (43.66%), a logistic regres- sion analysis was conducted to explore if and how the two findings are related. A test of the full model against a constant only model was statisti- cally significant, indicating that the predictors as a set reliably predicted the likelihood to DBF, v2(3) = 11.345, p < .01. Prediction success overall was 65.9%, however, a Nagelkerke’s R2 of .06 indi- cated that the model accounts for 6% of the vari- ance. The Wald criterion demonstrated that only twins who have been conceived via IVF have a higher likelihood of belonging to the no DBF group (p = .001), whereas infants who are twins but con- ceived spontaneously (p = .089; ns) and singletons who have been conceived via IVF (p = .327; ns) do not.

In order to explore the notion that GA does not
affect the inclination to DBF, a chi-square test was
conducted to examine the relation between

extremely premature infants (24–28 weeks GA) and
belonging to the no DBF group. The relation
between these variables was not significant,
v2(1) = 0.13, p = .723; ns, indicating that extremely
premature infants are not more likely to be in the
no DBF group.

In order to explore the notion that DBF in the
NICU may be a factor in NICU outcomes, a MAN-
COVA was conducted, controlling for factors that
differed between the DBF and no DBF groups, that
is, twinhood and IVF. The NICU feeding method
outcome relations to DBF indicated that infants in
the DBF group were more likely to receive MM at
discharge (M = 83 � 38%) compared with infants
in the no DBF group (M = 18 � 39%), F(1, 251) =
148.61, p < .001, g2 = .37 (see Figure 2), and received a higher percentage of MM during their NICU stay (M = 82 � 24%) compared to infants in the no DBF group (M = 26% � 33), F(1, 251) = 223.58, p < .001, g2 = .47 (see Figure 2). No group differences were noted in length of the transition period, PMA at full oral feeding accomplishment, and weight and PMA at discharge.

Of the infants in the DBF group, 60.36%
(n = 102) were DBF prior to being bottle fed. In
order to explore the importance of feeding imprint-
ing, that is, the importance of being exposed to

0
10

20

30

40

50

60

70

80

90

100

MM at Discharge MM En�re NICU Stay

% No DBF

DBF

** **

Figure 2. MM provision in DBF versus no DBF groups. NICU = neonatal intensive care unit; DBF = direct breastfeeding; MM = mother’s
milk.
**p < .01.

6 Suberi, Morag, Strauss, and Geva

DBF on the first oral feeding exposure, as compared
with being exposed to DBF after having been
exposed to bottle feeding, a MANOVA and a chi-
square analysis were conducted to explore perinatal
differences between infants who were first DBF
prior to being bottle fed (DBF initial exposure
group [DBF-IE]; n = 102, 40% of the total sample)
and infants who were DBF later during their NICU
stay (bottle IE group [bottle-IE]; n = 66, 25.88% of
the total sample). In comparing the demographic
characteristics of IE-type groups, a selective bias
was noted. The bottle-IE group was found to have
a higher percentage of infants diagnosed with
IUGR (18.18%) compared to the DBF-IE group
(2.94%), v2(1, 168) = 11.45, p < .001. Accordingly, infants in the bottle-IE group were found to have a lower birth weight (M = 1,190.55 � 303.18 g) than infants in the DBF-IE group (M = 1,369.32 � 305.3 g), F(1, 163) = 13.82, p < .001, g2 = .08, and higher CRIB II scores (M = 6.86 � 2.86) than infants in the DBF-IE group (M = 5.86 � 2.92), F(1, 163), p < .03, g2 = .03, suggesting a more complicated course for participants in the bottle-IE group.

A MANCOVA was then conducted, controlling for
IUGR, birth weight, and CRIB II scores in order to
explore differences in NICU outcomes between the

two groups. The analysis showed that infants in the
DBF-IE group had a shorter transition period
(M = 9.22 � 5.29) than infants in the bottle-IE
group (M =11.53 � 6.66), F(1, 162) = 6.74, p < .011, g2 = .04, they accomplished full oral feeding at a younger PMA (M = 35.36 � 0.85) than infants in the bottle-IE group (M = 35.76 � 1.39), F(1, 162) = 7.51, p < .007, g2 = .044, and were discharged at a younger PMA (M = 36.80 � 0.96), almost a week earlier, than infants in the bottle-IE group (M = 37.44 � 1.72), F(1, 162) = 11.43, p < .001, g2 = .066. In addition, once DBF was initiated, infants in the DBF-IE group had a higher percentage of DBF meals (M = 4.2 � 3.6%) compared to infants in the bottle-IE group (M = 2.8 � 3.5%), F(1, 162) = 6.42, p < .028, g2 = .038 (Figures 3 and 4). No differences were found in the percentage of MM throughout the NICU stay, DBF and MM pro- vision at discharge, and weight at discharge between the groups.

In order to explore the factors involved in feeding
imprinting, stepwise multiple regressions were con-
ducted predicting (a) length of transition period, (b)
PMA at full oral feeding accomplishment, and (c)
PMA at discharge, using weight at birth, GA, sex,
CRIB II score, Apgar 1, Apgar 5, singleton or twin,
IVF, IUGR, maternal age, primiparous or

35

35.5

36

36.5

37

37.5

38

Full Oral Feeding Accomplishment Discharge

PM
A

(W
ee

ks
)

DBF-IE

Bo�le-IE

***

**

Figure 3. PMA at full oral feeding accomplishment and discharge of DBF-IE versus bottle-IE groups (adjusted means). PMA = post-
menstrual age; DBF = direct breastfeeding; IE = initial exposure.
**p < .01. ***p < .001.

Feeding Imprinting 7

multiparous, PMA at first bottle feeding, PMA at first
DBF, number of DBF meals prior to first bottle feed-
ing, and percentage of MM consumed. Comparable
models were explored with one caveat: In Regression
Analyses 1 and 2, predicting length of transition per-
iod and PMA at full oral feeding accomplishment,
the percentage of MM consumed up to full oral feed-
ing accomplishment was entered, whereas in Regres-
sion 3, predicting PMA at discharge, percentage of
MM consumed up to discharge was entered.

The data contained approximately normally dis-
tributed measures and had met the assumptions of
collinearity, homogeneity of variance and linearity,
and independent errors (Durbin–Watson: Regres-
sion 1 = 1.702, Regression 2 = 1.673, Regression
3 = 1.86). Analyses of standard residuals indicated
two outliers in Regression 1, one outlier in Regres-
sion 2, and five outliers in Regression 3. The out-
liers were not included in the analyses. The final
step of each regression is presented in Table 3.

Testing for predictors of length of the transition
period, birth weight, IUGR, maternal age, and the
number of DBF meals prior to bottle feeding were
entered into the regression equation. Other vari-
ables were not found to predict the length of the
transition period and were therefore not included.

According to the multiple correlation coefficients
(R2 change), birth weight accounted for approxi-
mately 20.2% of the variance, IUGR accounted for
approximately 4.9% of the variance, maternal age
4.2% of the variance, and number of DBF meals
prior to bottle feeding accounted for additional
2.3% of the variance.

Similarly, testing for predictors of PMA at full
oral feeding accomplishment yielded comparable
variables, with PMA at first bottle feeding account-
ing for approximately 50.3% of the variance, birth
weight for 7.8% of the variance, maternal age 2%,
GA 1.7%, CRIB II score 2%, and number of DBF
meals prior to bottle feeding accounted for addi-
tional 0.8% of the variance.

Testing for predictors of PMA at discharge
showed that PMA at first bottle feeding accounted
for approximately 46.9% of the variance, birth
weight for 7.0%, IUGR for 2.5%, number of DBF
meals prior to bottle feeding 1.6%, and PMA at first
DBF accounted for additional 1.6% of the variance.
No correlation was found between PMA at first
bottle feeding and the number of DBF prior to bot-
tle feeding (r = �.099, p < .116; ns).

In order to evaluate which variables predicted
PMA at first bottle feeding, a stepwise regression

Figure 4. Transition period and DBF meals in DBF-IE versus bottle-IE groups (adjusted means). DBF = direct breastfeeding; IE = initial
exposure.
*p < .05. **p = .011.

8 Suberi, Morag, Strauss, and Geva

was conducted using a comparable regression
model (see Table 4). IUGR, GA, CRIB II, and Apgar
5 scores were entered into the regression equation.
The rest of the variables were not found to predict
PMA at first oral feeding and were therefore left
out. IUGR accounted for 29.5% of the variance, GA
accounted for 2.4%, CRIB II score 3.7%, and Apgar
5 score accounted for additional 1.2% of the vari-
ance. Experience with DBF did not account for
PMA at first bottle feeding.

Finally, in order to evaluate the relations
between maternal age, parity, the inclination to
DBF, and NICU outcomes (i.e., age at full oral feed-
ing accomplishment, length of transition period,
and age at discharge), a MANOVA was conducted.
The analysis indicated that the interaction between

the number of previous pregnancies and DBF was
significant, F(3, 236) = 2.77, p < .05; Wilk’s Ʌ = .966, partial g2 = .34, as well as the interaction between maternal age and DBF, F(3, 236) = 2.984, p < .05; Wilk’s Ʌ = .963, partial g2 = .037, indicat- ing that the older and more experienced the mother who directly breastfed, the better infant outcomes were. More specifically, univariate tests show that the older the mother, the shorter the transition per- iod, F(1, 238) = 4.778, p < .05, partial g2 = .02, and the younger the infant at full oral feeding accom- plishment, F(1, 238) = 4.267, p < .05, partial g2 = .018. There was no main effect of the number of previous gestations on NICU outcomes, F(1, 238) = 2.198, p = ns; Wilk’s Ʌ = .973, partial g2 = .027, indicating that in exploring maternal

Table 3
Stepwise Regressions Predicting Length of Transition Period, PMA at Full Oral Feeding Accomplishment, and PMA at Discharge

Dependent variable
Independent variables

entered B t R2 F
R2

change
F

change df1 df2

Length of transition period (days) (Constant) 24.850 10.152** .316 28.035** .023 8.014** 4 243
Birth weight �0.006 �4.695**
IUGR 5.047 4.078**
Maternal age �0.228 �3.948**
DBF before bottle (count) �0.400 �2.831**

PMA at full oral feeding
accomplishment

(Constant) �4.440 �1.646 .647 73.602** .008 5.759* 6 241
PMA at first bottle feeding 0.973 11.541**
Birth weight �0.001 �2.268*
Maternal age �0.038 �4.488**
GA 0.267 4.588**
CRIB II 0.164 3.781**
DBF before bottle (count) �0.051 �2.400*

PMA at discharge (Constant) 2.380 0.780 .596 71.762** .016 9.764** 5 243
PMA first bottle feeding 1.035 11.558**
Birth weight �0.001 �3.386**
IUGR 0.862 3.896**
DBF before bottle (count) �0.101 �4.114**
PMA first DBF 0.011 3.125**

Note. DBF = direct breastfeeding; GA = gestational age; PMA = postmenstrual age; IUGR = intrauterine growth restriction.
*p < .05. **p < .01.

Table 4
Final Step of Regression Testing for Predictors of PMA at First Bottle Feeding

Dependent variable Independent variables entered B t R2 F R2 change F change df1 df2

PMA at first bottle feeding (Constant) 30.018 33.185** .368 35.004** .012 4.535* 4 245
IUGR 0.532 5.514**
GA birth 0.131 4.838**
CRIB II 0.056 3.546**
Apgar 5 �0.037 �2.130*

Note. GA = gestational age; CRIB = Clinical Risk Index for Babies; IUGR = intrauterine growth restriction; PMA = postmenstrual age.
*p < .05. **p < .01.

Feeding Imprinting 9

maturational factors, it is not the number of previ-
ous gestations alone that affects NICU outcomes.

Discussion

The present study sought to revisit the construct of
feeding imprinting by using the test case of very pre-
term infants given the stronger implications feeding
trajectories serve in this cohort. Key findings of this
study suggest that a feeding imprinting process
occurs in very preterm infants, with DBF imprinting
leading to improved NICU outcomes. More specifi-
cally, findings showed that DBF imprinting was
related to an earlier and quicker attainment of full
oral feeding, a higher percentage of DBF throughout
the NICU hospitalization period, and an earlier dis-
charge from the NICU. In addition, similar to other
imprinting phenomena, a dose–response function
was seen, such that the number of DBF meals prior
to first bottle feeding predicted the length of the
transition period to full oral feeding, PMA at full
oral feeding accomplishment, and PMA at dis-
charge. This finding is consistent with the classic
Sluckin and Salzen’s (1961) framework by which
imprinting in precocious organisms (in their case,
birds) occurs in a sensitive time period and is
strengthened by the amount of experience or expo-
sure to the stimulus (Sluckin & Salzen, 1961). This
conclusion should be treated with caution, as poten-
tial mediators and moderators may be effective in
this process.

In considering the exposure notion, current data
with infants born very preterm seem to take apart
some of the unique contributions of each process in
neonatal feeding, thus enabling the exploration of the
role of exposure to content, administration mode, and
timing of the exposure within the sensitive time period.
Specifically the frequency of DBF meals prior to first
bottle feeding was found to be a significant predictor
of length of transition period, and PMA at full oral
feeding accomplishment and discharge, but the per-
centage of MM consumed was not found to predict
any of these variables. This finding uncovers the bene-
fits of DBF in the process of oral feeding acquisition,
thus suggesting that the known nutritional benefits of
MM to the infant (Andreas, Kampmann, & Mehring
Le-Doare, 2015; Eidelman & Schanier, 2012) are aug-
mented by early exposure to DBF.

This was shown in two ways: First, infants who
were DBF in the NICU received more MM through-
out their NICU stay and at discharge compared to
infants who were not DBF in the NICU, thereby
replicating previous work by Pineda (2011a).

Second, infants who were DBF imprinted obtained
the ability to fully feed orally in a shorter amount
of time compared to infants who were bottle
imprinted, and accomplished full oral feeding at an
earlier PMA, resulting in higher rates of DBF and a
NICU discharge earlier by almost a week.

What accounts for this effect? It appears that mat-
uration does not account for the DBF effect. Overall,
PMA at first oral feeding was found to be a signifi-
cant predictor of PMA at discharge and PMA at full
oral feeding accomplishment, suggesting that earlier
exposure to oral stimulation, regardless of stimula-
tion type, possibly facilitates the acquisition of feed-
ing skills. Importantly, however, earlier exposure
did not predict the length of the transition period,
indicating that there is more to the acquisition per-
iod than timing and earlier onset of exposure.

Ease of feeding may partly apply to the DBF
effect. DBF has been considered by some as more
strenuous than bottle feeding for infants in general
(Ahluwalia et al., 2005; Lagan et al., 2014) and
specifically for infants born preterm (Briere, 2015).
Yet, data regarding very low birth weight (VLBW)
infants have shown a greater stability of oxygen
saturation and breathing during DBF when com-
pared with bottle feeding (Blaymore Bier et al.,
1993; Dowling & Thanattherakul, 2001).

Consequently, the process seems to be dependent
on neonatal tailored exposure, specifically to tactile
sensory stimuli, achieved through Merkel cell
mechanosensors in the buccal mucosa (Mobbs et al.,
2016). The oral tactile imprint is a learned form of
perceptual recognition via Merkel cell mechanosen-
sation which governs the imprinting process (Mak-
simovic, Baba, & Lumpkin, 2013). Other effects of
DBF include somatosensory exposure along with an
opportunity for bonding. Specifically, skin-to-skin
contact, which naturally comes into play during
DBF, has been shown to activate oxytocin release
and reduce stress and anxiety responses in parents
of preterm infants (Cong et al., 2015).

DBF could therefore set the beginning of the oral
feeding journey with a more positive experience
leading to a quicker learning process with more
successful results, with more intensive exposure
resulting in a more efficient transition. Indeed, the
regression models underscored the number of DBF
meals prior to the first bottle feeding as an impor-
tant predictor of the length of the transition period
to full oral feeding, PMA at full oral feeding accom-
plishment, and PMA at discharge.

Importantly, of all the variables found as predic-
tors of these outcome measures, the number of DBF
meals prior to the first bottle feeding is the only

10 Suberi, Morag, Strauss, and Geva

one over which caregivers may have some control.
Being able to affect NICU outcomes directly is
extremely significant, as most infant variables in the
NICU are uncontrollable (i.e., birth weight, GA,
health condition, etc.).

Pending replication, these findings may easily be
translated into practice for all dyads with some
caveats. Current data uncovered some demographic
biases of infants’ likelihood of receiving DBF. First,
we found that infants born as part of a multiple
were less likely to be DBF than singletons, in a
manner compatible with some previous research
(Geraghty, Pinney, Sethuraman, Roy-Chaudhury, &
Kalkwarf, 2004; McDonald et al., 2012; Yokoyama
et al., 2006) but not with others who examined
VLBW infants born as part of a multiple birth
(Pineda, 2011b; Smith, Durkin, Hinton, Bellinger, &
Kuhn, 2003). The different finding may be
explained by a higher rate of twins in the current
cohort as compared with the latter cohorts (20%
and 24.6%, respectively; Pineda, 2011b; Smith et al.,
2003; compared to 53% twins in the present cohort)
and higher birth weights, more mature GA, and
sociodemographic advantages compared to the cur-
rent cohort, differences that may have contributed
to their high DBF rates (Smith et al., 2003). Further
research is recommended in order to clarify this
issue.

Another factor affecting the likelihood of DBF
was conception via IVF. We found that infants con-
ceived via IVF were less likely to be DBF than
infants conceived spontaneously. This finding is
partially concordant with data in other cohorts who
do not necessarily comprise of infants born very
preterm, showing that mothers who conceived via
IVF were less likely to exclusively DBF their infants
yet were as likely to provide some DBF (Castelli
et al., 2015; Fisher et al., 2013), if not more so
(Hammarberg, Fisher, Wynter, & Rowe, 2011), than
mothers who conceived spontaneously.

Both conception of twins and conception via IVF
involve significant segments of populations of
infants born preterm. However, because conception
via IVF often results in multiparous gestations, it is
important to explore the interaction between these
two factors as a selected group may explain these
effects. Current data enabled us to explore this
interaction. A logistic regression analysis showed
that twins conceived through IVF were less likely
to receive DBF compared to spontaneousely con-
ceived singletons, an effect not seen among non-IVF
twins or IVF singletons. This then may point to a
subgroup of mothers, mothers who conceived via
IVF and gave birth to twins, who may require a

targeted attention, as they are possibly challenged
by their increased demands.

Finally, with regard to demographic characteris-
tics that possibly play a role in the feeding imprint-
ing process, maternal age predicted the length of
the transition period and PMA at full oral feeding
accomplishment. Note that the current study
included mothers aged 20–51 and thus did not
include teenage mothers. Findings showed that the
older the mother, the shorter the transition period
and the younger the infant is at full oral feeding
accomplishment. Furthermore, the older and more
experienced the mother who directly breastfed was,
the better infant outcomes were. Note that solely
having had previous pregnancies did not affect the
NICU outcomes measured. This possibly under-
scores the role of maternal experience and matura-
tion as a broader process that reflects a more
complex process than solely the mother’s personal
direct experience. Given the wide age range of
motherhood these days, the current finding sug-
gests that an exploration of the topic is required.

Being a retrospective analysis, this study was
limited by the inability to influence data collection.
Data that were not available to be tested for media-
tory or moderator effects on this study’s findings
include mother-related feeding measures (e.g., skin-
to-skin care, prior maternal experience in DBF, and
parental involvement in infant care), data regarding
respiratory and feeding complications, and input
from members of the multidisciplinary team at the
NICU. Further research in the field may gain from
addressing these variables.

Overall, current findings are suggestive of feeding
imprinting in human infants by showing that DBF
can help in facilitating infant thriving, thereby possi-
bly contributing to public policy development and
assisting NICU staff in forming evidence-based
guidelines for team and parents regarding infant
feeding in the NICU. There are a few protocols avail-
able to guide clinicians, yet they are not always
soundly based on research evidence (Pickler, Reyna,
Wetzel, & Lewis, 2015), and they are only partly
adopted by NICU staff (Jackson et al., 2015). Pend-
ing replication, current results may yield future pub-
lic policy changes in oral–motor intervention
protocols for premature infants, as the data refuted
the claims that infants who are DBF in the NICU are
discharged later or at a lower weight than infants
who are fed by bottle solely. This may imply that
NICU staff may encourage mothers of premature
infants to DBF their infants as many times as possi-
ble prior to the first bottle feeding, even if exclusive
DBF is unattainable. That is, findings support the

Feeding Imprinting 11

notion of feeding imprinting in late term age, high-
lighting the importance of further research into this
vital process, not only for supporting infant survival
and growth, but also for supporting infants’ physical
and emotional thriving later on.

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