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Memory
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Inhibitory control of threat remembering in PTSD
Andrei-Cristian Tudorache, Wissam El-Hage, Géraldine Tapia, Nelly
Goutaudier, Sandrine Kalenzaga, Badiâa Bouazzaoui, Nemat Jaafari & David
Clarys
To cite this article: Andrei-Cristian Tudorache, Wissam El-Hage, Géraldine Tapia, Nelly
Goutaudier, Sandrine Kalenzaga, Badiâa Bouazzaoui, Nemat Jaafari & David Clarys
(2019) Inhibitory control of threat remembering in PTSD, Memory, 27:10, 1404-1414, DOI:
10.1080/09658211.2019.1662053
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Inhibitory control of threat remembering in PTSD
Andrei-Cristian Tudorachea, Wissam El-Hageb, Géraldine Tapiac, Nelly Goutaudiera, Sandrine Kalenzagaa,
Badiâa Bouazzaouia, Nemat Jaafarid and David Clarysa
aCentre de Recherches sur la Cognition et l’Apprentissage, UMR CNRS 7295, Universite ́ de Poitiers, Université de Tours, Poitiers, Tours,
France; bUMR 1253, iBrain, Université de Tours, CHRU de Tours, Inserm, Tours, France; cLaboratoire de Psychologie EA4139, Université de
Bordeaux, Bordeaux, France; dUnité de recherche clinique intersectorielle en psychiatrie à vocation régionale Pierre Deniker du Centre
Hospitalier Henri Laborit, Inserm CIC-P 1402, Inserm U 1084 Experimental and Clinical Neurosciences Laboratory, Université de Poitiers, CHU
Poitiers, Groupement De Recherche CNRS 3557, Poitiers, France
ABSTRACT
Intrusive traumatic recollections suggest an inability in Posttraumatic Stress Disorder (PTSD) to
control and notably to inhibit memories for trauma-related information. Supported by inhibitory
deficits found on experimental settings in PTSD, memory functioning and memory biases in the
disorder were usually explained through inhibitory and control deficits in the processing of
trauma-related information. The present study aimed to directly assess this hypothesis by
investigating memory control abilities for emotional information in PTSD. For this purpose, 34
patients diagnosed with PTSD were compared to 37 non-PTSD controls on an item-cued
directed forgetting paradigm for emotional words combined with a Remember/Know
recognition procedure.
revealed enhanced amounts of Remember recognitions for
trauma-related words in PTSD. Moreover, we replicated findings of memory control
impairments in the disorder. However, such impairments only occurred for non-trauma-
related words. Accordingly, it appeared that PTSD patients presented preserved memory
control abilities for trauma-related words, at the expenses of other emotional valences.
Surprisingly, PTSD patients presented a preserved ability to control and notably to inhibit
their memory functioning for trauma-related material. In addition to potential theoretical and
clinical relevance, these results are discussed in the light of resource reallocation hypotheses
and vigilant-avoidant theories of information processing in PTSD.
ARTICLE HISTORY
Received 1 March 2019
Accepted 25 August 2019
KEYWORDS
Posttraumatic Stress Disorder
(PTSD); memory; inhibition;
emotion; remember/know;
directed forgetting
The constant re-experiencing of traumatic events through
involuntary and uncontrollable intrusive reminiscences is
one of the most salient and distressing symptoms of Post-
traumatic Stress Disorder (PTSD; Diagnostic and statistical
manual of mental disorders 5th ed., DSM-5; American Psy-
chiatric Association, APA, 2013). Among other specificities,
the strong emotional and sensorial reliving, the lack of
control or the enhanced vividness (i.e., flashbacks) dis-
tinguish intrusive symptoms from other types of memories
(APA, 2013; Brewin, Gregory, Lipton, & Burgess, 2010; Ehlers
& Clark, 2000; Foa, Molnar, & Cashman, 1995; Harvey &
Bryant, 1999). Conceived as a central factor not only in
the distress caused by the disorder, but also in the develop-
ment and maintenance of symptoms (e.g., Brewin et al.,
2010; Ehlers & Clark, 2000; Rubin, Berntsen, & Bohni,
2008), memory functioning in PTSD inspired numerous
amounts of studies in the past decades. However, it is
important to note that, despite large quantities of data in
this area, investigations of memory functioning based on
standardised memory tests have yielded inconsistent
findings, reporting alternately impaired or preserved
memory skills in PTSD (see review by Tapia, Clarys, El-
Hage, & Isingrini, 2007). Nevertheless, some interesting
results have emerged from experimental approaches in
which memory is assessed in conjunction with other fea-
tures of PTSD symptomatology, such as emotional proces-
sing (Golier, Yehuda, Lupien, & Harvey, 2003), attention
allocation (Paunovic, Lundh, & Öst, 2002), states of con-
sciousness (Tapia, Clarys, Bugaiska, & El-Hage, 2012), and
executive functioning (Cottencin et al., 2006).
Among these features, emotional processing was
largely questioned in PTSD. Regarding memory, the
highly distressing emotional reliving associated with
trauma memories drew attention to the interactions
between emotions and memory functioning in PTSD, as
highlighted in the review by Tapia and colleagues (2007).
In studies conducted in community samples, manipulation
of the emotional valence of processed material usually
highlighted a beneficial effect for memory performance
of emotionally salient stimuli compared with neutral ones
(see review by Hamann, 2001). However, transposed to
PTSD patients, the study of emotional processing has
revealed biases in favour of threatening information
specifically. While performing poorly for neutral and
© 2019 Informa UK Limited, trading as Taylor & Francis Group
CONTACT Andrei-Cristian Tudorache andrei.cristian.tudorache@univ-poitiers.fr Centre de Recherches sur la Cognition et l’Apprentissage, Maison des
Sciences de l’Homme et de la Société, CNRS UMR 7295 – Université de Poitiers, 5 rue Théodore Lefebvre, TSA 21103, F-86073, Poitiers CEDEX 9, France
MEMORY
2019, VOL. 27, NO. 10, 1404–1414
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mailto:andrei.cristian.tudorache@univ-poitiers.fr
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positive stimuli, PTSD patients demonstrated improved
memory performance for negative or trauma-related
stimuli compared with non-PTSD controls (e.g., Golier
et al., 2003; Lin, Hofmann, Qian, & Li, 2015; Moradi,
Taghavi, Neshat-Doost, Yule, & Dalgleish, 2000; Tapia
et al., 2012; Thomas, Goegan, Newman, Arndt, & Sears,
2013; Zeitlin & McNally, 1991).
In addition to their emotional intensity, traumatic remi-
niscences can become markedly vivid and conscious to the
point that patients can have the impression that the event
is occurring at the moment (APA, 2013; Ehlers & Clark,
2000). While the involuntary, unorganised and fragmented
aspects of intrusive symptoms led cognitive models of
PTSD to posit deficits in memory contextualisation (e.g.,
Brewin et al., 2010; Ehlers & Clark, 2000), the “here and
now” quality suggest contextualisation could otherwise
reach unusually high levels for specific aspects of trauma
memories. Although rarely investigated in PTSD studies,
this consideration echoes Tulving’s (1985) proposal to sep-
arate the declarative memory system into episodic and
semantic components based on the states of conscious-
ness associated with memory. Whereas the noetic con-
sciousness refers to the awareness of knowing and
reflects the semantic memory system, the autonoetic con-
sciousness, associated with episodic memory, implies the
ability to “travel back in time”, getting the impression of
reliving the encoding of an event. Accordingly, semantic
memory is considered a stock of general and uncontextua-
lized knowledge about the world and environment (e.g.,
the knowledge of capital cities), whereas episodic
memory is a stock of highly contextualised personally
experienced events (e.g., the remembering of your last
holiday), including notably emotional and perceptual
details. Based on auto-evaluations of their associated
states of consciousness, the Remember/Know (R/K) para-
digm was designed for experimental assessments of
these two memory forms (Tulving, 1985). This paradigm
respectively reflects autonoetic and noetic states of con-
sciousness by distinguishing a Remember (R) response
type when a stimulus is retrieved with contextual details
from its encoding (e.g., associated items, memories,
images, feelings), and a Know (K) response type when no
contextual information could be provided.
As far as the characteristics of PTSD intrusive memories
are concerned, the R/K paradigm has initially been used to
assess the hypothesis of general impairments in contextua-
lising memory acquisitions. A study conducted in this frame-
work confirmed this hypothesis by revealing a specific
deficit in R recognitions for neutral words in PTSD partici-
pants as compared to un-traumatized control ones. In con-
trast, K responses were preserved (Tapia, Clarys, El Hage,
Belzung, & Isingrini, 2007). In another study, Tapia et al.
(2012) compared PTSD to un-traumatized anxious/depress-
ive participants and healthy control ones on a R/K recog-
nition procedure of positive, neutral or negative words.
Interestingly, this study highlighted that recognition of
negative stimuli was accompanied by R responses to a
greater extent in the PTSD group compared with the
control sample (Tapia et al., 2012). Suggesting that recollec-
tion of negative stimuli in PTSD could be associated with
enhanced reliving of the memory acquisition, this result
emphasises the relevance of the R/K paradigm in exper-
imental approaches of intrusive symptoms. However, it is
interesting to note that there were not statistically signifi-
cant differences when PTSD patients were compared with
anxious and depressive patients. Moreover, the negative
stimuli used in this study encompassed both trauma-
related stimuli (e.g., accident, weapon, death) and non-
trauma-related ones (e.g., sadness, tiredness, delirium). It
is thus unclear whether or not qualitatively improved
access to negative information reflects a general negativity
bias in PTSD due to anxious or depressive comorbidities, or a
specific preferential processing of reminders of traumatic
experiences. Focusing on this issue appears to be critical
for interpretation of R/K findings in PTSD.
Accordingly, the present study sought to replicate Tapia
et al. (2012) methodology, using a R/K paradigm to dis-
tinguish between the encoding and recognition of positive,
neutral, non-trauma-negative and trauma-related words. In
addition to examination of emotional biases in PTSD
memory functioning, a second aim was to evaluate the cog-
nitive mechanisms underlying such biases. In this regard,
both the inability of PTSD patients to inhibit their trauma-
related thoughts and experimental investigations of infor-
mation processing in PTSD suggested the presence of
inhibitory deficits in the processing of negative or trauma-
related information (e.g., El Khoury-Malhame et al., 2011;
Fleurkens, Rinck, & van Minnen, 2011; Paunovic et al.,
2002). Mainly investigated through Emotional Stroop
tasks, inhibitory deficits on experimental settings were
translated by enhanced interferences in colour naming in
the presence of negative or trauma-related stimuli (see for
instance the meta-analysis by Cisler et al., 2011). These
inhibitory deficits may appear disjointed from clinical inhibi-
tory deficits in preventing trauma-related intrusions and re-
experiencing. However, some studies revealed that inhibi-
tory or control deficits on cognitive tasks specifically corre-
lated with re-experiencing symptoms (e.g., Bomyea, Amir,
& Lang, 2012; Vasterling, Brailey, Constans, & Sutker, 1998).
As a consequence, such inhibitory deficits became
common explanations of memory biases in PTSD.
However, studies focusing on this hypothesis highly
diverge regarding both findings and methodological
choices. Moreover, to our knowledge, few studies have
experimentally investigated memory control abilities for
emotional material in PTSD and, to date, none have jointly
examined the distinction between R or K memories.
Among methodological choices, the directed forgetting
task appeared highly promising for memory control assess-
ments. Conceived as a classical memory task, the directed
forgetting procedure differed in that instructions to mem-
orise or inhibit the memorisation are given after each item
(item method) or after a list of items (list method). Prior
research has shown that healthy participants completing
MEMORY 1405
this paradigm often display a directed forgetting effect,
illustrated by worse memory performance for “to-be-for-
gotten” items than for “to-be-remembered” ones
(MacLeod, 1999). Regarding PTSD, studies have found a
reduced directed forgetting effect, suggesting that PTSD
could be associated with memory inhibition deficits (Cot-
tencin et al., 2006; Zwissler et al., 2012). Interestingly,
McNally, Metzger, Lasko, Clancy, and Pitman (1998) com-
pared participants with and without PTSD on a directed
forgetting paradigm using positive versus neutral versus
trauma-related words. Contrary to their expectations,
PTSD participants tended to present a directed forgetting
effect only for trauma-related words. However, rather
than reflecting an improved ability to inhibit the encoding
of threatening stimuli, this result was mainly due to an
enhanced recall in PTSD participants for trauma-related
words “to-be-remembered” compared with other types of
words. Furthermore, no differences for recall of trauma-
related words were observed between groups. Considering
these prior findings, results remain unclear regarding
memory control and inhibitory abilities in PTSD.
In sum, the present study aimed to investigate the role
played by inhibitory deficits in the ease to access R recog-
nition during retrieval of threatening information in PTSD.
Our methodology consisted of a novel item-cued directed
forgetting task for emotional words combined with a R/K
recognition procedure. In light of prior studies, we antici-
pated replication of Tapia et al.’s (2012) findings of an
increased production of R recognitions for threatening
words in the “to remember” encoding condition. However,
earlier studies have used negative words regardless of
their traumatic relevance. In the present study, we hypoth-
esised that that effects are not related to a general nega-
tivity bias per se, but mainly to the fact that a significant
portion of the words used could be trauma relevant. In
line with studies suggesting a specific sensitivity in PTSD
towards trauma-related material (e.g., Stanford, Vasterling,
Mathias, Constans, & Houston, 2001), we expected that
the PTSD group would present increased R recognitions
during retrieval of trauma-related words specifically.
Secondly, we wanted to assess the extent to which inhibi-
tory deficits were associated with memory biases. Given
that PTSD patients both presented inhibitory deficits in
the processing of trauma-related information and in pre-
venting the onset of their traumatic memories, we hypoth-
esised decreased ability to succeed in the queries of the “to
forget” encoding condition. Consequently, directed forget-
ting effects should be limited to non-trauma related words
in the PTSD group as a result of an increased production of R
recognitions for trauma-related words “to be forgotten”.
Finally, consistent with Tapia et al.’s (2012) findings, we pre-
dicted K recognitions to be unaffected in PTSD.
Participants
Our sample was composed of 34 individuals diagnosed with
PTSD (25 women and 9 men) and 37 non-PTSD control sub-
jects (25 women and 12 men). Participants in the PTSD
group were treatment-seeking patients of French university
hospitals. PTSD symptoms, as defined by the DSM-IV (APA,
1994), were measured using the Clinician Administered
PTSD Scale (CAPS; Blake et al., 1995). Their control counter-
parts were recruited through university mailing lists. Only
respondents matching patients’ ages, years of education,
and with no traumatic experiences on the Life Events Check-
list (Gray, Litz, Hsu, & Lombardo, 2004) were included. For
both groups, exclusion criteria were: the presence of other
comorbid psychiatric diagnoses (e.g., bipolar disorder, sub-
stance abuse, psychotic-related disorders), a main diagnosis
of Major Depressive Disorder, newly introduced medi-
cations (i.e., <1 month), and/or history of head injury.
PTSD patients were included regardless of the type of
trauma(s) experienced (most occurrences were related to
sexual or physical assaults, relative’s death by suicide, ill-
nesses, or severe injuries). Most of the individuals in the
PTSD group experienced multiple traumatic experiences.
Groups differed significantly on depressive symptoms,
assessed with the Montgomery and Asberg Depression
Rating Scale (MADRS; Montgomery & Åsberg, 1979), disso-
ciative symptoms, assessed with the Dissociative Experi-
ence Scale Taxon (DES-T, Waller, Putnam, & Carlson, 1996),
and anxiety symptoms, assessed with the State Trait
Anxiety Inventory (STAI; Spielberger, 1983). Participants’
characteristics are presented in Table 1. Participation in
the study was voluntary, and all participants gave their
informed written consent. Recruitment and testing pro-
cedures received the approval of the psychiatrists in
charge of our PTSD participants and were in accordance
with ethical guidelines of the declaration of Helsinki.
Measures
The Life Events Checklist is a 17-item scale assessing for
exposure to most commonly encountered traumatic
events. While the first 16 items present most commonly
Table 1. Means and standard deviations of age, yeas of education and
clinical scales’ scores for the two groups.
PTSD Controls
F(1,69)
(n = 34) (n = 37)
M SD M SD
Age (years) 35.24 17.13 34.12 16.36 <1 Educational level (years) 12.80 1.69 12.00 1.89 <1 CAPS total 51.64 15.95 – – – STAI-S 56.20 23.33 26.66 6.85 22.11*** STAI-T 63.20 21.10 36.13 9.86 20.24*** MADRS 18.73 10.66 3.60 6.29 22.40*** DES-T 37.13 41.39 3.44 4.79 9.80**
Note: **p < .01; ***p < .001; M: mean; SD: standard deviation. The Clinician Administered Posttraumatic Stress disorder Scale (CAPS) is from Blake et al. (1995); The State Trait Anxiety Inventory (STAI-S; STAI-T) is from Spiel- berger (1983); The Montgomery and Asberg Depression Rating Scale (MADRS) is from Montgomery and Åsberg (1979); The Dissociative Experi- ence Scale Taxon (DES-T) is from Waller et al. (1996).
1406 A.-C. TUDORACHE ET AL.
experienced events, the last item allows respondents to
add other potential traumatic events not listed before.
Each item is rated on a 4-point scale (1 = happened to me,
2 = witnessed it, 3 = learned about it, and 4 = does not
apply). Gray et al. (2004) reported overall adequate psycho-
metric properties.
The CAPS (Blake et al., 1995) is a largely used structured
interview for PTSD diagnosis and symptoms assessment.
The version used in this study, encompasses, through 17
items, the DSM-IV diagnostic criteria for PTSD. Weathers,
Keane, and Davidson (2001) reported overall adequate psy-
chometric properties.
The MADRS (Montgomery & Åsberg, 1979) is a 10-item
structured interview forassessmentof depressive symptoms
(i.e., apparent sadness, reported sadness, inner tension,
reduced sleep, reduced appetite, concentration difficulties,
lassitude, inability to feel, pessimistic thoughts, suicidal idea-
tions). Symptom severity is rated on a 7-point scale ranging
from 0 to 6. Total score range from 0 to 60 with high scores
indicating elevated anxiety and depressive symptoms and a
cut-off score of 20 as an indicator of probable depression.
Psychometric properties have been reported to be generally
good to excellent (Bondolfi et al., 2010).
The DES-T (Waller et al., 1996) is an 8-item self-admini-
strated measure of pathological dissociation. For each
item, respondents have to rate the frequency of experien-
cing the dissociative state described (from 0% = Never to
100% = Always). The total score is usually obtained by aver-
aging percentages obtained on individual items with high
percentages indicating elevated dissociation. Waller et al.
(1996) estimated adequate reliability.
The STAI (Spielberger, 1983) is composed of two 20-item
self-administrated questionnaires assessing anxiety symp-
toms expressed at the moment (STAI State) and general
anxiety (STAI Trait). Respondents rate their experiences on
4-point Likert scales (STAI State: 1 = no at all, 4 = very
much; STAI Trait: 1 = almost never, 4 = almost always). High
scores indicate elevated anxiety. Barnes, Harp, and Jung
(2002) reported overall good psychometric properties.
Materials
Memory was assessed using 80 French words divided into
positive, neutral, negative and trauma-related according
to French databases (Bonin et al., 2003; Messina, Morais, &
Cantraine, 1989; Vikis-Freibergs, 1976). Since multiple
trauma experiences were expected, trauma-related words
were selected in order to reflect mostly encountered trau-
matic events according the authors’ clinical experiences
with PTSD patients. Additionally, imagery and number of
syllables were controlled using BRULEX lexical data
(Content, Mousty, & Radeau, 1990). The 80 selected words
were divided into two 40-words lists, both composed of
10 positive, 10 neutral, 10 negative and 10 trauma-related
words. The lists were counterbalanced between partici-
pants to serve alternatively as target words for the encoding
task or as distracter words for the recognition task. Each list
was divided into two 20-words sub-lists composed of five
words per emotional valence. These counterbalanced sub-
lists constituted the target words for the “to remember”
and “to forget” encoding conditions associated with the
directed forgetting paradigm. Finally, the recognition task
was operationalised using a random presentation of the
40 studied words and the 40 distracter words.
Procedure
Prior to the study, potential participants were provided
with general information regarding the study aims and
methodology. After giving their written consent, they
were administered the DES, CAPS, MADRS and STAI scales.
The directed forgetting protocol was computerised using
E-Prime 2.0 software (Psychology Software Tools Inc., Schnei-
der, Eschman, & Zuccolotto, 2002). Each memory phase was
preceded by a training trial composed of six unstudied words
for the encoding phase, completed by six unstudied distrac-
tors for the recognition phase. After familiarisation, the test
phase started, preceded by the same instructions. For the
encoding phase, each word appeared for 3 s, followed by a
3 spresentationofthe“toremember”or“toforget” encoding
instructions. The general instructions specified to memorise
the words when they were followed by “to remember” and
to inhibit their memorisation when they were followed by
“to forget”. The four minutes encoding phase was separated
from the recognition phase by a five minutes retention
interval.
After this interval, participants completed the R/K recog-
nition procedure on the 40 studied words and the 40 unstu-
died distracters. Instructions were once again provided both
on the screen and orally. The words were randomly pre-
sented. Participants were asked to press the “yes” key if
they had already seen the word, regardless of the encoding
instructions, and the “no” key if they did not remember
seeing the word. If the “yes” key was pressed, participants
were invited to report the state of consciousness associated
with the recognition by pressing the “A”, “B” or “C” key.
Neutral terminology of “A”, “B” and “C” rather than “R”, “K”
or “Guess (G)” was chosen according McCabe and Geraci’s
(2009) recommendations. Instructions specified that an
“A” answer implies a specific remembering of the word in
which contextual details of its presentation during encod-
ing phase could be recalled (including notably associated
personal memories, images, or inter-item associations),
whereas a “B” answer implies a strict remembering of the
word without retrieval of any contextual details. Finally,
the “C” answer was designed in order to avoid unreliable
“B” responses by assessing uncertainty about the presence
of the word during encoding (Gardiner & Conway, 1999).
Regarding the R/K paradigm, “A”, “B” and “C” responses
respectively represent R, K and G recognitions. In order to
ensure the accurate categorisation, participants were
invited to justify their first three R answers by reporting
the images, thoughts, memories or feelings associated
with the recognised word at the encoding. Conversely, for
MEMORY 1407
the first three K recognitions, participants were invited to
confirm that no such information was elicited by, or associ-
ated with, the word at the time of encoding.
Analyses
Dependent variables were the overall proportion of recog-
nised words (number of recognised words/number of
words per category) and the proportion of recognised
words labelled with a R recognition for each experimental
condition (R responses/number of words per category). In
line with the Independent R/K (IRK) procedure (Yonelinas
& Jacoby, 1995), K recognitions were computed indepen-
dently from R recognitions by dividing the total of K
responses by the number of trials without R responses [K
responses/(number of words per category – R responses)].
Given that G recognitions were only designed for improv-
ing the quality of K responses and that their proportion was
judged to be too low, they were not analysed.
In order to investigate directed forgetting effects,
three 2 (Group: PTSD versus controls) × 2 (Encoding: to
remember versus to forget) × 4 (Valence: positive versus
neutral versus negative versus trauma-related) analyses
of variance (ANOVA) were conducted on the total of
recognised words, R responses, and IRK scores. Addition-
ally, in order to investigate the memory performance and
the memory inhibition abilities of the participants, R
responses and IRK scores were analysed separately by a
2 (Group) × 4 (Valence) ANOVA for each Encoding.
Overall, the Group was considered as a between-groups
factor, whereas the Valence and the Encoding were con-
sidered as within-groups factors. Analyses were con-
ducted using Dell Statistica 12 (Dell Inc., 2015). Given
that high correlations between clinical scales (DES, STAI,
MADRS, CAPS) were found (Pearson’s r ranging from .64
to .77) and there were no significant covariant effects
of the DES, STAI and MADRS scales, covariant analyses
are not reported.
Results
Directed forgetting effects on total recognition
scores
The analyses conducted on total recognition scores by
Group, Valence, and Encoding revealed no significant
Group effect, F(1,69) < 1, indicating that the two groups dis-
played the same recognition pattern. Consistent with the
classical directed forgetting effect, there was a significant
effect of Encoding, F(1,69) = 56.31, p < .001, ηp² = .45, indi-
cating a decreased performance for the items “to-be-for-
gotten” compared with the items “to-be-remembered”.
Moreover, there was a significant interaction between
Group and Encoding, F(1,69) = 12.18, p < .001, ηp² = .15.
Contrast analyses revealed that the difference between
the words “to-be-remembered” and the words “to-be-
forgotten” was reduced in the PTSD group, F(1,69) = 7.73,
p = .007, ηp² = .09, compared to the control group,
F(1,69) = 63,11, p < .001, ηp² = .48, suggesting a reduced
directed forgetting effect in PTSD. No other effect was
significant.
Directed forgetting effects on R responses
The analysis conducted on R responses by Group, Encoding,
and Valence revealed no significant effect of Group,
F(1,69) = 2.19, p = .143, ηp² = .03, suggesting that control
participants and PTSD patients produced similar amounts
of R recognitions. However, there was a significant effect
of the Encoding, F(1,69) = 44.92, p < .001, ηp² = .37, reflect-
ing the classical directed forgetting effect (i.e., more
R responses for the “to-be-remembered” encoding
condition than for the “to-be-forgotten” condition). More-
over, the significant interaction between Encoding and
Group, F(1,69) = 6.21, p = .015, ηp² = .05, revealed a
reduced directed forgetting effect in the PTSD group,
F(1,69) = 12.83, p = .001, ηp² = .28, compared with the
control group, F(1,69) = 33.71, p < .001, ηp² = .48. No signifi-
cant interaction was found between Valence and Group,
F(3,207) = 1.24, p = .29, ηp² = .02, nor between Valence and
Encoding, F(3,207) < 1. There was a significant Valence
effect, F(3,207) = 3.06, p = .029, ηp² = .04, and a significant
interaction between the three variables, F(3,207) = 4.21,
p = .006, ηp² = .06. Contrast analyses revealed that control
participants presented a significant effect of the Encoding
for all emotional valences. More precisely, R recognition
was higher in the “to remember” condition compared
with the “to forget” condition for positive F(1,69) = 14.56,
p < .001, ηp² = .28, neutral F(1,69) = 23.87, p < .001,
ηp² = .43, negative F(1,69) = 28.15, p < .001, ηp² = .44, and
trauma-related words F(1,69) = 6.47, p = .013, ηp² = .28.
However, PTSD patients only presented this directed for-
getting effect for trauma-related words F(1,69) = 18.76,
p < .001, ηp² = .37, while neither positive F(1,69) < 1,
neutral F(1,69) = 3.18, p = .08, ηp² = .08 nor negative words
F(1,69) = 1.39, p = .243, ηp² = .04 reached significance. Find-
ings are presented in Figure 1.
Directed forgetting effects on IRK scores
The analysis conducted on IRK scores by Group, Encoding,
and Valence revealed no significant effect of Group,
F(1,69) = 1.64, p = .20, ηp² = 02, suggesting that PTSD and
control participants produced similar amounts of IRK recog-
nitions. The significant effect of the Encoding reflects the
classical directed forgetting effect, F(1,69) = 10.98, p = .001,
ηp² = .12. Moreover, there was a significant interaction
between Encoding and Group, F(1,69) = 8.62, p = .005,
ηp² = .10. Contrast analyses revealed that only control par-
ticipants presented a directed forgetting effect on IRK
scores F(1,69) = 20.39, p < .001, ηp² = .35, whereas PTSD
patients did not, F(1,69) < 1. No other effect was significant.
Means andstandarddeviationsarepresentedin
.
1408 A.-C. TUDORACHE ET AL.
Memory performance
The analysis conducted on R recognitions for the words
“to-be-remembered” revealed no significant Group effect,
F(1,69) < 1, suggesting that overall the two groups produced
the same amount of R recognitions. Moreover, while no sig-
nificant Valence effect was found, F(3,207) = 1.51, p = .212,
ηp² = .02, there was a significant interaction between
Group and Valence, F(3,207) = 3.71, p = .012, ηp² = .05. Con-
trast analyses revealed that PTSD and control participants
only differed on the recognition of trauma-related words,
with PTSD patients producing significantly more R recog-
nitions than control participants for trauma-related words,
F(1,69) = 5.65, p = .020, ηp² = .07, but not for positive,
neutral, or negative words, all Fs(1,69) < 1.
The analysis of IRK scores for the words “to-be-remem-
bered” revealed a significant Group effect, F(1,69) = 4.69,
p = .034, ηp² = .06, indicating that the control group
produced more K recognitions than the PTSD group. There
was neither Valence effect, F(3,207) < 1, nor interaction
between Group and Valence, F(3,207) = 1.98, p = .119,
ηp² = .03.
Memory inhibition
Analyses conducted on the words “to-be-forgotten” revealed
that PTSD patients produced significantly more R recognitions
for these words than their control counterparts, F(1,69) = 5.95,
p = .017, ηp² = .08. There was no significant Valence effect, F
(3,207) = 2.28, p = .080, ηp² = .03, nor a significant interaction
between Valence and Group, F(3,207) = 1.17, p = .32,
ηp² = .01. Finally, there was no significant effect on IRK scores.
Aiming to assess memory control abilities in PTSD, the
current study was led by the hypothesis that PTSD patients
would demonstrate increased R recognitions for threaten-
ing material as a result from an inability to successfully
inhibit the encoding of trauma-related information.
First, regarding memory functioning, our findings
revealed that, overall, PTSD patients recognised the same
amount of words as healthy controls. While in line with
some prior research (e.g., Tapia et al., 2012; Vrana,
Roodman, & Beckham, 1995), this result otherwise diverges
from other findings (e.g., Golier et al., 2003; Moradi et al.,
2000). Explanations of these discrepancies might emerge
from methodological considerations. Indeed, most
studies having revealed memory impairments in PTSD
used free recall rather than recognition procedures.
Accordingly, present findings are in line with prior
studies emphasising that, in comparison to free recalls,
memory deficits in PTSD may be reduced on cued recalls
or recognition procedures (e.g., Jenkins, Langlais, Delis, &
Cohen, 1998; Zoellner, Sacks, & Foa, 2003). In light of the
inconsistent outcomes regarding this issue (see review by
Tapia, Clarys, El-Hage, et al., 2007), it is difficult to conclude
that memory functioning is unaffected by PTSD. Moreover,
although no overall impairments were reported, it is impor-
tant to note that PTSD patients produced more R recog-
nitions than controls for trauma-related words
specifically. Consistent with our hypothesis, this result
suggests that the enhanced R recognition found by Tapia
et al. (2012) for negative words might reflect the high
trauma-relevance of the negative stimuli used, rather
than a general negativity bias.
Typically, cognitive theories conceived emotional biases
as factors of maintenance for many disorders (e.g., Moradi
et al., 2000). Describing a vicious cycle from negative
emotions to emotional biases, such theories could
account for memory functioning in PTSD. Thus, the high
prevalence of intrusive traumatic memories would favour
processing and notably the encoding of trauma-related
Figure 1. Difference in proportions (and standard error bars) of R responses between the “to remember” and “to forget” conditions (i.e., directed forgetting
effect) by group and emotional valence.
MEMORY 1409
material, which could in turn elicit the memories of trauma.
Considering that only R recognitions were affected,
memory biases in PTSD could be translated by enhanced
associations between trauma-related materials and contex-
tual information. In this view, the constant re-experiencing
of personal traumatic memories and associated features
(e.g., emotions, sensations, images) could have provided
numerous associative cues for trauma-related stimuli, con-
tributing to their improved encoding and increasing the
probability to obtain R responses during recollection.
Additionally, trauma-related stimuli might themselves
trigger personal traumatic memories (e.g., Long, Chamber-
lain, & Vincent, 1994; Williams, Mathews, & MacLeod, 1996).
In line with cognitive models of PTSD (e.g., Ehlers & Clark,
2000), current findings suggest that PTSD patients easily
associate environmental stimuli with their own traumatic
experience, resulting in memory improvements, and poss-
ibly, in return, reinforcing their own traumatic memories.
However, statements of enhanced memory functioning
for trauma-related material in PTSD should be taken care-
fully regarding the non-significant differences between
emotional valences within the PTSD group. Nevertheless,
PTSD patients only presented a directed forgetting effect
for R recognitions of trauma-related words. Supporting
the findings of McNally et al. (1998) and the hypothesis
of biased information processing towards trauma-related
material in the disorder (e.g., Golier et al., 2003; Lin et al.,
2015; Stanford et al., 2001; Zeitlin & McNally, 1991), this
effect conversely challenged the hypothesis of inhibitory
deficits in memory functioning for threatening information.
Nevertheless, overall our data replicate prior findings of
inhibitory impairments in the disorder (e.g., Stein, Kennedy,
& Twamley, 2002; Wu et al., 2010), by revealing an
increased recognition of “to-be-forgotten” words in PTSD
patients when compared to controls. However, while this
effect was, as expected, specific to R responses, PTSD
patients presented a preserved directed forgetting effect
on R recognitions of trauma-related words. As a conse-
quence, contrary to predictions, despite generally impaired
inhibition ability, it appeared that PTSD patients presented
a preserved ability to control their memory functioning for
trauma-related information.
Regarding difficulties encountered by PTSD patients in
preventing the outcome of their traumatic reminiscences,
this effect appears quite counterintuitive. While on the
one hand patients are suffering from involuntary intrusive
memories, which are moreover easily triggered by environ-
mental stimuli (e.g., Ehlers & Clark, 2000), on the other
hand, associative encodings for trauma-related stimuli
can be willingly controlled in experimental settings. In
line with Stanford et al.’s (2001) findings, a possible expla-
nation might emerge from a preferential allocation of cog-
nitive resources towards threatening elements in PTSD. As
a consequence, the processing of non-threatening infor-
mation would face resources limitations. According to
their findings, the trauma saliency of the stimuli is a deter-
mining factor of the cognitive resources re-allocation.
Consequently, in addition to providing a possible expla-
nation for the reduced directed forgetting effect found in
positive and neutral words, these data also offer interpret-
ation clues for the reduced directed forgetting effect for
negative words, despite the anxious and depressive
comorbidities found in the PTSD group.
Interpretations of this preserved directed forgetting
effect in PTSD are limited by non-significant differences
on R recognitions between words’ emotional valences
within the PTSD group in both “to remember” and “to
forget” conditions. However, the significant difference
between the two conditions could reflect PTSD symptoma-
tology, which is characterised by the coexistence of both
intrusive and avoidant symptoms. While intrusive symp-
toms might have favoured R recognitions for trauma-
related words, the avoidant symptomatology, described
as a persistent avoidance of stimuli and thoughts associ-
ated with the traumatic event (DSM-5; APA, 2013), could
have trained patients to easily disengage from trauma-
related information when they were perceived to be irrele-
vant to the task.
Interestingly, the combined role of these processes has
already been pointed out in the Vigilant-Avoidant model of
attention biases (Mogg, Mathews, & Weinman, 1987).
Developed in PTSD for integrating divergences of
findings in the studies exploring attention allocation, this
model suggests that patients could develop either an
attention focus towards threat when attention is measured
in the first steps of processing, or a subsequent attention
distraction away from threat when measures are delayed
(Adenauer et al., 2010; Thomas et al., 2013). Occurring gen-
erally sequentially, the initial focus is usually conceived as
unstoppable as it depends on bottom-up uncontrolled pro-
cesses, whereas the secondary disengagement, which is
more top-down dependent, could be controlled when con-
scious efforts are deployed (Bardeen & Orcutt, 2011). As the
directed forgetting paradigm evaluated voluntary and
control-dependent inhibitory processes, it is possible to
analyse findings in terms of attention allocation. From
this perspective, if in both “to-remember” and “to forget”
conditions attention could have been initially allocated to
trauma-related stimuli, thus contributing to an encoding
ease, the secondary control-dependent disengagement
could have been either blocked in the “to remember” con-
dition or used in order to ease the inhibition of the “to-be-
forgotten” words. Consequently, it is possible that the
inhibitory deficits hypothesis is not necessarily irrelevant
but that such deficits could occur on more uncontrolled
processes, probably in the first steps of information
processing.
Given the limitations of the current study, some points
could be taken into account as far as future studies are con-
cerned. First of all, regarding our sample, although all
patients met criteria for clinical diagnosis of PTSD, they
differed on the traumatic events experienced. Conse-
quently, even if the words labelled as trauma-related
appeared relevant for the most commonly encountered
1410 A.-C. TUDORACHE ET AL.
traumatic events (i.e., interpersonal violence, physical and
sexual abuse), we were not able to ensure that every
trauma-related word was actually relevant for each partici-
pant. Facing this inherent limitation, a clue for future
studies would be to include ratings of the traumatic rel-
evance of the words used. Moreover, it is possible that
negative or even neutral or positive words could also
have constituted reminders of traumatic experiences.
While this constraint seems limited regarding the clear
differences observed between trauma-related and other
type of words, perhaps effect sizes would have benefited
from assessments of the individual trauma relevance of
the processed material. Along with these considerations,
further studies could additionally benefit from contrasting
different types of stimuli. Considering that trauma-related
intrusions notably include images and visual memories
(Brewin et al., 2010; Ehlers & Clark, 2000), it would be inter-
esting to replicate this investigation with pictorial stimuli.
Finally, it would be interesting to include a group of partici-
pants who have been exposed to traumatic events without
developing PTSD. The advantage of such a group would be
to allow for examination of whether the trauma relevance
bias could be attributed to the development of the dis-
order or rather reflective of the familiarity of trauma-
related words.
In conclusion, the aim of the current study was to assess
inhibitory control abilities in memory functioning for
trauma-related information in PTSD. While only few
studies have used the R/K paradigm for memory investi-
gations in PTSD, our findings revealed specifically
increased R recognitions for trauma-related material in
PTSD patients when compared to non-PTSD controls.
Moreover, despite generally impaired memory inhibition
skills, PTSD patients presented a preserved ability to
control and notably to inhibit their memory functioning
for trauma-related material specifically. Consequently, at
this point, rather than the expected impaired control abil-
ities, memory processing of trauma-related material
seemed consistent with theories of cognitive resources
reallocation toward threatening material, at the expense
of other types of information. While unexpected, the pre-
served ability to control memory functioning for threaten-
ing information in PTSD could find some support in a
recent study revealing a generalised improvement in
memory inhibition following trauma exposure in a Think/
No-Think task (Hulbert & Anderson, 2018). While limited
and specific to trauma-related material, the preserved
memory control abilities found in our study suggest that
supporting the reallocation of cognitive resources from
trauma-related to general information might reduce
threat-related biases in PTSD, and by extension could con-
tribute to symptoms reductions.
The authors thank Ashley Smith Watts for English editing of this manu-
script and the International Neuropsychological Society (INS)
International Liaison Committee (ILS) Research Editing and Consulting
Program for their assistance. Additionally, the authors thank the
Poitou-Charentes region and the Collaborative Research Actions
(ARC, 2014) from the universities of Tours and Poitiers for providing
material support.
No potential conflict of interest was reported by the authors.
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Appendix A
Mean proportions (and standard errors) of total recognitions, Remember responses and IRK scores by group, encoding condition and emotional
valence.
Note: * p < .05; ** p < .01; *** p < .001M: mean; SE: standard error. IRK stands for Independent Know responses calculation according the Inde- pendent Remember-Know procedure (Yonelinas & Jacoby, 1995)
1414 A.-C. TUDORACHE ET AL.
APA Style Citation:
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