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Journal of Psychiatric Research 40 (2006) 70–80

PSYCHIATRIC

RESEARCH

Directed forgetting in PTSD: A comparative study versusnormal controls

O. Cottencin a,*, G. Vaiva b, C. Huron c, P. Devos d, F. Ducrocq a, R. Jouvent c,M. Goudemand a, P. Thomas e

a Department of Psychiatry, FONTAN Hospital, University of Lille II, School of Medicine, Rue Verhaeghe, 59037 Lille Cedex, Franceb INSERM U513 Neurobiologie et Psychiatrie Faculte de Medecine, 8, rue du General Sarrail 94010 Creteil Cedex, France

c University of Paris VI, School of Medicine, Franced Department of Statistics, University of Lille II, School of Medicine, France

e Lab. Neurosciences Fonctionnelles & Pathologies CNRS FRE 2726 CHRU Lille, University Lille 2, 59037 Lille Cedex, France

Received 14 July 2004; revised 16 March 2005; accepted 5 April 2005

Abstract

The most characteristic feature of Post-Traumatic Stress Disorder (PTSD) is the reexperiencing syndrome. The patient�s memoryseems to be fixed on the traumatic event, which may be due to disturbance of the autobiographic memory. To retrieve memories,others have to be inhibited. These inhibition mechanisms have been studied using the Directed Forgetting Paradigm, which mea-sures the capacity to forget recently processed information and to retain the relevant information.

Our hypothesis is that during PTSD, the memory is saturated with traumatic memories, so that the patients are no longer able touse the inhibitory processes. Therefore, during a Directed Forgetting Task (DFT) in which words ‘‘to remember’’ and words ‘‘toforget’’ are given, PTSD patients cannot inhibit the words ‘‘to forget’’, and so recall more words than the controls.

We studied 30 patients with PTSD and compared them with 30 healthy controls, using DFT. The results show that the patientsremembered significantly fewer words overall, and fewer of the words ‘‘to remember’’ than the controls, both for immediate andfinal recall.

Our results are in favor of a reduction in directed forgetting in patients suffering from PTSD, resulting in difficulty in inhibitingirrelevant information from the overall information. There seems to be a deficit in the inhibitory processes in the memory in PTSD.� 2005 Elsevier Ltd. All rights reserved.

Keywords: Directed forgetting; Autobiographical memory; PTSD

1. Introduction

One of the characteristic clinical features of Post-Traumatic Stress Disorder (PTSD) is the reexperiencingsyndrome (APA, 1994). The patient continuously relivesthe initial event which caused the disorder. The reexpe-riencing can take different forms (nightmares, hallucina-tions of the traumatic event, intrusive memories of thetrauma, emotional crises from reexperiencing, etc.).

0022-3956/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jpsychires.2005.04.001

* Corresponding author. Tel.: + 33 3 20 44 45 84; fax: + 33 3 20 44 6265.

E-mail address: ocottencin@chru-lille.fr (O. Cottencin).

These psychopathological manifestations are due to adisturbance in the autobiographical memory (McNallyet al., 1995). The patient�s psychological function seemsto be fixed on the traumatic event, causing difficulty inthinking about the future (McNally, 1997a). The mem-ory of the trauma may range from total amnesia, toreexperiencing it day and night with a very painful feel-ing, which even affects the autonomic nervous system(McNally, 1997b). We noted that these patients havejust as many memory deficits for the traumatic event it-self, as for other information, apparently unconnectedwith the trauma (McNally, 2003).

O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80 71

The memory disturbance found in patients withPTSD was particularly deficits in Wechsler�s memoryscale (immediate and final recall, visual memory andverbal memory) (Bremner et al., 1993). Later on, manyauthors studied different aspects of the memory distur-bance in these patients, noting that there was sometimesa mixture of past and present experiences (Yehuda et al.,1995), or a deficit in the explicit memory (Jenkins et al.,1998). Regarding the organization of the memory inpsychologically traumatized patients, Vasterling et al.(1998) found a deficit in the inhibition of imprecise re-sponses and filtering of irrelevant information in PTSDpatients. Therefore, PTSD patients responded to moredistractions than controls, which suggest that they havemore difficulty in inhibiting irrelevant information froma task.

This dysfunction in inhibiting irrelevant informationwas noted by Brewin et al. (1996), who put forward amemory function model having two modes.

� There may be a verbally accessible memory (VAM),which would allow a memory to be deliberatelyretrieved from a store of autobiographical experi-ences (Conway, 1997).

� Information provided by a traumatic event may alsotake another form or a group of forms, which are notdeliberately accessible: the situational accessiblememory (SAM). Its representations are accessibleautomatically, in particular when the patient is in asituation with similar characteristics, or a similarmeaning to the traumatic event (intrusive ideas fromthe trauma, similar scenes seen on the television forexample).

Starting with this two-mode memory retrieval theory,Brewin and Andrews (1998) investigated the linkbetween forgetting of traumatic events and the inhibi-tory processes. They looked again at the studies per-formed on the different inhibition processes in dailycognitive function (repression, dissociation, simple for-getting and creation of false memories). By adaptingthe Directed Forgetting Paradigm (Bjork, 1989) foremotional material (Myers et al., 1998), they observeda greater tendency to forget words with a negative con-notation, that those with a positive connotation. Therewere therefore psychotraumatized individuals, whohad difficulty with the process dealing with informationwith a negative connotation, although it was not knownwhich mechanisms were involved. It would be useful torepeat this study with words with a neutral emotionalvalue.

Directed forgetting task was initially used to investi-gate whether PTSD patients exhibit an avoidant encod-ing style and impaired memory for trauma cues(McNally et al., 1998). But, current research of post-trauma sequelae suggests that intrusive rather than

avoidant-dissociative models more accurately representthe encoding processes of the trauma cues involvingthe role of dissociation in impairing encoding (Zoellneret al., 2003). However, studies to elucidate information-processing abnormalities in people with PTSD shownthat individuals with PTSD exhibit difficulty forgettingtrauma words during directed forgetting; and exhibitproblems retrieving specific autobiographical memoriesin response to cue words, instead recalling ‘‘overgen-eral’’ memories (McNally, 1998).

To remember new information, it is necessary to beable to distinguish it from older information, but alsoto stop old information interfering with new (Conway,1997). Bjork (1989) considered that mechanisms existed,when necessary, to make some information becomemore important, with respect to the rest of the informa-tion in the memory. He studied these mechanisms usingthe Directed Forgetting Paradigm, in order to examinethe capacity to forget recently processed information,and the capacity to retain relevant information. A seriesof stimuli were presented, which, according to theinstructions given, some were to be remembered andothers to be forgotten. The patient was then asked to re-call as many of the items to be remembered as possible,then to remember all the items, both those ‘‘to remem-ber’’ and those ‘‘to forget’’.

Brewin therefore contributed to the understanding ofthe memory processes of psychotraumatized patients byhis theory, which fits in perfectly with the clinical pictureof the traumatic reexperiencing syndrome, the experi-ences coming from the patient�s conscious mind, withouthis knowing it. Controlled memories are painful andcause well-known avoidance behavior patterns, butuncontrolled memories envelop the patient in the mostemotional and physiological aspects of the trauma.

Our hypothesis is that the cognitive memory inhibi-tion processes are faulty in patients with PTSD, and thatwhen a Directed Forgetting Task is performed, a patientwith PTSD cannot inhibit the words ‘‘to forget’’ andremembers more of them than the healthy controls,whereas a healthy person gives more of the words ‘‘toremember’’ than the words ‘‘to forget’’.

We studied the memory inhibition processes bymeans of the Directed Forgetting Task in patients suffer-ing with PTSD, using neutral words devoid of any emo-tional value, without a positive or negative connotation,and comparing them with healthy controls.

2. Materiel and methods

2.1. Subjects

The study was performed on consecutive patientsexamined at the Psychiatric Consultation of the Univer-sity Hospital Center of Lille (France), and was approved

72 O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80

by the Ethical Committee (decision number CP 98/89).The patients gave their informed consent to participatein the study.

2.1.1. Patients with PTSD

All of the patients who presented with PTSD, accord-ing to the DSM-IV criteria (APA, 1994), which had beendeveloping for more than 6 months and who acceptedthe principle of the protocol, were included in the study.The patients were not selected with respect to the type oftrauma, and we kept them in the order that they arrivedat the consultation.

Using the MINI-DSM-IV Check list, we excluded pa-tients with cerebral lesions, those with known memorydisorders before the trauma, those treated with benzodi-azepines before the trauma and up to one month beforethe tests, those diagnosed as being drug or alcohol ad-dicts, and those who had consumed cannabis resinderivatives at least 6 months before testing (Lecrubieret al., 1997).

The patients were allowed to continue psychotropictreatment other than benzodiazepines, providing thatit was being taken before the study. During the study,no changes in psychotropic drugs were permitted.

2.1.2. Controls

We compared the patients with 30 controls, compara-ble for age, sex and socio-cultural level. They were re-cruited in the environment of the patients and theinvestigators. None of them had suffered any psycholog-ical trauma, none had past or present PTSD, or anyother psychiatric disorders (MINI-DSM-IV Check list)(Lecrubier et al., 1997). None of them were addictedto any toxic substances, none had any past or presentpsychiatric disorder and none had been treated with apsychotropic drug for at least one month before thestudy.

2.2. Evaluation instruments

The diagnosis of Post-Traumatic Stress Disorder wasmade according to the criteria of DSM-IV (APA, 1994).The patients benefited from a general psychopathologi-cal evaluation, using the Minimal International Neuro-psychiatric Interview for DSM-IV, to show up anypossible comorbidity (Lecrubier et al., 1997).

The Clinical Administered for PTSD Scale (Blakeet al., 1990) was used to evaluate the PTSD symptom-atology and the Impact of Event Scale, to evaluate theeffects of the disorder on the patients (Horowitz et al.,1979; Hansenne et al., 1993, French Translation).

The psychological evaluation included the VerbalFluency Test (1 min; three semantic and three phonolog-ical categories), the Stroop Task (Stroop, 1935) and anevaluation of the Intelligence Quota using an abridgedversion of Wechsler�s Revised Intelligence Scale for

Adults (Wechsler, 1980; Britton and Savage, 1989),including four subtests (Crawford et al., 1992). The totalmemory performances were evaluated using the revisedversion of Wechsler�s Memory Scale (Wechsler, 1984).

Neuropsychological evaluation of the memory wasperformed using an adapted version of the Long-termDirected Forgetting Task by Zacks et al. (1996). Fourlists of 24 words were successively shown to the patients.The 24 words of each list belonged to 6 different seman-tic categories. Each word was shown on a card for 5 s.On the next card, the instruction: ‘‘REMEMBER’’ or‘‘FORGET’’ was shown for 2 s. Each list included 12words ‘‘to remember’’ and 12 words ‘‘to forget’’. Theinstruction was shown after the word had been shown,so that the patients did not know in advance whichwords were to be remembered and which were to be for-gotten. For the four words belonging to the samesemantic category, the instruction ‘‘to remember’’ wasrandomly attributed from a list of numbers, to 0, 1 or2 words. The instruction ‘‘to forget’’ was attributed tothe rest. The categories and their corresponding wordswere chosen from commonly known French literature,taking care to choose ‘‘neutral’’ categories and words,that is without any direct relationship with traumaticevents (e.g., incest, rape, accidents, automobiles, etc.).The words were chosen according to how often they ap-peared in written French, using the BRULEX database(Content et al., 1990), so that the categories were homo-geneous for their frequency in the literature (between100 and 10,000). Homophonic words were excluded.Variance Analysis (ANOVA) was performed to find adifference between the four lists for the frequency ofappearance of the words in the literature. This analysisdid not show any significant difference between the listsfor the frequency of the words (F = 0.11; p = 0.95).

The order of showing the lists, the categories and thewords was made by drawing lots, first for the lists, thenfor the categories and finally for the words within eachcategory. This initial order was maintained for all ofthe patients.

The performances of the patients were measured foreach phase, by the total number of words remembered,the total number of words ‘‘to remember’’ and ‘‘to for-get’’, the number of words ‘‘to remember’’, the numberof words ‘‘to forget’’, the number of repetitions andintrusions (words not in the lists, but recalled by the par-ticipants). The results refer to the mean recall over eachof the four trials for the immediate conditional recall.

2.2.1. Procedure

The psychological tests were performed by the sametwo trained psychologists (G. de F.; R.B.). The othertests were performed by the main investigator (O.C.).The order of performing the tests and the clinical evalu-ations over three visits was: (1) meeting the main inves-tigator (O.C.) who performs diagnostic evaluation

O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80 73

(DSM-IV), clinical evaluation for PTSD (CAPS andIES), explanation of the protocol and its use, and givingthe patient an information letter; (2) (the next day) sign-ing the information letter. Performing the Directed For-getting Test, Stroop�s task and the verbal fluency test(O.C.); (3) (at 48 h) performing WAIS-R (four items)and WMS (G. de F., R.B.). The inter-rater reliabilityfor PTSD diagnosis was not measured.

DFT. After being shown each of the four lists, the pa-tients had to remember as many as possible of the words‘‘to remember’’ shown to them, over a time limited to 2min: immediate conditional recall phase. After the fourlists were shown, the patients were asked for some bio-graphical information for 10 min. After this phase, theywere asked to remember all of the words from the fourlists, both those that they should have remembered andthose they should have forgotten, over a time limited to5 min: final unconditional recall phase.

2.3. Statistical analyses

Analyses were performed using SAS (V8.0, SAS Insti-tute) software. Descriptive univariate analysis of thedata was performed using the mean values (M) andthe standard deviations (SD) for the interval data. Com-parison of the mean values was made using parametrictests, assuming a normal distribution. Comparisons be-tween the mean values for the PTSD patients and thecontrols were performed using the Wilcoxon tests forthe Directed Forgetting Task, and for each of the othertests (verbal fluency, Stroop task, WAIS-R and WMS).

For the correlation analyses, we calculated the coeffi-cient for Spearman�s correlation. In the PTSD patientgroup, we compared the clinical scales (IES and CAPS),the psychometric tests (WAIS-R and WMS) and theDirected Forgetting Task. Then for each group, wecompared the Directed Forgetting Task and the psycho-metric tests.

3. Results

We studied a population of 30 patients (20 womenand 10 men), who had been victims of psychologicaltrauma, which had caused a PTSD, according to the cri-teria of DSM-IV (APA, 1994), that had been developingfor a mean of 59.03 months (SD 101.44), and which hadoccurred either in a group or individually (Table 1).They were aged between 20 and 61 years old, their meanage being 37.2 years old (SD 12.43).

Eighteen patients were taking antidepressants, sevenwere taking nonbenzodiazepine anxiolytics, and 25 ben-efited from psychotherapy. Wilcoxon�s test showed thatthe two groups did not differ significantly for age(p = 0.89) or for their socio-cultural group (p = 0.37).

3.1. Directed forgetting task

The results obtained by the patients with PTSD andthe healthy controls are shown in Figs. 1 and 2.

3.1.1. Immediate conditional recallFor the number of words remembered (mean recall

over each of the four trials), the patients recalled signif-icantly fewer words overall than the controls [M = 7.89(SD 1.65); M = 9.55 (SD 1.64) (p = 0.0011)] and signif-icantly fewer words ‘‘to remember’’ and ‘‘to forget’’ thanthe controls [M = 7.58 (SD 1.59); M = 9.44 (SD 1.66)(p = 0.0002)]. The patients [M = 5.70 (SD 1.73); M =1.87 (SD 1.10) (p > 0.001)] and the controls [M = 8.71(SD 1.17); M = 0.72 (SD 0.45) (p < 0.001)] rememberedsignificantly more items ‘‘to remember’’ than items ‘‘toforget’’.

The patients with PTSD recalled significantly feweritems ‘‘to remember’’ than the healthy controls [M =5.70 (SD 2.15); M = 8.71 (SD 2.12) (p < 0.0001)] butmore items ‘‘to forget’’ [M = 1.87 (SD 1.47); M = 0.72(SD 0.90) (p < 0.0001)].

3.1.2. Final unconditional recall

The PTSD patients recalled a significantly lower totalnumber of words [M = 32.76 (SD 10.06); M = 43.96(SD 11.64) (p = 0.0006)], ‘‘to remember’’ and ‘‘to for-get’’ [M = 29.76 (SD 8.80); M = 42 (SD 11.21)(p < 0.0001)] than the controls. The patients[M = 16.16 (SD 5.30); M = 13.6 (SD 4.25) (p = 0.001)]and the controls [M = 27.66 (SD 6.82); M = 14.26 (SD5.11) (p < 0.001)] recalled significantly more items ‘‘toremember’’ than items ‘‘to forget’’.

Finally, we noted that the patients recalled signifi-cantly fewer words ‘‘to remember’’ than the controls[M = 16.16 (SD 5.30); M = 27.66 (SD 6.82)(p > 0.0001)]. The difference between the recall of items‘‘to remember’’ and ‘‘to forget’’ was significantly smallerin the PTSD patients than in the controls. In otherwords, the patients remembered proportionally moreitems ‘‘to forget’’ than the controls.

Otherwise, we did not note any list-specific effect,either for conditional recall or for unconditional recall,which indicates that the patients and the controls didnot give more words from any one of the four lists. Inthe two groups, the number of repeated words andintrusive words was very small. Comparison of the meannumbers of repeated words and intrusive words did notshow any significant difference between the patients andthe controls.

3.2. Results of the complementary tests

The patients and the controls did not have signifi-cantly different Intelligence Quotas. However, the re-sults for the WMS scale showed significantly worse

Immediate Conditional Recall

0

2

4

6

8

10

12

TO BE REMEMBERED TO BE FORGOTTEN

type of item

nb

of

item

s re

calle

d

PTSD

CONTROLS

*

*

Fig. 1. Items recalled by PTSD and controls during the immediateconditional recalls. *:significant difference.

Final Unconditional Recall

0

5

10

15

20

25

30

35

40

TO BE REMEMBERED TO BE FORGOTTENtype of item

nb

of

item

rec

alle

d

PTSD

CONTROLS*

Fig. 2. Items recalled by PTSD and controls during the finalunconditional recall. *:significant difference.

Table 1Description of PTSD and controls

Patients Controls

No. Sex Age Traumatic event D CAPS ANX ATD PsyTh SCL Age Sex SCL

1 F 59 Physical attack 120 84 0 0 1 11 53 F 112 F 53 Physical attack 8 111 1 1 1 17 49 F 153 F 35 Physical attack 12 113 0 1 1 15 34 F 154 M 40 Electrocution 48 94 0 1 1 11 43 M 115 M 25 Child abuse 180 92 1 0 0 11 25 M 116 F 27 Sexual assault 24 94 0 1 1 15 29 F 187 F 31 Sexual assault 180 93 1 0 0 11 30 F 118 F 20 Sexual assault 24 103 0 0 1 11 21 F 119 F 30 Traumatic bereavement 14 65 0 0 0 11 34 F 1110 M 48 Physical attack 12 75 0 1 1 9 53 M 911 F 25 Bomb attack 24 86 0 0 1 15 24 F 1412 M 30 Motor vehicle accident 60 119 0 1 1 11 33 M 1113 F 29 Sexual assault 24 88 0 1 1 15 27 F 1714 M 60 Physical attack 13 111 1 1 1 14 60 M 1415 F 45 Child sexual abuse 420 106 0 0 1 15 45 F 1516 M 39 Traumatic bereavement 8 96 1 1 1 12 38 M 1817 F 30 Physical attack 6 99 0 0 1 17 30 F 1818 F 60 Drowning 12 80 0 0 1 11 63 F 1119 M 32 Physical attack 24 92 0 0 0 12 33 M 1820 F 45 Traumatic bereavement 12 108 1 1 1 11 43 F 1421 F 45 Physical attack 9 108 1 0 1 16 46 F 1222 F 29 Physical attack 8 107 0 1 1 12 29 F 1823 M 61 Physical attack 60 102 0 1 1 9 62 M 924 M 42 Physical attack 12 94 0 0 1 15 41 M 1825 F 30 Automobile accident 7 124 0 1 1 19 30 F 1726 F 21 Automobile accident 6 101 0 1 1 15 22 F 1527 F 21 Sexual assault 12 119 0 1 1 11 20 F 1428 M 25 Automobile accident 12 85 0 1 0 15 25 M 1429 F 40 Automobile accident 60 103 0 1 1 15 39 F 1230 F 40 Child sexual abuse 360 88 0 0 1 9 40 F 12

M 37.2 59.03 98 13.03 37.37 13.8SD 12.43 101.44 13.13 2.65 12.29 2.94

D: Duration of illness (months); CAPS: Clinical Administered for PTSD Scale; ANX: non-benzodiazepine anxiolytic; ATD: SSRI Antidepressant;PsyTh: Psychotherapy, SCL: socio-cultural level (number of years of studies).

74 O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80

O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80 75

scores for the patients, except for the attention-concen-tration index (Table 2).

Similarly, the results for verbal fluency showed thatthe patients recalled significantly fewer words than thecontrols in all of the categories (Table 3).

The results of the Stroop test did not show any signif-icant difference between the patients and the controls(Table 4).

3.3. Correlations analyses

In the PTSD patient group, we did not find any cor-relation between the clinical scales (IES and CAPS) andthe psychometric tests (WAIS-R and WMS). Similarly,we did not find any correlation between the same clinicalscales and the Directed Forgetting Task. We also didnot find any significant correlation between the Directed

Table 2Results of the complementary tests

PTSD n = 30

M SD

WAIS-R

Verbal IQ 111.87 20.571Performance IQ 99.967 21.272Total IQ 106.87 20.304

Wechsler Memory Scale

General memory 91.3 18.561Verbal memory 103.93 20.055Visual memory 98.967 16.431Attention-concentration 90.267 16.032Differed recall 101.1 19.144

Table 3Results of the verbal fluency test

Verbal fluency PTSD n = 30

M SD

Words beginning by P

Total recall 17.5 5.2243Corrects words recall 17.267 4.9406

Words beginning by R

Total recall 15.867 5.211Corrects words recall 15.567 5.2238

Words beginning by V

Total recall 15.767 5.3219Corrects words recall 15.567 5.2567

Animals

Total recall 23.133 7.3893Corrects words recall 23.033 7.2611

Fruits

Total recall 16.767 3.8118Corrects words recall 16.567 3.6642

Furniture

Total recall 12.467 3.3294Corrects words recall 11.8 2.8696

Forgetting Task and the psychometric scales (WAIS-Rand WMS), with the Intelligence Quota. However, inboth the patients and the controls, we only found signif-icant correlations with a limited number of items inWMS (Tables 5 and 6).

4. Discussion

Our study included 30 patients suffering from PTSDwithout any other comorbidity, and compared themwith 30 healthy controls. PTSD had been developingfor a mean of 59.03 months (SD 101.44) and had aCAPS score of 98 (SD 13.13).

The results obtained with the Directed ForgettingTask, showed that the patients remembered fewer words‘‘to remember’’ than the controls for immediate conditional

Controls n = 30 Wilcoxon p

M SD

118.17 22.822 0.3036105.1 18.847 0.1598114.63 21.344 0.1980

101.77 23.254 0.0156117.6 12.317 0.0013110.57 13.95 0.0041100.7 17.197 0.1254113.97 14.85 0.0086

Controls n = 30 Wilcoxon p

M SD

23.967 5.1694 <0.000123.6 5.13 <0.0001

21.333 4.744 0.000220.933 4.7265 0.0003

19.967 5.0752 0.003019.5 5.0086 0.0047

29.8 6.008 <0.000129.433 5.9867 <0.0001

20.7 3.2393 <0.000120.433 3.3701 <0.0001

14.333 3.155 0.016013.8 2.8575 0.0077

Table 4Results of the Stroop test

Stroop test PTSD n = 30 Controls n = 30 Wilcoxon p

M SD M SD

Denomination

Time (s) 62.133 12.495 65.2 23.247 0.9705Number of errors 0.7667 1.0063 0.9333 1.2576 0.8530Number of corrected errors 0.7667 1.0063 0.8 1.0954 0.9548Number of non-corrected errors 0 0 0.1333 0.3457 0.0418

Lecture

Time (s) 46.533 7.4173 49.833 14.702 0.6621Number of errors 0.0667 0.2537 0.2 0.5509 0.3708Number of corrected errors 0.0667 0.2537 0.2 0.5509 0.3708Number of non-corrected errors 0 0 0 0 1

Interference

Time (s) 111.97 21.669 126.3 40.99 0.1410Number of errors 2.3333 2.2024 2.9333 4.6678 0.5363Number of corrected errors 1.7 1.3684 2.1 2.8205 0.7104Number of non-corrected errors 0.6333 1.2726 0.8333 2.0858 1

Differences of times and errors

Time interference – time lecture 49.833 18.193 61.1 35.418 0.0645Time interference – time denomination 65.433 21.048 76.467 37.842 0.1452Errors interference – errors lecture 1.5667 2.445 2 4.2345 0.8628Errors interference – errors denomination 2.2667 2.1324 2.7333 4.6382 0.4479Corrected errors interference – corrected errors lecture 0.9333 1.5742 1.3 2.6281 0.9161Corrected errors interference – corrected errors denomination 1.6333 1.2994 1.9 2.8082 0.5503Non-corrected errors interference – non-corrected errors lecture 0.6333 1.2726 0.7 2.0536 0.7556Non-corrected errors interference – non-corrected errors denomination 0.6333 1.2726 0.8333 2.0858 1

Table 5Correlations DFT and WMS in PTSD

PTSD Verbal memory Visual memory General memory Attention-concentration Differed recall

Immediate Total r 0.41a 0.22 0.27 0.26 0.22Conditional TBR r 0.60a 0.28 0.49a 0.43a 0.53a

Recall TBF r �0.32 �0.13 �0.29 �0.28 �0.42a

Final Total r 0.51a 0.13 0.29 0.08 0.30Unconditional TBR r 0.50a 0.21 0.25 0.26 0.41a

Recall TBF r 0.45a 0.13 0.24 �0.02 0.22

a Significant results (p < 0.05).

Table 6Correlations DFT and WMS in controls

Controls Verbal memory Visual memory General memory Attention-concentration Differed recall

Immediate Total r 0.42a 0.17 0.62a 0.21 0.66a

Conditional TBR r 0.45a 0.16 0.68a 0.32 0.69a

Recall TBF r �0.01 �0.02 �0.19 �0.35 �0.14

Final Total r 0.34 �0.10 0.31 �0.07 0.30Unconditional TBR r 0.33 �0.07 0.36a �0.04 0.38a

Recall TBF r 0.38a �0.11 0.26 �0.06 0.23

a Significant results (p<0.05).

76 O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80

recall and for final unconditional recall. We also notedthat the number of correct words (‘‘to remember’’ and‘‘to forget’’) recalled by the patients in the final recall task,was smaller than for the controls. These results arecompatible with the data in the literature, which found

an explicit memory deficit in patients suffering fromPost-Traumatic Stress (Jenkins et al., 1998).

During the immediate recall task, whose instructionswere to recall the words ‘‘to remember’’, the patientsrecalled more words ‘‘to forget’’ than the controls.

O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80 77

Similarly, in the final recall task, we noted that the differ-ence between the recall of words ‘‘to remember’’ andwords ‘‘to forget’’ was less for the patients. There wastherefore a relative (but not absolute) increase in the recallof the words ‘‘to forget’’ compared with the words ‘‘toremember’’, in the patients compared with the controls.In the patients, the number of items ‘‘to remember’’ wasalmost the same as the number of items ‘‘to forget’’.

To be successful at a directed forgetting task, the fol-lowing trends are seen:

1. The presence of ‘‘to forget’’ items on a list does notreduce recall or recognition of ‘‘to remember’’ items.

2. they are few intrusions of ‘‘to forget’’ items when par-ticipants are asked – in the immediate recall – toreport only ‘‘to remember’’ items.

3. and performance on ‘‘to forget’’ items is relativelypoor when – in the final recall – they are asked torecall all of the words (‘‘to remember’’ and ‘‘to for-get’’) (Zacks et al., 1996).

We note that in this study, the patients with PTSD had areduced directed forgetting effect compared with thehealthy controls. We suggest that this reduction maybe secondary to a difficulty in inhibiting the items ‘‘toforget’’, which may mean that PTSD patients have adeficit in the inhibitory processes, in other words theyhave difficulty in inhibiting information which is irrele-vant to the overall information.

The situation of the immediate recall test should cre-ate a particularly sensitive task environment for demon-strating some of the predicted differences between thetwo populations. It should be more difficult to suppressthe items ‘‘to forget’’ from a category when others itemsfrom the same category have to be remembered (Zackset al., 1996). In the final recall test, both patients andcontrols were expected to show greater retention ofitems ‘‘to remember’’ than items ‘‘to forget’’. The re-duced ability of the patients to inhibit processing ofthe items ‘‘to forget’’ at encoding should result in smal-ler ‘‘to remember’’-‘‘to forget’’ differences for this group.In other words, PTSD patients were expected to showbetter long-term retention of items ‘‘to forget’’ than con-trols (Zacks et al., 1996).

Zacks et al. (1996) proposed several processes used ina Directed Forgetting Task, some of which have aninhibitory function. During encoding, the individualshould stop remembering the items ‘‘to forget’’, inaccordance with the instructions given, and should sep-arate the items memorized. During memory retrieval,mechanisms have to be used to impede the recall of irrel-evant words. These authors suspect that the attentioninhibitory processes control access and temporary stor-age of irrelevant information in the working memory.A disorder of inhibition would be manifested by thepresence of distracting information, which could inter-

fere with performing the task being done, and couldoverload the working memory. Irrelevant information(environmental details, personal memories or interests,or interpretations inadapted to the context) would haveaccess to the working memory and have an abnormallystrong activation. The association in the memory of rel-evant and irrelevant information (because of their prox-imity in time) would therefore cause competition duringmemory retrieval. This inhibition disorder also encour-ages poor quality initial encoding, and competition be-tween associated information (Zacks et al., 1996).

This hypothesis takes the clinical situation of patientswith PTSD into account. The memory is saturated withspontaneous and voluntary traumatic memories (Brewinet al., 1996), which largely disrupt the weighting given toinformation within the working memory. However, thisis not directly tested. The irrelevant traumatic informa-tion is activated abnormally strongly. The defective (oroverloaded) attention inhibition mechanisms wouldtherefore let traumatic information enter into competi-tion with relevant information, when it is recalled. Evi-dence from neuroimaging studies has suggested areasof the brain that may be damaged by psychologicaltrauma: structural findings as hippocamal volume reduc-tion (which may limit the proper evaluation and catego-rization of experience), functional changes as increasedactivation of the amygdala after symptom provocation(which may reflect its role in emotional memory) and de-creased activity of Broca�s area at the same time (whichmay explain the difficulty PTSD patients have in label-ing their experience) (Hull, 2002).

The profile of their response to the Directed Forget-ting Task fits in with this: since they have difficulty inprocessing the relevance of information, during condi-tional recall, they cannot recall correctly the instructionsgiven of what they should forget. Two associated piecesof information then enter into competition, during finalunconditional recall, and the patients remember almostas many words ‘‘to forget’’ as words ‘‘to remember’’.However, we have to notice the absence of PTSD-re-lated differences in intrusive errors in our study. Thisfact might impact our theory. Is it linked with the choicewe made of neutral words in this particular DirectedForgetting Task?

A hypothesis could be made by which there is a defectin marking items ‘‘to forget’’ or ‘‘to remember’’, duringencoding. However, this does not agree with the resultsof immediate recall in the Directed Forgetting Task inPTSD patients. In fact, during conditional recall, thePTSD patients recalled more items ‘‘to remember’’ thanitems ‘‘to forget’’, which tends to show that the itemswere well associated with the words that were shownto them.

The hypothesis that there may be an error in sourcemonitoring, that is confusion between the two types ofwords (‘‘to remember’’ and ‘‘forget’’), should also be

78 O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80

excluded. During the conditional recall task (recall ofthe words ‘‘to remember’’), the patients responded tothe instructions given to them, by recalling many morewords ‘‘to remember’’. That therefore shows that theywere well able to distinguish between the two types ofitems (relevance), but that it was at the memory recallstage that inhibition failed, and so through a lack ofinhibition, they recalled more words ‘‘to forget’’.

In this way, the patients, being unable to inhibit irrel-evant information, they were unable to inhibit the reac-tivation of the words ‘‘to forget’’, which were thenprocessed as words ‘‘to remember’’. They encoded theinformation correctly, but because of their inhibitiondeficit, they were no longer able to attribute the correctweighting to the information, at the time of recall.

One question which cannot be answered is whetherthe inhibition defect occurs at the time of encoding orat the time of memory retrieval. From a theoreticalpoint of view, Basden and Basden (1996) suggested thatthe directed forgetting phenomena could be explainedby inhibitory mechanisms acting mainly on encoding.The individual would then separate the two types ofitems into two groups, each being dealt with in a differ-ent way: the items ‘‘to remember’’ would be recapitu-lated and the items ‘‘to forget’’ would be seen as ifthey no longer existed, and so would be inhibited. Theyshowed that the mechanisms involved depend on themethodology used. In the studies in which the instruc-tions ‘‘to remember’’ and ‘‘to forget’’ were given imme-diately after presentation of each word (wordprocedure), the directed forgetting effect was obtainedboth in free recall and in word recognition, whereas inthe studies in which the same instructions were givenafter a series of items (list procedure), the directed for-getting effect was obtained in free recall but not in wordrecognition. Therefore, according to these authors, theresults observed in the list procedure are compatiblewith the hypothesis of inhibition of the items ‘‘to forget’’during memory retrieval, whereas the results obtained inthe word procedure are more compatible with thehypothesis of differentiation of the items ‘‘to remember’’and ‘‘to forget’’ during encoding. To reconcile theseideas, Zacks et al. (1996) suggested that there are inhib-itory mechanisms at the time of encoding and at mem-ory retrieval, and that the respective weight of theinhibitory mechanisms depend on the methodologyused. In any case, in our study we used a word proce-dure, and we noted an absence of forgetting in the pa-tients and directed forgetting in the controls in the twophases (immediate and final recall), so we can neitherconclude that there is an inhibition defect at the timeof encoding or at memory retrieval. Although the failureto find a significant effect in the Stroop task arguesagainst an inhibitory deficit of the patient group.

We chose to set up this test using neutral words, withreference to the study by McNally et al. (1998), who

studied the Directed Forgetting Task in women whowere victims of sexual abuse in childhood, with or with-out PTSD, and compared them with controls. Theirhypothesis was that there was ‘‘avoidance encoding’’of the traumatic information. They showed the partici-pants traumatic words (‘‘incest’’), positive words (‘‘cele-brate’’) and neutral words (‘‘mailbox’’). They found adirected forgetting effect for traumatic words in thePTSD sufferers, but a reduction in the directed forget-ting effect for neutral and positive words. Their othertwo groups had a directed forgetting effect for all typesof words. This agrees with our results with respect toneutral words.

However, the directed forgetting effect observed withtraumatic words shows that the deficit in the inhibitorymechanisms depends on the emotional value of thewords. These words would then be given a particular rel-evance, not given to neutral words. This point is com-pletely in agreement with the importance of theweighting given to information in a PTSD patient�smemory, which seems to be linked to the traumaticevent (McNally, 1997a).

The choice of our PTSD patients was not without sig-nificance. We chose a population with ‘‘pure’’ Post-Traumatic Stress Disorder symptomatology. We knowthe complex interrelations between memory disordersand other psychiatric disorders. Patients had no comor-bid mood disorder according to the MINI-DSM-IV(Lecrubier et al., 1997). It is well known that the impactof mood disorders is important on the autobiographicalmemory: depressed and suicidal patients have great dif-ficulty to accessing personal memories in response to cuewords and cannot retrieve a specific memory (inMcNally, 1997a). In addition, the results from directedforgetting task demonstrated a differential directed for-getting effect that depended on the mood state of theindividual and the valence of the material to-be-forgot-ten (Power et al., 2000). Our choice was essential in or-der to understand better and isolate the memorymechanisms involved better. However, it could bejudged that this population without associated comor-bidity (neither psychiatric nor somatic) does not reflectclinical practice. It is in fact frequent to encounter otherpsychiatric disorders (amongst others, depression, anxi-ety disorders, addictive behavior, etc.) and somatic com-plications (head injuries, multiple injuries, etc.).

We checked if there were any correlations betweenthe clinical profile, the DFT and the psychological tests.First, there was no correlation between age, gender andsocio-cultural level and the tests. There was no correla-tion between the Directed Forgetting Task and WAIS-R, which made us conclude that the results of this testare not linked to the Intelligence Quota. On the otherhand, we found significant differences in Wechsler�smemory scale (except for the attention-concentrationindex), which shows that overall, the PTSD patients

O. Cottencin et al. / Journal of Psychiatric Research 40 (2006) 70–80 79

performed less well than the controls. This agrees withthe results obtained by Bremner et al. (1993) and addsweight to our idea that patients with PTSD have an ex-plicit memory deficit. This is also confirmed by the pa-tients� poorer performance in verbal fluency tests.Nevertheless, the significant impairment in memoryand verbal fluency suggests a rather broad memory def-icit in the patient group, which argues against a specificinhibition deficit in PTSD.

Otherwise, we found correlations between the DFTand the WMS for some items (verbal memory, generalmemory and final recall). Although these partial correla-tions are inconclusive, nevertheless, there seems to be arelationship between a worse performance in recallingwords ‘‘to remember’’ and a worse performance for ver-bal memory and final recall for WMS. There was a ten-dency for the directed forgetting effect to correlate witha good performance for WMS.

5. Conclusion

Our results seem to confirm that patients with PTSDhave a deficit in the inhibitory mechanisms of the mem-ory. A traumatic memory, whose invasive thoughts donot allow the inhibition processes to distinguish betweenrelevant and irrelevant information, either internal orexternal. Failure of these mechanisms is seen clinicallyby various memory disorders (amnesia, hypermnesia,ecmnesia), but the common feature is invasion of the pa-tients� consciousness. An improvement in the inhibitorycapacity may be accompanied by a progressive libera-tion of the processing resources in the working memory.We know that the best sign of improvement in a patientwith PTSD is a reduction in intrusion phenomena (reex-periencing). It would be interesting to continue the fol-low-up of these patients, to check their performance toa Directed Forgetting Task once their symptoms havebeen healed. However, these abnormalities could as eas-ily be a risk factor for PTSD as a consequence of it.From these results, it would be of interest to extend thisstudy to other aspects, both quantitatively (longitudinalstudy) and qualitatively (traumatized patients withoutPTSD, Acute Post-Traumatic Stress). In fact, it seemsto be important to deepen our knowledge of the inhibi-tory mechanisms involved in psychotrauma, with re-spect to their function and their clinical implications.Finally, the question remains about how prevention ortreatment could be envisaged for these aspects of PTSD.

Acknowledgement

We thank G. de Falco and R. Baert for their help intesting patients.

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