Memory and action: an experimental study on normal subjects and schizophrenic patients

Neuropsychologia 43 (2005) 281–293

Memory and action: an experimental study on normal subjects and schizophrenic patients Elena Daprati a, b, ∗ , Daniele Nico c, d , Arnaud Saimpont b , Nicolas Franck b, e , Angela Sirigu b a

Dipartimento di Fisiologia Neuromotoria, IRCCS Fondazione Santa Lucia, Via Ardeatina, 354, I-00179 Rome, Italy b Institut des Sciences Cognitives, CNRS, 67 Boulevard Pinel, F-69675, Bron, France c Dipartimento di Psicologia, Universit` a di Roma “La Sapienza”, via dei marsi 78, I-00185 Rome, Italy d Dipartimento di Neuropsicologia, IRCCS Fondazione Santa Lucia, via Ardeatina, 306, I-00179 Rome, Italy e Centre Hospitalier Le Vinatier, 95 Boulevard Pinel, F-69675, Bron, France

Abstract Psychologists have shown that recall of sentences describing previously performed actions is enhanced compared to recall of heard-only action-phrases (enactment effect). One interpretation of this effect argues that subjects benefit from a multi-modal encoding where movement plays a major role [see Engelkamp, J. (1998). Memory for actions. Hove, UK: Psychology Press, for a review]. In line with this motor account, it is conceivable that the beneficial effect of enactment might rely, at least in part, on procedural learning, thus tapping more directly implicit memory functions. Neuropsychological observations support this hypothesis, as shown by the fact that the enactment effect is quite insensitive to perturbations affecting declarative memories. i.e. Alzheimer disease [Karlsson, T., B¨ackman, L., Herlitz, A., Nilsson, L. G., Winblad, B., & Osterlind, P. O. (1989). Memory improvement at different stages of Alzheimer’s disease. Neuropsychologia, 27, 737–742] or Korsakoff syndrome [Mimura, M., Komatsu, S., Kato, M., Yashimasu, H., Wakamatsu, N., & Kashima, H. (1998). Memory for subject performed tasks in patients with Korsakoff syndrome. Cortex, 34, 297–303]. The present study attempts to evaluate whether pure motor activity is sufficient to guarantee the described memory facilitation or alternatively, whether first-person experience in carrying out the action (i.e. true enactment) would be required. To this purpose, in a first experiment on healthy subjects, we tested whether sentence meaning and content of the executed action should match in order to produce facilitation in recall of enacted action-phrases. In a second experiment, we explored whether the enactment effect is present in patients suffering from psychiatric disorders supposed to spare procedural memory but to alter action awareness (e.g. schizophrenia). We show that better recall for action phrases is found only when the motor component is a true enactment of verbal material. Moreover, this effect is nearly lost in schizophrenia. This latter result, on the one hand, queries the automatic/implicit nature of the enactment effect and supports the role of the experience of having performed the action in the first-person. On the other hand, it questions the nature of the memory impairments detected in schizophrenia. © 2004 Elsevier Ltd. All rights reserved. Keywords: Memory; Patients; Response times; Enactment effect; Schizophrenia

1. Introduction Studies in cognitive psychology have shown that encoding an action-phrase by enactment significantly facilitates recall with respect to pure verbal encoding (enactment effect, see Engelkamp, 1998, for a review). This effect has been described for phrases denoting simple actions such as “to wash one’s hands”, “to throw a ball” and the like, and it has been reported for lists of variable length, that are either lis∗

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0028-3932/$ – see front matter © 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2004.11.014

tened to (verbal encoding) or additionally acted out by the subjects (enactment encoding). Action-phrases can describe either common body-related actions (i.e. “to nod with your head”) or object-related actions (i.e. “to smoke a cigarette”). In the latter case, objects can be either real objects or imaginary ones, without modifying the effect that does not rely on object qualities. The reason why enacting should facilitate memory functions has been variously interpreted and several non-mutually exclusive accounts have been proposed. An interesting hypothesis suggests a pivot role of the motor system in inducing the effect, thus favoring the assumption of multiple

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modality-specific memory subsystems (Engelkamp & Zimmer, 1994a). Several lines of evidence support the motor specificity of the effect: in line with the reactivation hypothesis (Damasio, 1989), recent neuroimaging studies have shown activations in comparable areas during encoding and retrieval of memorized information (Nilsson et al., 2000; Nyberg et al., 2001). In particular, when subjects recalled enacted actionphrases a significantly increased activity was found in motor areas, suggesting that motor information may have become part of the memory trace. Similarly, behavioral studies have shown that when asked to recognize (within a list) those items that had been previously encoded by enactment, subjects mistakenly chose alternatives describing actions that required movements similar to those executed in the encoding phase (Engelkamp & Zimmer, 1994b; Mohr, Engelkamp, & Zimmer, 1989). On the contrary, they did not seem concerned by items requiring different motor acts, even when the content was semantically related. Likewise, a stable memory trace for action-phrases seems to rely on the actions having actually been carried out. merely concentrating on the movement as while observing (Engelkamp, 1997) or mentally simulating enactment (Denis, Engelkamp, & Mohr, 1991) although effective, does not produce the same high-quality encoding as real enacting. A further interesting issue pertaining the enactment effect arises from the possibility that the beneficial effect of enactment might rely, at least in part, on procedural learning, thus tapping more directly on procedural memory functions. Although the verbal format of both stimuli and response indicates that declarative forms of memory are also involved, neuropsychological evidence suggests a certain degree of independence from explicit memory systems. For instance, it has been shown that the enactment effect is quite insensitive to perturbations due to ageing (B¨ackman & Nilsson, 1985) and – more interestingly – to Alzheimer disease (Karlsson et al., 1989). Indeed, even if in this latter condition declarative memory functions are often deeply perturbed, the enactment effect is still detectable. This dissociation is in line with previous demonstrations of preserved motor skills in Alzheimer patients (Fleischman & Gabrieli, 1999) and strengthens the hypothesis of an involvement of motor procedures to the enactment effect. Similarly, despite the severe anterograde amnesia frequently described in Korsakoff syndrome, these patients have been found to benefit from the enactment effect as do normal controls (Mimura et al., 1998), suggesting a preserved implicit (most likely motor) memory system. To our knowledge, research on the enactment-induced memory facilitation has left unsolved one interesting question, namely whether pure motor activity is sufficient to elicit it or alternatively, whether true enactment (i.e. first-person experience in carrying out the action) would be required. Most reports have described the enactment effect for over-learned actions that is for well-established associations between verbal and motor semantics, thus preventing any distinction between these two alternatives. However, recent data collected on professional actors (Noice, Noice, & Kennedy, 2000) – and

later replicated in a population of non-actors (Noice & Noice, 2001) – suggest that also apparently unrelated movements may increase memory for verbal material. These authors argued that motor activity per se might be sufficient for the enrichment of the memory trace, likely through a non-specific mechanism. Alternatively, they proposed a more conservative explanation: given the communicative role of gesturing in acting, participants may have produced new “semantic” associations between the actions and speeches they performed in the play (Noice et al., 2000; Noice & Noice, 2001). Hence, apparently unrelated actions would have become a genuine enactment of the corresponding discourse, in agreement with previous reports on the enactment effect. However, we think that a further possibility could account for these results, namely that the experience of having carried out an action in the first-person (rather than motor activity per se), might facilitate recall. In other words, a specific episodic memory trace rather than an implicit memory facilitation would be involved. The present study attempted to directly address these issues. We predicted that if motor activity per se enhances memory traces, verbal material encoded in association to a motor component would produce better recall regardless of the semantic congruence between the two elements. Secondly, we expected that patients affected by psychiatric disorders affecting awareness states but not procedural memory should present this effect. On the contrary, if true enactment (i.e. the experience of having performed the action in the first-person) is required, we expected pure motor activity to be ineffective and defective awareness to interfere with recall.

2. Experiment 1 In the first experiment, we investigated the role that congruence between verbal and motor content plays on memory for action events. We assumed that if the facilitating effect of enactment depends on a non-specific motor enrichment of the trace, congruence between the sentence describing the action and the corresponding movement should not be critical. 2.1. Methods Before running the main experiment, two pre-tests were conducted on a preliminary pool of approximately 100 phrases describing common actions, in order to select those that yielded to comparable and recognizable pantomimes, and that required comparable effort to be verbally processed (see Appendix A). 2.1.1. Participants Sixteen right-handed volunteers, recruited among students and hospital staff, gave informed consent to participate to the experiment. They had normal/corrected to normal vision and did not report previous history of neurological/psychiatric disorders. Subjects were pseudo-randomly assigned to either

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the motor congruent condition (four women, four men, mean age 22.1 ± 2.2 years, range 18–26 years) or the motor incongruent condition (four women, four men, mean age 22.3 ± 2.1 years, range 19–26 years). 2.1.2. Procedure The experiment was organized in two parts, which were run within one session. Instructions for each part were separately read aloud to each participant by one experimenter. Instructions for the first part included a step-by-step description of the procedure, but made no reference as to the content of the second part of the session, or to the number of phrases presented. However, subjects were explicitly asked to pay attention to all the aspects of the task as they would receive questions on it in the later session. This was done in order to limit the possibility that subjects reverted to explicit encoding strategies. When ready, subjects entered a small cabin (200 cm × 200 cm × 70 cm) where they stood still, face to a computer screen located at approximately 1.5 m from the frontal plane. They were informed that a red or green box would appear on the screen. Then, they would hear a recorded male voice pronouncing an action phrase, quickly followed by a video presenting an actor pantomiming the corresponding action. Subjects were instructed to simply listen to the phrase if the cuebox was red and to perform the movement required by the experimental condition if the cue-box was green. In both cases, they were explicitly requested to pay attention to both the spoken phrase and the video because in the next part of the session they would be interviewed on these stimuli. A list of 30 common action-phrases (i.e. ‘to cross your fingers’, ‘to open the door’) was presented to each subject. For each phrase, time-course was the following: voice-onset was followed by cue-appearance by a random interval of 800–1000 ms and preceded video-onset by a randomized 500–800 ms interval. The experimenter initiated each trial by pressing a key. The cue-box (2 cm × 2 cm) appeared in the upper third of the computer screen and was either green (meaning ‘act’) or red (meaning ‘don’t move’) (Fig. 1). Two conditions were tested: (1) motor congruent and (2) motor incongruent. In the motor congruent condition, the motor activity requested by the green cue was a true pantomime of the action-phrase (enactment). In contrast, in the motor incongruent condition, motor activity was a standard act, namely to pull a rope through a pulley fixed to the computer desk, as if to collect it at one’s feet. This motor act was selected as it involved both proximal and distal movements of the upper limb and was likely to induce comparable motor activity across subjects. In both the congruent and incongruent condition, when enactment was required, subjects were instructed to move as soon as they heard the phrase. In the congruent condition, they were asked to rely on the video only if they felt puzzled on how/what to do. Subjects’ performance was recorded by a camera placed in a hidden location within the cabin in order to monitor whether errors in the procedure occurred: when subjects did not restrain from moving

Fig. 1. Procedure followed in the first session of all experiments. A list of 30 action-phrases was read to the subjects one item at a time. Each item was preceded by either a green or a red box instructing subjects to enact (green) or simply listen to the phrase and observe the video (red), respectively. Auditory presentation preceded video-onset by a random interval (500–800 ms) and followed the cue by a 800–1000 ms random interval. According to the experimental condition, on the green cue, subjects either enacted the phrase (congruent condition), or executed a standard motor act (incongruent condition).

when the red cue was on or failed to move when the green cue had been displayed the trial was discarded. Furthermore, for the enacted items, we recorded whether subjects moved in response to the auditory presentation (true enactment) or imitated the actor on the screen. Actions executed by the subjects were shown to two na¨ıve judges who rated whether they were recognizable pantomimes (congruent condition), and/or involved comparable motor activity across subjects (both conditions). Eight different 30-item lists were created from the pool of 60 items retained by the pre-test (see Appendices A and B for details), including both intransitive actions, such as ‘cross your fingers’ and the like, and actions that involved object use (i.e. ‘to open the door’). In the latter case, real objects were not provided and subjects had to pantomime the interaction. Each list included 15 to-be-enacted items (enacted) and 15 to-be-verbally encoded ones (verbal). Before testing recall, subjects were engaged for approximately 10 min in a visuo-spatial task (Raven Progressive Matrices PM47, 1940). Then, memory for the action phrases was tested by two measures of recall. The first was Free Recall, namely subjects were asked to write down a list including as many of the phrases they heard as they could. A time limit of 5 min for completing the task was given. Next, subjects were engaged in a second visuo-spatial task (Position of the Gap Match Test from B.O.R.B., Riddoch & Humphreys, 1993) lasting approximately 5 min. Finally, the second recall measure was required, namely a Recognition Task. Sixty sentences were presented one at a time in the center of a computer screen. For each sentence, subjects were required to decide whether it was old (i.e. an item they had heard during stimuli presentation) or new to them (i.e. an item that had not been previously presented). Subjects gave their responses

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by pressing one of two adjacent keys (M- and N-key) of the computer keyboard, and were instructed to respond as fast and as accurately as they could. 2.1.3. Data analysis Data recording and analysis was identical for both the congruent and the incongruent conditions. For Free Recall, only items that entirely corresponded to the original phrase were considered as correctly recalled. A strict criterion was applied and synonyms, singular/plural switches or other minor changes were not accepted. For Recognition, items that were correctly recognized as “old” were analyzed. For both measures, proportion of correctly recalled phrases (number of correctly recalled items/total of correctly encoded items) was computed for the “enacted” and the “verbal” items. Response times (RTs) required by subjects to decide whether an item was old were also computed for both the “enacted” and “verbal” items. Trials corresponding to errors in the procedure during stimulus presentation or retrieval phase were discarded, as were RTs greater than 7000 ms. Means were compared by three separate ANOVAs, run on proportion of correctly recalled items for Free Recall and Recognition Task, respectively, and on mean RTs for the Recognition Task. For all analyses, between groups factor was Motor Congruence (motor congruent versus motor incongruent group) and within subjects factor was Type of Encoding (enacted versus verbal). In order to control for the effects of a skewed distribution and satisfy the conditions for parametric statistical test, proportion of correct responses was previously submitted to arcsine transformation whereas RTs were submitted to logarithmic transformation. Scheff´e test was used for post hoc comparisons on significant interactions.

3. Results and discussion In the Free Recall Task, subjects entering the motor congruent condition correctly recalled about 40% of the phrases presented. This percentage decreased to 27% for those performing in the incongruent condition. In both groups of subjects, an additional 14% of items was recalled although using synonyms or containing singular/plural switches and other minor changes, and was thus discarded from analysis (motor congruent 14.7%; incongruent 13.7%). In the Recognition Task, subjects correctly recognized over 80% of items in both conditions, confirming that they all had attentively performed in the encoding phase.

As can be seen in Table 1, results obtained in the congruent condition are consistent with previous studies: subjects recalled more enacted items compared to verbally encoded ones. This was true for both the Free Recall and the Recognition Task. Response times were similarly affected. Interestingly, this pattern was almost reversed for the incongruent condition: namely, subjects recalled less enacted phrases when a standard motor act was associated, and required more time to discriminate them from the new items. Statistical comparisons confirmed these observations: for Free Recall, the ANOVA showed a main effect of Group (F(1, 14) = 6.304, p < .03) and a significant interaction between Group and Type of Enactment (F(1, 14) = 39.137, p < .00002). In other words, subjects in the congruent condition recalled more items than those in the incongruent condition. More interestingly, as suggested by the significant interaction, this difference was due to the larger number of enacted items recalled by subjects in the congruent condition (see Fig. 2, left panel), suggesting that only execution of a congruent motor act improves recall of the corresponding action-phrase. Post hoc analysis confirmed that no difference between groups emerged for verbally encoded items (motor congruent condition: 0.21 ± 0.12; motor incongruent condition: 0.36 ± 0.11, p = ns). In contrast, the two groups significantly differed for the proportion of enacted items correctly recalled (motor congruent condition: 0.58 ± 0.13; motor incongruent condition: 0.19 ± 0.11, p < .0001). Accordingly, the enactment effect was found only for the motor congruent condition (p < .0008). A similar pattern emerged when analyzing data from the Recognition Task. Again, at the ANOVA, both main effect of Group (F(1, 14) = 5.321, p < .04) and interaction between Group and Type of Encoding were significant (F(1, 14) = 47.257, p < .00001, Fig. 2 right panel, main graph). Post hoc analysis confirmed that no difference was present between groups as for proportion of “verbal” items that were correctly recognized. On the contrary, the two groups significantly differed for the amount of “enacted” items recalled (motor congruent condition: 0.99 ± 0.02; motor incongruent condition: 0.77 ± 0.13, p < .0001). Again, the enactment effect was found only for the motor congruent condition (verbal items 0.79 ± 0.11, enacted items 0.99 ± 0.02, p < .00001). These observations were confirmed by chronometric data: ANOVA results showed both a significant main effect of Group (F(1, 14) = 17.862, p < .0008) and of the interaction between Group and Type of Encoding (F(1, 14) = 16.996, p < .001, Fig. 2 right panel, detail). Namely,

Table 1 Summary of the results of Experiment 1: mean and S.D. for enacted and verbally encoded items in the two measures of retrieval examined Condition

Congruent Incongruent

Free Recall

Recognition

Proportion correct

Proportion correct

Response times

Enacted

Verbal

Enacted

Verbal

Enacted

Verbal

0.58 (0.13) 0.19 (0.11)

0.22 (0.12) 0.36 (0.11)

0.99 (0.02) 0.78 (0.13)

0.79 (0.11) 0.83 (0.12)

1153.45 (249.23) 1784.79 (274.74)

1277.88 (262.42) 1666.76 (221.31)

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Fig. 2. Experiment 1 – Effect of motor congruence. Left panel: proportion of correctly recollected items in the Free Recall Task for subjects entering the Congruent condition (diamonds, solid line) or the Incongruent condition (squares, dotted line), according to Type of Encoding (enacted vs. verbally encoded items). Error bars represent standard errors. Right panel: proportion of items correctly recollected as ‘old’ ones in the Recognition Task (main graph) and time required to classify them (detail). Other captions as for the left panel.

subjects in the motor congruent condition responded faster (1215.7 ± 252.8 ms) than those in the motor incongruent condition (1725.8 ± 226.9 ms); consistent with data on proportion of correct responses, the enactment effect emerged only within the former group (enacted items 1153.5 ± 249.23 ms; verbal items 1277.9 ± 262.42 ms, p < .005). Subjects in the incongruent condition showed the opposite pattern (standard motor act items: 1784.8 ± 274.7 ms; verbal items: 1666.8 ± 221.3 ms, p < .0.03). One possible explanation for these results could be the peculiarity of the present experimental set-up. Differently from previous studies, we provided redundant information, as subjects both listened to an action-phrase being spoken and observed the corresponding action on the screen. There is evidence for a modest effect of action observation on memory for actions (Engelkamp, 1997): hence, the present procedure might have slightly enhanced recall of verbal items and reduced the enactment effect. This was clearly not the case: although this procedure applied to both conditions, the enactment effect failed to emerge only in the incongruent condition. More appealingly, results of Experiment 1 suggest that in order to benefit from the enactment effect, an established semantic correspondence between content of the phrase and motor activity is required. If unrelated to the semantic content of the phrase, movement interferes with – rather than facilitates – memory processes. This seems to be true even when motor activity is associated to non-action phrases, namely when no interference between enacted and observed/listened actions could be expected. To test this issue, we run a preliminary test on four more subjects (two women, two men, mean age 22.2 ± 1.3 years, range 21–24 years). Procedure was kept identical to that of Experiment 1, except for the verbal material that included only non-action phrases (i.e. “le singe est agile”, the monkey is lively; “l’interpr´etation

est fid`ele”, the interpretation is correct). As in the previous case, these subjects reported fewer items in the Free Recall Task (12%), compared to Recognition (67%). Proportion of correctly retrieved items during Free Recall did not significantly differ between items associated (0.12 ± 0.10) and not associated to motor activity (0.12 ± 0.11, p = ns). The same was true in the Recognition Task (motor activity: 0.58 ± 0.03; no motor activity: 0.77 ± 0.13; p = ns), where also RTs for recognizing as old one item did not differ according to whether it was encoded with/without motor activity (motor activity: 1479.8 ± 124.7 ms; no motor activity: 1567.3 ± 198.6 ms, p = ns). Although preliminary, these results seem to further support those of Experiment 1, which indicates an extremely specific contribution of the motor system to the encoding phase. This observation is in line with previous studies on movement similarity and with the assumption of a specific motor memory-module (Engelkamp & Zimmer, 1994a,b; Mohr et al., 1989). The novel finding is that we can now qualify the nature of this contribution as a motor memory trace that matches the verbal one in semantic terms. In this view, data collected on professional actors as reported by Noice et al. (2000) and Noice and Noice (2001) can be accounted for by their more conservative hypothesis: for the purpose of the play, actors had likely ascribed an equivalent meaning to words and actions otherwise unrelated, thus establishing a specific correspondence through new semantic associations, capable to induce an enactment effect.

4. Experiment 2 As true enactment seems to be the relevant issue, it appears that the experience of having carried out the action, rather than motor activity per se, enhances memory for enacted phrases.

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Psychiatric Association, 1994) were recruited at the psychiatric hospital “Le Vinatier” in Lyon, France. All were native French speakers. Main clinical and demographic data are summarized in Table 2. Five patients met the criteria for undifferentiated schizophrenia, two for paranoid schizophrenia and one for disorganized schizophrenia. At the time of testing, only four patients (P2, P4, P7, P8) presented a hallucination subscale score of 3 or greater (i.e. medium to severe; SAPS mean 3.5 ± 4.3, range 0–12), although all patients had a reported history of hallucinations. All were clinically stable at the time of testing. In three cases, dosage and type of anti-psychotic drugs suggested a possible interference with memory functions. Thus, these subjects (P5, P6, P7) were also administered a verbal memory test (Grober & Buschke’s Test, French adaptation by Ergis, Van Der Linden, Boller, Degos, & Deweer, 1995). In one case only, performance was at the lower limits of the normal range for certain measures (see Table 3). Nevertheless, as this patient (P5) was highly collaborative and did not differ from the rest of the group in her performance at the present task, she was retained. Basic neuropsychological screening was administered to all patients, confirming that they showed normal non-verbal intelligence (Raven Progressive Matrices PM47), no short-term memory deficit (Digit Span) and good perceptual abilities (Position of the Gap Match Task, subtest of B.O.R.B., Riddoch & Humphreys, 1993). Eight age-matched controls were recruited among students and hospital staff (see Table 4 for details). They had normal/corrected to normal vision, and did not report previous history of neurological/psychiatric disorders. In order to ensure that the two groups did not statistically differ on the main demographic and cognitive variables separate t-test for independent samples were run on those parameters (age, education level, handedness index, Raven, Gap Match and Digit Span). A significant difference emerged only for the Raven

This conclusion raises the question whether the enactment effect can be entirely considered as a form of procedural learning. Data on amnesic patients (Mimura et al., 1998) indicate that the enactment-induced facilitation may not require conscious access to the encoded information at retrieval. Indeed, motor-encoded items are best remembered even when subjects are unable to explicitly access their memory. We explored this issue in a different pathological condition, i.e. schizophrenia, where procedural memory functions are reported to be almost entirely spared (Clare, McKenna, Mortimer, & Baddeley, 1993; Danion, Meulemans, KauffmannMuller, & Vermaat, 2001; Kazes et al., 1999; Keri et al., 2000). As is the case for amnesia, in this condition consciously accessed processes are more attained, although in the absence of documented brain damage to the classical declarative memory systems. Interestingly, recent studies support the notion of a disorder of motor awareness in schizophrenia (Daprati et al., 1997; Fourneret, Franck, Slachevsky, & Jeannerod, 2001; Franck et al., 2001; Frith, Blakemore, & Wolpert, 2000), which may eventually arise from a defective monitoring of self-generated actions (Frith, 1987, 1992). In other words, these patients may suffer from a higher order deficit in perceiving the origin of a given action, suggesting that their first-person experience when carrying out a movement may be incomplete. This creates an interesting dissociation for the study of memory for action events. Indeed, if the enactment effect relies on procedural “motor” learning and does not require consciously accessed processes we should be able to detect it even in schizophrenic patients. 4.1. Method 4.1.1. Subjects Eight patients (four women, four men, mean age 38.25 ± 13.4 years, range 22–61 years) with a clinical diagnosis of schizophrenia according to DSM-IV (American Table 2 Main demographic and clinical details of patients involved in Experiment 2 Patients

P1

P2

P3

P4

P5

P6

P7

P8

Mean

Age Gender Education Handednessa Illness durationb Typec Medicationd SAPS score SANS score Raven PM47 Gap Matche Digit Spanf

46 m 13 1.0 26 U 300 26 17 31 34 –

32 f 12 1.0 2 D 100 34 60 30 29 6/4

38 f 13 0.85 9 P 250 30 10 33 36 7/4

61 m 12 0.95 36 P 350 31 76 29 33 5/3

51 f 11 0.85 16 U 200 30 38 20 27 5/4

22 m 9 0.90 4 U 100 15 44 17 33 5/3

27 f 11 −0.35 9 U 200 25 37 32 36 7/5

29 m 9 0.95 4 U 800 19 41 25 36 5/4

38.25 (±13.39) 4 f, 4 m 11.25 (±1.58) 0.77 (±0.46) 13.25 (±12.08)

a b c d e f

According to the Edinburgh Inventory (Oldfield, 1971). Time elapsed since onset of psychotic symptoms. Schizophrenia subtypes according to DSM-IV. U, undifferentiated; D, disorganized; P, paranoid. Mean dose (chlorpromazine equivalents) for the last 3 months. Position of the Gap Match Task, subtest of B.O.R.B. (Riddoch & Humphrey, 1993), normal range 24–39. Subtest of W.A.I.S. (Wechsler, 1991), forward/backward Digit Span; cut-off = 4.

287.50 (±224.8) 26.25 (±6.45) 40.38 (±21.23) 27.13 (±5.89) 33.00 (±3.38) 5.71/3.86 (±0.95/0.69)

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Table 3 Results of the verbal memory test (Grober & Buschke’s Test, adapted by Ergis et al., 1995) for P5, P6 and P7 Patients

Immediate Recall

P5 P6 P7

13 15 16

Controls Mean S.D.

15.7/15.5 (0.7/0.9)

Free Recall

Cued Recall

1st

2nd

3rd

1st

2nd

3rd

5 7 8

5 9 12

9 13 10

5 4 8

5 4 4

3 3 5

10.3/11.6 (2.6/2.0)

12.1/13.5 (3.0/1.5)

9.4/9.6 (2.6/2.6)

5.3/5.2 (2.0/2.1)

5.0/3.9 (2.3/1.8)

3.5/2.3 (2.4/1.4)

Testing was administered before patients entered the experimental sample. Controls normative values for the two age groups (P5/P6–7) are reported below.

Type of Encoding (enacted versus verbal). In order to control for the effects of a skewed distribution and satisfy the conditions for parametric statistical test, proportion of correct responses was previously submitted to arcsine transformation whereas RTs were submitted to logarithmic transformation. Scheff´e test was used for post hoc comparisons on significant interactions. As one patient was ambidextrous and the Recognition Task required manual response with the dominant hand, data from P7 were not included in the analysis.

Progressive Matrices (PM47), where patients scored below the controls’ means (t = 3.143, p < .01). Although the latter test is considered a measure of non-verbal intelligence, this difference was nonetheless taken into account in the analyses: a test was run to exclude that results obtained in the memory task correlated with the performance at the Raven test. In accordance with the local ethical committee (and Declaration of Helsinki), all participants signed informed consent before volunteering for this study. 4.1.2. Procedure The apparatus and procedure previously described for the motor congruent condition of Experiment 1 were employed. Stimuli were driven from the same pool of 60 action-phrases and eight different 30-item lists were created, each including 15 to-be-enacted items (enacted) and 15 to-be-verbally encoded ones (verbal). Subjects and patients were assigned to one of the lists according to recruitment order. Testing for recall followed the same procedure used in Experiment 1, although only a 5-min interval was imposed between the end of stimulus presentation phase and the first recall test.

5. Results and discussion All patients correctly understood the task and errors in the procedure were rare, accounting for 5.8% of trials. As expected, for both patients and controls, performance was better in the Recognition Task than in Free Recall, although this difference was more important in the patients’ group. On average, control subjects freely recalled about 32.9% of the action-phrases. An additional 13.7% of items was recalled with minor changes, and was thus discarded from analysis. Patients as a group were able to freely recall only 13.8% of the presented items; the amount of items recalled although with minor distortions was equally smaller (9.2%). In the Recognition Task however, percentages of correctly recognized items raised to 89.2% for controls and 71% for the patients, confirming that both groups had correctly attended to the task in the encoding phase. As shown in Table 5, controls reported more enacted items than verbally encoded ones, consistently with previous observations. This was true for both the Free Recall and the

4.1.3. Data analysis Data recording and analysis was identical to Experiment 1. For each group, recall of “enacted” and “verbal” items was measured as proportion of correctly recalled/recognized items in the Free Recall and Recognition Task, respectively, and as mean response times in the Recognition Task. Means were then compared by three separate ANOVAs. For all analyses, between-groups factor was Group (schizophrenic patients versus control group) and within-subjects factor was Table 4 Main demographic details of control subjects involved in Experiment 2 Controls

C1

C2

C3

C4

C5

C6

C7

C8

Mean

Age Gender Education Handednessa Raven PM47 Gap Matchb Digit Spanc

44 f 11 0.95 36 37 7/5

53 f 14 0.80 34 27 5/4

59 m 7 0.60 34 28 6/4

44 f 15 0.90 35 38 7/5

22 m 12 0.90 36 35 7/4

38 m 11 0.90 34 38 7/7

23 f 12 0.80 36 40 7/6

26 f 12 0.85 36 39 7/5

38.63 (±13.64) 5 f, 3 m 11.75 (±2.38) 0.84 (±0.11) 35.13 (±0.99) 35.25 (±5.01) 6.63/5.00 (±0.74/1.07)

a b c

According to the Edinburgh Inventory (Oldfield, 1971). Position of the Gap Match Task, subtest of B.O.R.B. (Riddoch & Humphrey, 1993), normal range 24–39. Subtest of W.A.I.S. (Wechsler, 1991), forward/backward Digit Span; cut-off = 4.

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Table 5 Summary of the results of Experiment 1: mean and S.D. for enacted and verbally encoded items in the two measures of retrieval examined Group

Schizophrenics Controls

Free Recall

Recognition

Proportion correct

Proportion correct

Response times

Enacted

Verbal

Enacted

Verbal

Enacted

Verbal

0.12 (0.13) 0.42 (0.15)

0.15 (0.13) 0.24 (0.12)

0.80 (0.20) 0.98 (0.03)

0.71 (0.13) 0.82 (0.15)

1874.74 (678.55) 1281.02 (402.59)

1866.58 (592.37) 1421.80 (480.40)

Recognition Task. Response times were similarly distributed, and enacted phrases were also recognized faster. On the contrary, patients performed poorly in both categories in the Free Recall Task. In the Recognition Task, proportion of correctly recognized items was slightly larger for enacted than for verbal items, although this effect was not confirmed by comparably distributed response times. Statistical comparisons confirmed these observations: for Free Recall, the ANOVA showed a main effect of Group (F(1, 14) = 9.348, p < .009) and a significant interaction between Group and Type of Enactment (F(1, 14) = 7.354, p < .02). In other words, controls recalled more items than patients (proportion of correctly recollected items: controls 0.33 ± 0.12, patients 0.14 ± 0.12). More interestingly, as suggested by the significant interaction, this difference was due to the larger number of enacted items recalled by controls (see Fig. 3, left panel), suggesting that only within the former group enactment was effective. Post hoc analysis confirmed that no difference between groups emerged for verbally encoded items (controls: 0.24 ± 0.12; patients: 0.14 ± 0.13, p = ns). In contrast, the two groups significantly differed for the proportion of enacted items correctly recalled (controls: 0.42 ± 0.15; patients: 0.14 ± 0.13, p < .0001). Accordingly, the enactment effect was found only within the control group (p < .02).

For the Recognition Task, the ANOVA showed again the main effect of Group (F(1, 13) = 6.079, p < .05) and Type of Encoding (F(1, 13) = 13.334, p < .002, Fig. 3 right panel, main graph), although the interaction failed to reach significance. This failure may partly arise from a ceiling effect, given that almost all controls scored close to 100% and several patients scored over 90% correct in both conditions. Moreover, a consistent enactment effect as described by the literature (and as found in controls) was found for patient P4 only (enacted items 0.85, verbal items 0.53). In two other patients, verbal items were recognized slightly better than enacted ones (P2, P8), the remaining patients showing no clear difference between the two conditions. The absence of an enactment effect for Recognition Task in the patients’ group was confirmed by chronometric data: ANOVA on response times clearly showed a significant interaction between Group and Type of Encoding (F(1, 13) = 5.244, p < .03, Fig. 3 right panel, detail). In other words, controls required shorter latencies to recognize as old the enacted items (enacted 1290.9 ± 401.5 ms, verbal 1497.6 ± 531.8), thus showing a consistent enactment effect. This was not the case in patients who were significantly slower than controls when recognizing enacted items (1874.7 ± 678.5 ms) and showed no difference between the

Fig. 3. Experiment 2 – effect of motor awareness. Left panel: proportion of correctly recollected items in the Free Recall Task for control subjects (diamonds, solid line) and schizophrenic patients (squares, dotted line), according to Type of Encoding (enacted vs. verbally encoded items). Error bars represent standard errors. Right panel: proportion of items correctly recollected as ‘old’ ones in the Recognition Task (main graph) and time required to classify them (detail). Other captions as for the left panel.

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two types of encoding. Post hoc analysis confirmed that the two groups significantly differed for the time required to recognize as old the enacted items (p < .00001) and that the enactment effect was found only within the control group (p < .02). Results of Experiment 2 show that, differently from controls, schizophrenic patients did not benefit from performing the action in the retrieval conditions we analyzed. Whereas control subjects reported more items from the ‘enact’ category and responded faster when recognizing them, this was not the case for our patients. Although striking, the present result should be regarded with caution, due to the small sample of patients tested and to the nature of their disorder. Four patients scored below the controls’ mean as for measure of non-verbal intelligence as the Raven Progressives Matrices (PM47), suggesting a possible cognitive impairment. However, no correlation emerged between responses in the memory task and performance at the Raven test (Pearson Product Moment Correlation: Free Recall, r = .695 p = ns; Recognition: proportion correct, r = .310, p = ns; response times, −0.682, p = ns). One alternative interpretation for the absence of enactment effect in the patients’ group could be a broad memory impairment, as severe memory deficits had been reported in schizophrenia (Aleman, Hijman, de Haan, & Kahn, 1999; Saykin et al., 1991). Similarly, since most patients were receiving medication, one could speculate that treatment may have contributed to the impairment in recall/recognition memory. However, neither possibility is supported by the present data. Had illness and/or drug treatment been involved, we would have expected it to affect to a comparable extent memory for both enacted and verbally encoded items. This was not the case: in the present group of patients, the amount of items recalled following verbal encoding was not significantly different from that of normal controls, suggesting an adequate ability to store information in memory. Moreover, in those patients where a standardized verbal memory test (Grober & Buschke’s Test, French adaptation by Ergis et al., 1995) was administered, performance was generally within normal range (see Table 3). Finally, no correlation between performance and dose of anti-psychotic agents was found. Although with the limitation discussed above, we think that two comments should be drawn from results of Experiment 2: first, the absence of enactment effect in our sample of schizophrenic patients contrasts with the hypothesis that the beneficial effect of enactment might rely, at least in part, on procedural learning, which is supposed to be preserved by schizophrenia. Second, the richer encoding for the enacted items should have eventually facilitated recall by the patients (Br´ebion, Smith, Amador, Malaspina, & Gorman, 1997; Ragland et al., 2003), which was surprisingly not the case. With respect to the former issue, although other forms of procedural learning were not directly tested, it seems that in the present task these patients behaved differently from other subjects for whom a dissociation between declarative and procedural memory has been evoked. As previously re-

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ported, the enactment effect is present in patients suffering from Alzheimer disease (Karlsson et al., 1989) or Korsakoff syndrome (Mimura et al., 1998) and, interestingly, also in patients with frontal lobe damage (McAndrews & Milner, 1991). One possible interpretation to account for both discordances may be that an impaired ability to identify the origin of a given motor act may have lead schizophrenic patients to pay a cognitive cost similar to that showed by normal subjects in the motor incongruent condition of Experiment 1. Indeed patients appear to produce a poor memory trace of the event, thus reducing the strength of motor encoding, i.e. the difference between enacted and verbal items. This would not be the case for neuropsychological patients where this latter skill is spared.

6. General discussion It has been widely demonstrated that when learning a list of action-phrases, encoding becomes more efficient if enactment is added to the verbal input. This effect suggests that action-phrases may be encoded through a multi-modal storage that involves both semantic and kinaesthetic memories of previously performed movements (Engelkamp & Zimmer, 1994a). Whereas verbal encoding likely depends on explicit memory functions, the motor component has been suggested to be based – at least in part – on procedural learning and accordingly, on implicit memory processes. According to an influential theory (see for example, Schacter, Chiu, & Ochsner, 1993), explicit memory is the intentional (i.e. conscious) storing and/or recollection of previous experiences. On the contrary, the term implicit memory refers to those modifications of knowledge or behavior that can be ascribed to information/skills subjects have “implicitly” acquired. Namely, information that subjects were not explicitly required to learn or to recollect – and may not even be able to. In the present case, even if recall/recognition of action-phrases involved explicit retrieval, the difference found between enacted and verbally encoded items would be better attributed to the activity of an implicit memory system, most likely a motor memory system. Results on normal subjects support the hypothesis that movement is part of the memory trace (Nilsson et al., 2000; Nyberg et al., 2001): here, retrieval of action-phrases benefits from congruent motor activity but is interfered by incongruent one (see Section 2). Although preliminary due to the small dimension of the sample examined, results of Experiment 2 indicate a failure to find a consistent facilitation for enacted items in schizophrenic patients. This result may be conservatively explained as an implicit memory deficit. Basal ganglia, and particularly the striatum, have long been considered a relevant part of the implicit memory system: procedural learning deficits are frequent in patients suffering from basal ganglia dysfunction, such as Parkinson’s disease (Brown & Marsden, 1990; Krebs, Hogan, Hening, Adamovich, & Poizner, 2001; Saint-Cyr, Taylor, & Lang, 1988; Sarazin et al., 2002).

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Similarly, the ventral region of striatum, pallidum and tegmental area have been also claimed to be involved in the pathogenesis of schizophrenia (see Graybiel, 2000 for a brief review). Accordingly, reduction of the enactment effect in these patients may reflect poor functioning of implicit memory systems, as sustained by basal ganglia dysfunction. An alternative hypothesis would be that the facilitation induced by enactment requires a reliable episodic memory trace of the event, which could be acquired only in presence of an efficient conscious monitoring of actions while encoding. This interpretation may account for the negative result found in schizophrenics: indeed an impairment in the ability to monitor willed actions has been invoked to explain several of the symptoms described in these patients (Frith, 1992). Here, a defective ability to keep trace of one’s own actions may have weakened the difference between observed and enacted items and, as a result, reduced the enactment effect in schizophrenics. Tulving (1983) proposed a distinction between “autonoetic consciousness”, i.e. the awareness of subjective experiences, and “noetic consciousness”, defining more general knowledge (semantic). Thus, autonoetic awareness would be a special feature of episodic memory, being characterized by mentally “re-living” events from one’s personal past. The socalled “remember/know” paradigm (Tulving, 1985) attempts to dissociate these experiences: an item is ‘remembered’ when subjects can consciously recollect something they experienced at the time when the item was learnt. In contrast, an item is ‘known’ when it is recognized on some other basis – i.e. familiarity. It has been shown that schizophrenic patients show reduced ‘remember’ but normal ‘know’ responses (Huron et al., 1995). This failure would derive from inability to bind together the different aspects of an event, such as a content and its source (‘representational binding’, Danion, Rizzo, & Bruant, 1999; Rizzo, Danion, Van der Linden, Grange, & Rohmer, 1996). As a consequence, patients would be unable to reconstruct the original experience and fail to have a proper recollection (‘remember’). Data showing that patients with schizophrenia suffer from source memory impairments, partially support this hypothesis (Franck et al., 2000; Harvey, 1985; Vinogradov et al., 1997). Here, the reduced memory for enacted items in schizophrenics is suggestive of an impairment in their autonoetic awareness. Performed actions may have lost the specific trace induced by first-person experience as a consequence of defective binding between the action-representation stored in memory on the one side, and knowledge of the “self” as the author of the action on the other. One last point could be addressed. Memory deficits in schizophrenia have been linked to negative symptoms, more precisely to depressive symptoms and anergia (Br´ebion et al., 1997; Goldberg, Weinberger, Pliskin, Berman, & Podd, 1989; Tamlyn et al., 1992). A comparable correlation was found also in the present case: proportion of correctly recalled items in the Free Recall, as well as response times in the Recognition Task, correlated with those sub-items of the Scale for the

Assessment of Negative Symptoms (Andreasen, 1983) suggestive of a depressive state (i.e. poverty of content of speech (r = −.827; p < .01), unchanging facial expression (r = −.770; p < .02), lack of vocal inflections (r = −.782; p < .02)). Patients receiving high scores in those items reported less correct responses, with longer delays, suggesting a more compromised memory module. However, no correlations were found with respect to the memory task. Although speculative, it is worthy of note that both memory deficits and depressive symptoms in schizophrenic patients have been related to abnormal activity in the prefrontal cortex (Dolan et al., 1993; Fletcher et al., 1995). Morphological modifications in ventral frontal cortex have been reported, and the suggestion has been made that these variations may play a role in the patients’ abnormal behavior (Chemerinski, Nopoulos, Crespo-Facorro, Andreasen, & Magnotta, 2002). Interestingly, prefrontal cortex seems also involved in maintaining autonoetic awareness (Wheeler, Stuss, & Tulving, 1995): damage to this area might impair the capacity to re-experience retrieved information as part of one’s past (Levine et al., 1998). Furthermore, the same area has been recently claimed to play a role in conscious monitoring of actions (Slachevsky et al., 2003). With respect to this issue, comparison between the performance of patients with frontal brain damage and schizophrenic subjects on an identical paradigm should make the object of future studies. In conclusion, on the basis of the present data, we confirm that the beneficial effect of enactment on memory for actions relies on the motor system. In addition, we provide novel evidence that in order for this facilitation to take place, awareness of action while enacting and/or a correct binding between stored representations of the action and of the “self” as the agent is also required.

Acknowledgements The authors are indebted to L. Granjon for his patience and assistance in organizing most technical aspects of the paradigm, to T. Nazir and N. Benboutayab for help in dealing with the linguistic aspects of the task and to M. Hoen for being the excellent mime of our videos. E.D. is grateful to Prof. G. Rizzolatti for discussion of the data. Research supported by CNRS.

Appendix A. Selection of action-phrases A.1. Actions selection procedure A male right-handed actor, dressed in black, performed the actions in front of a dark background, maintaining a neutral facial expression. Whenever objects were involved in the action, a pantomime was produced. The actor’s face and body (to knee level) were recorded by a digital video camera and each action was then converted in a video-clip lasting 4 s. These videos were shown in random order to 18

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subjects (9 men, 9 women, mean age 24.2 ± 3.6 years, range 21–30 years) who rated motor complexity and produced a short sentence – whenever possible in the verb/article/noun form – which could describe the action they had just seen. Each video could be seen twice. All responses were typed and classified. “Don’t know” responses were allowed. As actions described common activities, most pantomimes elicited the same phrase. Videos that produced a consistent description in over 75% of subjects were retained and the most frequent sentence produced by the subjects was coupled to that video. A.2. Phrases selection procedure Phrases retained from the previous test were inspected for uniformity of grammatical structure: 85% of the sentences had a “verb/article/name” structure or close variants. Other structural classes (i.e. “verb/adjective/verb/adjective”) accounted for 15% of all phrases and were uniformly distributed across object-related and non-object-related action-phrases. Word frequency, phonemes and number of syllables for each phrase were computed on the basis of BRULEX database for French language (Content, Mousty, & Radeau, 1990). A list of 60 action-phrases (36 object-related and 24 nonobject-related) that did not statistically differ on the abovementioned measures (at an ANOVA for repeated measures) was thus selected. Reading and processing time for these sentences were determined by means of a plausibility task. Each action-phrase was paired to a meaningless sentence sharing the same structure/length for a total of 120 items. Nine subjects (eight women, one man, mean age 26.0 ± 4.61 years, range 22–37 years) were asked to read each sentence wordby-word and to decide whether it corresponded to a meaningful or meaningless sentence. Single words appeared in the middle of a computer screen – written in black ink – one at a time. Subjects pressed the Ø-key of the computer keyboard to display the next word, and (once the last word had been read) to get the question they should respond to (“is it a meaningful sentence?”/“is it a meaningless sentence?”). Subjects were instructed to press the 1-key/2-key for “yes”/“no” responses respectively. Two lists of 60 sentences were created associating each phrase to either type of question. Subjects were randomly assigned to either list. Reading time (=time elapsed between appearance of the first word and last Ø-key press) and decision time (=time elapsed between question presentation and 1-key/2-key press) for each sentence’s main category (object-related actions/non-object-related actions) were submitted to separate ANOVAs for repeated measures. Response times shorter than 150 ms or longer than 2000 ms (for Ø-key press) or 5000 ms (for 1-key/2-key press) were discarded as errors (percentage of errors <0.1% for all subjects). No significant differences were detected, suggesting that sentences were comparable both in terms of structure (reading time) and meaning (decision time). Average reading time was 1642.8 ± 548.9 ms and average decision time 1011.8 ± 261.6 ms.

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Appendix B. Complete phrase list B.1. Action phrases B.1.1. Object-related actions jouer aux casino (to play slot-machines); peindre un mur (to paint a wall), jouer au basket (to play basket-ball), tourner une clef (to open with a key), repasser un drap (to iron a cloth), porter une valise (to lift a suitcase), ouvrir une porte (to open a door), tourner des pages (to turn pages), jouer aux billes (to play marbles), verser de l’eau (to pour water), caresser un chien (to pat a dog), jouer aux d´es (to play dices). secouer un shaker (to shake a shaker), ouvrir un store (to open a shutter), fermer un bocal (to close a jar), d´echirer une feuille (to tear a sheet of paper), jouer de la batterie (to play drums), e´ taler la pˆate (to spread pastry), couper de la viande (to cut meat), visser une ampoule (to change a lamp), distribuer les cartes (to distribute cards), planter un clou (to fix a nail), coudre un bouton (to sew a button), scier du bois (to saw a wooden stick). se peigner les cheveux (to comb one’s hair), r´epondre au t´el´ephone (to answer the phone), mettre un chapeau (to put one’s hat on), s’essuyer la bouche (to clean one’s lips), mettre des lunettes (to wear glasses), boire a` la bouteille (to drink from the bottle), manger de la soupe (to eat with a spoon), boutonner sa chemise (to button one’s shirt), mettre une e´ charpe (to put one’s scarf on), se couper les ongles (to cut one’s nails), enfiler un gant (to put one’s glove on), mettre sa montre (to wear one’s watch). B.1.2. Non-object-related actions tourner la tˆete (to turn one’s head), regarder en l’air (to look up), souffler tr`es fort (to blow hard), se gratter le nez (to rub one’s nose), se boucher les oreilles (to cover one’s ear), se recoiffer le cheveux (to pass one’s hand on one’s hair), e´ tirer les bras (to stretch one’s arms), se pencher en avant (to bend down), tourner sur soi (to rotate oneself), se frotter le bras (to rub ones’ arms), se frotter les mains (to rub one’s hands), se craquer les doigts (to stretch one’s finger). hausser les e´ paules (to show disappointment), faire une reverence (to bow), se prendre la tˆete (to take one’s head in one’s hands), faire le salut militaire (to salute militarily), faire signe de venir (to call someone), serrer la main (to shake hands), faire du stop (to hitchhike), faire c’est super (to make an OK sign), claquer des doigts (to snap one’s finger), croiser les doigts (to cross one’s finger), compter sur ses doigts (to count on ones’ finger), se tourner les pouces (to twiddle one’s thumbs). References Aleman, A., Hijman, R., de Haan, E. H. F., & Kahn, R. S. (1999). Memory impairment in schizophrenia: A meta-analysis. American Journal of Psychiatry, 156, 1358–1366. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington: American Psychiatric Association.

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