Altered Subjective Time of Events in Schizophrenia

BRIEF REPORTS Altered Subjective Time of Events in Schizophrenia Nicolas Franck, MD, PhD,*† Andrés Posada, PhD,*‡ Swann Pichon, MSc,* and Patrick Haggard, PhD§ Abstract: Time perception has long been known to be impaired in schizophrenia. Moreover, recent neuropsychological theories have postulated abnormalities of cognitive motor control in schizophrenia. However, the intersection of these two topics has rarely been studied, and it is unclear what role subjects’ own actions may play in the construction of subjective time representation. The present experiment compared the performance of 19 patients with schizophrenia and 24 normal controls in a timing judgment task. The results show that patients bind two consecutive movements more strongly than controls. This anomaly could play a role in the subjective pathological experiences of patients. Key Words: Schizophrenia, time, action, perception, binding, hyperbinding. *Institut des Sciences Cognitives, CNRS, Lyon, France; †Centre Hospitalier Le Vinatier and Université Claude Bernard, Bron, France; ‡Centro Internacional de Fisica, Bogota, Colombia; and §Institute of Cognitive Neuroscience and Department of Psychology, University College London, London, England. Send reprint requests to Nicolas Franck, MD, PhD, Institut des Sciences Cognitives (UMR 5015, CNRS & Université Claude Bernard, IFNL), 67 boulevard Pinel 69675 Bron cedex France. E-mail: [email protected]. Copyright © 2005 by Lippincott Williams & Wilkins DOI: 10.1097/01.nmd.0000161699.76032.09 S chizophrenia is particularly characterized by patients’ inability to understand the interaction of different agents (Frith and Frith, 1999). Impaired social relationships are an important part of the schizophrenic clinical presentation and may be consequences of this cognitive-motor deficit. The disturbed interaction between the schizophrenic patient and their environment can be considered as consequences not only of the patients’ beliefs but also of their abnormal feelings (Jaspers, 1922). Verbal hallucinations and delusions of influence are well known examples of schizophrenic pathological experiences. In addition, however, altered time perception is a common experience in schizophrenia and may indeed underlie hallucinations and delusions. Distorted time perception in schizophrenia was described initially by Minkowski (1927). Some patients mention that the course of the time seems modified to them. Furthermore, other patients appear unable to organize their activities in time. They may miss appointments and be unable to organize their daily life adequately (e.g., inversion of circadian rhythm, delayed activities or meals). Both the positive symptoms (e.g., delusions of influence) and the negative ones (e.g., avolition), such as disorganization, have a common point: they express themselves in the field of action. Action occupies a central place in recent theories of schizophrenia. For example, patients with schizophrenia 350 have trouble recognizing actions as their own (Jeannerod et al., 2003) and labeling those sensory events that arise from their own actions (Blakemore et al., 2000). However, the factors that lead subjects to misidentify and misperceive actions have not been fully identified. A possible explanation is that abnormal timing judgment leads to a deficit in action attribution and action perception (Haggard et al., 2003). For example, the normal suppression of sensory consequences of self-produced actions, and the attribution of such consequences to oneself, are known to depend on the time interval between action and effect (Blakemore et al., 1999; Wegner and Wheatley, 1999). Moreover, schizophrenic patients accept that a sensory event is caused by their own action over a wider temporal window than normals (Franck et al., 2001). The present experiment was accordingly designed to study the relation between action and time perception. Our paradigm was based on the paradigm by Libet et al. (1983), as modified by Haggard et al. (1999). A previous experiment using a similar method showed that patients with schizophrenia had strongly anticipatory perception of a sound that followed an action that they had produced themselves. They subjectively associated the two events, implying a subjective time interval shorter than the real one (Haggard et al., 2003). The current experiment was designed to test whether these effects would extend to judgments of other kinds of events and other action contexts. We therefore investigated the temporal representation of passive hand movements that could be triggered by one of several causes (a previous action by the subject herself, a similar action by the experimenter, or simply the computer) in two samples of subjects: one of normal controls and one of patients with schizophrenia. We speculated that patients might differ from controls in the ability to link somatic events such as passive movements with either their own action or the action of another person because of an abnormal model of agency. We expected an abnormal integration of these two sets of events in patients with schizophrenia compared with normal controls. METHODS Subjects In the 24 patients with schizophrenia (diagnosed according to the DSM-IV criteria) who participated in this study, five were eliminated because of the higher SD of their subjective responses, indicating a general inconsistency in the timing judgment task (SD ⬎ 170 milliseconds). The remaining 19 (5 F, 14 M) had a mean age of 33 ⫾ 10 years, one was left-handed, the clinical evaluations values of SAPS (Andreasen, 1984) was 26 ⫾ 24 and SANS (Andreasen, 1983) was 39 ⫾ 11, and the educational level was 11 ⫾ 2 years. All patients were under second-generation antipsychotic treat- The Journal of Nervous and Mental Disease • Volume 193, Number 5, May 2005 The Journal of Nervous and Mental Disease • Volume 193, Number 5, May 2005 ment during the experiment. None received concomitant benzodiazepine or antidepressant medication. All patients were clinically stable at the time of testing. Twenty-four normal controls with no history of neurological or psychiatric disorder participated in this study. They had a mean age of 29 ⫾ 7 years and an educational level of 16 ⫾ 2 years. All subjects gave written informed consent to participate in the study. None of them fulfilled DSM-IV criteria of substance dependence. Apparatus and Procedure Timing judgments were obtained using the method of Libet et al. (1983) adapted by Haggard et al. (1999). Briefly, subjects sat comfortably, facing a computer screen, on which a small clock hand (length, 11 mm) rotated around a conventional 5, 10, 15 . . . minutes scale. The rotation period was 2560 milliseconds. Subjects placed the index of both hands on two button boxes. A semitransparent mirror in front of the screen, at an angle of 45°, allow the subject to see his two hands immediately on either side of the clock (Figure 1). A solenoid (magnetic field generator) was installed in each box. Activating the solenoid under computer control made the corresponding response button move downward under the subject’s passive finger (Haggard et al., 2004). The subject was instructed to judge the subjective time of onset of the fall of the right hand index induced passively by the solenoid in four different conditions. These conditions differed only in the context provided by other events: the right hand’s passive movement was similar throughout: Time of Events in Schizophrenia 1. Baseline: The right response button went down under computer control, producing a passive movement of the right index finger. The left button and hand were completely still throughout. 2. Sequence: After a random period, the left button and left index finger went down under computer control, and the right button and right index finger went down 250 milliseconds later. 3. Agent: The subject pushed the left button with the left index finger at a time of his own free choice, and the right button and right index went down under computer control 250 milliseconds later. 4. Other: The experimenter substituted his left hand for that of the subject on the left button. The experimenter actively pushed the left button at a time of his own free choice. The right button and the subject’s right index went down 250 milliseconds later. After the passive movement of the right index, the clock continued to rotate for a brief random interval and stopped. The subject reported verbally the perceived position of the clock hand at which the right index finger began its passive movement. Each type of judgment was collected in a separate block of 40 trials, and each subject performed the blocks in a different random order. For each trial, a judgment error was calculated as the difference between the perceived time of an event and its actual time of occurrence. A positive judgment error corresponded to a delayed awareness of the passive movement, and a negative judgment error corresponded to an anticipatory awareness. The mean of the 40 judgment errors in each condition was calculated. Subjects with SD higher than 170 milliseconds in at least two conditions were eliminated from the study (five patients), because a large SD reflects a general inconsistency in temporal judgment. Similar criteria have been used in previous studies (Haggard et al., 2002). Data Analysis FIGURE 1. Simplified illustration of the experimental device. © 2005 Lippincott Williams & Wilkins Individual differences in timing judgments are substantial, largely because of how subjects choose to divide attention between the clock and the judged event (Libet et al., 1983). To control for these biases, we subtracted the baseline from the other conditions. The baseline-corrected judgment errors represent the shift in the perceived time of the passive movement of the right hand caused by the previous left hand event generated by the computer, by the subject’s voluntary action, or by the experimenter. Analysis of perceptual shifts in the three conditions was performed using a two-factor mixed ANOVA, with factors of group (between-subjects factor: patients and controls) and condition (within-subjects factor: sequence, agent, other). 351 The Journal of Nervous and Mental Disease • Volume 193, Number 5, May 2005 Franck et al. RESULTS The mean judgment errors and the perceptual shifts calculated with the baseline subtraction are shown in Table 1. The results suggest that the patients with schizophrenia could perform the task quite well, despite the complex cross-modal nature of the timing judgments using the clock and the high level of concentration required for the task. Analysis of the mean error judgments in the baseline condition did not differ between controls and patients (p ⫽ 0.34). For both groups, the judgments were significantly higher than zero (p ⬍ 0.001 for patients; p ⬍ 0.001 for controls), reflecting a delay between the subjective time of the movement and the real time of this event. Values in Table 1 clearly show that, in the patient group, the presence of a previous event in the left hand induced an anticipation (or binding) of the subjective time of the second event. This effect was particularly important for the sequence condition. In the control group, the anticipatory effect was present only in the sequence condition. Statistical ANOVA analysis of the corrected-conditions showed a group effect (F 关1,41兴 ⫽ 4.22; p ⫽ 0.046) and a condition effect (F 关2,82兴 ⫽ 5.86; p ⫽ 0.004. Post hoc analysis revealed a difference between the sequence and the agent conditions (p ⫽ 0.018). No interaction between group and condition factors was observed (F ⫽ 0.2), confirming that the higher binding effect in the patient group was independent of the condition. DISCUSSION The results of the present experiment confirm and generalize those of Haggard et al. (2003). In this previous experiment, it had been shown that patients with schizophrenia bind together their own action and a consequent auditory signal to a greater extent than controls. The present results show that this hyperbinding effect is found for somatic sensory events such as passive movements, as well as auditory events. Moreover, the increased binding in the schizo- TABLE 1. Mean and SD across Subjects in the Two Groups of Subjects for the Four Conditions Conditions Patients Controls 352 Baseline Sequence Agent Other Baseline Sequence Agent Other Mean judgment Mean perceptual shift error (ms) from baseline (ms) 52 ⫾ 49 ⫺19 ⫾ 103 49 ⫾ 110 29 ⫾ 86 37 ⫾ 53 16 ⫾ 90 62 ⫾ 88 51 ⫾ 94 — ⫺71 ⫾ 107 ⫺3 ⫾ 109 ⫺22 ⫾ 83 — ⫺21 ⫾ 72 25 ⫾ 80 14 ⫾ 79 phrenic group was present, and of comparable magnitude, for several different kinds of event pairings, including sequences of somatic sensations, the patient’s own agency, and a social condition in which the patient’s somatic sensations were triggered by the experimenter’s action. We hypothesize that, in real life, this binding between a movement and a previous causal action could impair the identification of the agent of the movement and could produce the feeling of being controlled by others or alien forces that is observed in delusions of influence. In addition, our results showed that the excessive contraction of subjective time in the patient group was a general feature of their perception. This general tendency to underestimate the temporal interval between events could reflect a tendency to overestimate the association between events. Our results can be related to several studies showing abnormal duration judgments in schizophrenia. A number of experiments have suggested that patients with schizophrenia misestimate temporal intervals (Elvevag et al., 2003; Tracy et al., 1998). However, these results point to overestimation or dilation of subjective time, whereas our results point toward underestimation or contraction of subjective time. In another unpublished study of Elvevag et al. (cited in Elvevag et al., 2003), subjects had to reproduce the rhythm of a metronome after its stop. In this experiment, patients with schizophrenia produced a rhythm faster than the metronome’s rhythm, contrary to normal controls. These observations drive us to speculate that, in schizophrenia, time perception or time utilization are abnormal. One possibility would be that time related to perception is slowed down in patients, whereas time related to action may be particularly sped up (Haggard et al., 2003). However, the present results showed the greatest binding effect for the sequence condition, which did not involve voluntary action, casting some doubt on this specific hypothesis. There is general agreement in the literature, however, that the subjective experience of time is altered in schizophrenia. We can interpret subjective time in terms of a continuity of psychological events or representations, each of which is individually discrete. No evidence supports the hypothesis that biological time is abnormal in schizophrenia. We might then speculate that impaired time perception could be based on an abnormal duration of each individual psychological event, or in the number of elementary events that jointly make up a given sequence. In this model, the subjective shortening of time judgments observed in the present experiments might reflect a short cut in the mental composition and representation of sequences and associations in schizophrenia. Our data may be relevant for the elaboration of a model of timing in schizophrenics and even in normal subjects. In particular, the reliable difference in the perceived time of a passive movement according to the context that elicited it suggests that the internal clock of the human scalar timing © 2005 Lippincott Williams & Wilkins The Journal of Nervous and Mental Disease • Volume 193, Number 5, May 2005 system (Wearden and Gringrod, 2003) is not totally selfsufficient but may establish subjective time by taking account of subjects’ behavior and interactions with environment. We suggest that excessive temporal integration may explain other schizophrenic deficits. When the subjective experience of events is excessively integrated, the individual representations of the separate events may be lost. This could, for example, make patients with schizophrenia unable to identify the beginning or the end of an action sequence (Zalla et al., 2004) or to judge the temporal order of actions (Dreher et al., 2001). Consistent with this view, impaired sequencing of actions has indeed been observed in schizophrenia (Zalla et al., 2004). A more general disorganization of behavior could possibly occur as a consequence of this deficit. Equally, if the schizophrenic patient cannot precisely represent the timing of each individual event within the whole sequence, any concepts of the relations between events, such as causation and association, would also be abnormal. A temporal impairment could also underlie the disturbed understanding of others’ actions seen in delusions of persecution and the impaired attribution of action seen in delusions of influence. The fundamental anomaly underlying all these symptoms could then be an excessive integration of sets of elementary events. 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