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Gaze discrimination is unimpaired in schizophrenia
Psychiatry Research 81 Ž1998. 67]75
Gaze discrimination is unimpaired in schizophrenia Nicolas Franck a,U , Elena Daprati b , Franc¸ois Michel c , Mohamed Saoudd , Jean Dalery ´ d,e , Michel Marie-Cardine d,e , Nicolas Georgieff a,e a
Institut des Sciences Cogniti¨ es, CNRS UPR 9075, 67, Bd Pinel 69675 Bron cedex, France Institute of Human Physiology, Uni¨ ersity of Parma, Via Gramsci 14, 43100 Parma, Italy c INSERM U280, Lyon, France d Hopital Le Vinatier,Lyon, France ˆ e Jeune Equipe 1943, Uni¨ ersite´ Claude Bernard, Lyon, France
b
Received 30 December 1997; received in revised form 29 June 1998; accepted 12 July 1998
Abstract Interpersonal communication is largely dependent on interpretation of facial expression and emotion. Difficulties in face processing, and more specifically in gaze discrimination, have been described in schizophrenic patients. According to Baron-Cohen ŽMindblindness. M.I.T. Press, Cambridge, MA, 1995., gaze discrimination relies on the functioning of a specific cognitive module, the Eye Direction Detector ŽEDD.. It has been proposed wRosse et al. Ž1994. Gaze discrimination in patients with schizophrenia: preliminary report. American Journal of Psychiatry 151, 919]921x that an impairment in gaze discrimination is present in schizophrenia, and plays a fundamental role in inducing the paranoid symptoms reported by many patients. However, in the previous studies, gaze direction detection and interpretation of gaze have never been completely dissociated. The present experiment attempts to test the schizophrenics’ skill in a simple gaze direction detection task. A series of photographic portraits of models looking at different directions have been presented to 22 schizophrenic patients and 36 control subjects. For each portrait subjects were asked to determine whether gaze was directed to the right or to the left by pressing a keyboard key. A forced choice paradigm was used. No differences were reported between schizophrenic patients and control subjects. That is, in the present paradigm, schizophrenic patients did not show any specific impairment in detecting the direction of gaze of the portraits. The results are discussed according to the notion that a dissociation is present in schizophrenia between implicit and explicit processes. The present case illustrates how the more automatic elementary functions, such as the detection of gaze direction, may be spared in schizophrenic patients, whereas explicit cognitive functions are likely more affected. Q 1998 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Perception; Eye direction; Automatic processes; Facial expression; Paranoid symptoms; Vision
U
Corresponding author. Fax: q33 437 911210; e-mail: [email protected]
0165-1781r98r$ - see front matter Q 1998 Elsevier Science Ireland Ltd. All rights reserved. PII S0165-1781Ž98.00082-1
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N. Franck et al. r Psychiatry Research 81 (1998) 67]75
1. Introduction It is well known that schizophrenic patients present a broad variety of communication problems ŽAndreasen, 1979., among which language ŽHoffman, 1986. and interaction disorders ŽFrith, 1992. have been largely studied. Several authors ŽFrith and Corcoran, 1996; Sarfati et al., 1997. have related such disturbances, as well as some of the positive symptoms of schizophrenia Že.g. delusions., to an impairment in the patients’ understanding of other people’s intentions. Most information about other people’s mental states is conveyed by facial expression and, very likely, by gaze direction ŽCampbell et al., 1990; Baron-Cohen, 1995.. Therefore a deficit at any of these levels might account for some of the patients’ communication disorders. Difficulties in face processing have been suggested for schizophrenic patients ŽSalem et al., 1996., as well as perception troubles responsible for an abnormal visual scan path in face observation ŽPhillips and David, 1997.. A specific deficit in gaze discrimination has also been hypothesized ŽRosse et al., 1994.. According to Baron-Cohen Ž1995., sensitivity to eye gaze relies on a specific cognitive module Ža specialized part of the human visual system., the Eye Direction Detector ŽEDD., which subserves three main functions. First, the EDD is involved in eyes detection. This capacity emerges very early, as demonstrated by the fact that infants approx. 2 months of age spend significantly more time looking at the eyes than at other parts of the face ŽMaurer, 1985.. Second, the EDD is used in order to establish direction of gaze, and especially to compute whether the eyes one is looking at are directed to the subject or somewhere else, an ability which is completely acquired by 3 years of age ŽBaron-Cohen and Cross, 1992.. Third, the EDD is implied in interpretation of gaze as seeing ŽBaron-Cohen, 1995.. That is, it intervenes in the interpretation of intentions of others, and allows us to establish what another person is interested in, wishes, or thinks when he or she looks at something or at somebody. Gaze discrimination processes have been linked to the activity of specific cells in the superior temporal sulcus ŽSTS., as suggested by clinical
data on prosopagnosic patients ŽPerrett et al., 1988; Campbell et al., 1990., and by neurophysiological evidence from monkey studies ŽPerrett et al., 1985; Perrett et al., 1992.. Neuroimaging studies ŽGur and Pearlson, 1993. and electrophysiological data ŽMcCarley et al., 1993. suggest that anomalies in the STS might be present in schizophrenic patients, thus accounting for disturbances in their gaze discrimination system. Rosse et al. Ž1994. tested subjective impressions concerning gaze discrimination in a group of schizophrenic patients. The authors presented them a series of slides showing portraits of a model, whose head position and gaze direction varied from trial to trial. Subjects were required to judge whether the portrait was looking at them or not. Schizophrenics reported the subjective impression of being looked at by the portraits significantly more often than control subjects. The authors concluded that a specific impairment in gaze detection, possibly linked to an anomaly in the STS, is present in the patients, and that it may be responsible for the paranoid symptoms often reported in schizophrenia. However, it is difficult to assert that a response bias in schizophrenics towards perceiving faces as looking at them results from the deficit of an elementary perceptual module responsible for the detection of eye direction. Rather we suspect such a bias to be the consequence of an impairment at the more complex level of mindreading, responsible for the interpretation of gaze as seeing in terms of mental states. As previously stated, in the model of Baron-Cohen Ž1995., the capacity to detect the direction of the eyes ŽEDD’s second basic function., and consequently to determine whether the eyes are directed towards the subject, is described as an automatic process which operates within very short delays during social interactions ŽPerrett et al., 1988., and which is not necessarily responsible for a conscious experience. On the other hand, interpreting gaze as seeing corresponds to reading gaze in terms of mental states, and should be mostly a conscious process ŽEDD’s third function.. The aim of the present experiment was to test in a more specific way the elementary gaze discrimination system. In other words, we were in-
N. Franck et al. r Psychiatry Research 81 (1998) 67]75
terested in reviewing whether the results by Rosse et al. Ž1994. in schizophrenics apply to the interpretation of gaze, or can be extended to the more basic automatic ability to detect direction of gaze. We predicted that this ability would not be impaired in schizophrenic patients, as most automatic processes are preserved in schizophrenia ŽCallaway and Naghdi, 1982; Dominey and Georgieff, 1997.. In order to test our hypothesis, we devised a simple experimental paradigm in which the analysis of gaze direction, rather than the subjective impression of being looked at, was investigated.
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Table 1 Characteristics of patients with schizophrenia and control subjects; means ŽS.D.. Schizophrenics Ž n s 22.
Normal controls Ž n s 36.
Age
31.5 Ž9.8.
27.7 Ž8.9.
Gender: Male Female
19 3
24 12
Educational level
10.4 Ž2.8.
13.3 Ž3.5.
Illness durationa
10.6 Ž9.1.
]
2.1. Participants
Typeb : Paranoid Undifferentiated Residual
11 9 2
] ] ]
Twenty-two patients and 36 control subjects participated in the study. All signed informed consent before testing.
Medicationc
2. Methods
2.2. Patients A total of 22 inpatients Žhospitalized in the Hospital Le Vinatier, Lyon., 19 males, three females, meeting DSM-IV ŽAmerican Psychiatric Association, 1994. criteria for schizophrenia, participated in the study Žsee Table 1.. Patients were screened for neurological and psychiatric conditions. Exclusion criteria were visual troubles, history of neurological illness or trauma, alcohol or drug dependence according to DSM-IV criteria, and aged over 65 years. The mean age of the schizophrenic patients was 31.5 ŽS.D., 9.8; range, 21]57.. They had a mean educational level of 10.4 years ŽS.D., 2.8; range, 5]16.. The mean average disease duration was 10.6 years ŽS.D., 9.1; range, 1]32.. All patients were receiving antipsychotic medication Žaverage daily chlorpromazine equivalent dose of 371 mg; S.D., 254; range, 0]1080., and were clinically stable at the time of testing. Eleven patients met DSM-IV criteria for paranoid schizophrenia, nine for undifferentiated schizophrenia, and two for residual schizophrenia. The patients’ symptomatology was quantified according to the Brief Psychiatric Rating Scale
371 Ž254.
]
B.P.R.S. score
53.0 Ž13.3.
]
S.A.P.S. score
31.2 Ž18.2.
]
S.A.N.S. score
47.2 Ž21.0.
]
a
Time elapsed since onset of psychotic symptoms. Schizophrenia subtypes ŽDSM-IV.. c Mean dose for the 3 last months Žchlorpromazine equivalents.. b
ŽB.P.R.S., Overall and Gorham, 1962., the Scale for the Assessment of Positive Symptoms ŽS.A.P.S., Andreasen, 1984., and the Scale for the Assessment of Negative Symptoms ŽS.A.N.S., Andreasen, 1983.. Mean scores were 53.0 for the B.P.R.S ŽS.D., 13.3; range, 30]77., 31.2 for the S.A.P.S. ŽS.D., 18.2; range, 6]67., and 47.2 for the S.A.N.S. ŽS.D., 21.0; range, 17]85.. All but two patients were right-handed according to the Edinburgh Inventory ŽOldfield, 1971.. 2.2.1. Control subjects Thirty-six control subjects were recruited from maintenance staff of the hospital, and from students of the Claude Bernard University ŽLyon, France.. There were 24 males and 12 females. Their mean age was 27.7 ŽS.D., 8.9; range, 19]63.,
N. Franck et al. r Psychiatry Research 81 (1998) 67]75
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and their mean educational level was 13.3 years ŽS.D., 3.5; range, 5]18.. Control subjects were excluded if they met DSM-IV criteria for depressive or psychotic syndromes, alcohol or drug dependence, or reported a history of neurological illness or trauma. All but four subjects were right-handed according to the Edinburgh Inventory ŽOldfield, 1971.. In both groups, vision was normal or corrected to normal. A t-test performed on educational levels indicated a significant difference between patients and control subjects Ž Ps 0.002; t s 3.2.. However, no correlation was found between educational level and performance in the experimental test Ž r s 0.3; F s 0.1; Ps 0.1.. 2.3. Apparatus and procedure The experiment was run on a Macintosh 7600r132 computer, equipped with a 17-inch color computer monitor ŽSamsung Syncmaster 17 Gli.. Subjects sat in front of the monitor and positioned their right index finger on the ‘r’ key of the keyboard and their left index finger on the ‘z’ key. The head was not fixed and distance between the eyes and the screen was approx. 70 cm. Stimuli were 30 digitalized color photographic portraits of six models ŽFig. 1.. The models were four males and two females, aged from 20 to 25 years, with a neutral facial expression. All pictures were full-face portraits, regardless of the gaze direction. For each model, five pictures were shown, each presenting one of five different di-
rections of gaze Žy308, y158, 08, 158 and 308.. In other words, five sets of six portraits Žone set for each gaze direction. were shown. The size of each picture was 13 = 15 cm. Each picture was presented at the center of the screen, on a white background. The order of presentation of the 30 pictures was randomized for each subject. In each trial one portrait was presented. Subjects were asked to determine the direction of its gaze by pressing the left key if the portrait was looking to the left, and the right key if the portrait was looking to the right. The instructions for the participants were the following: ‘In each trial, you are going to see one portrait, looking either leftward or rightward. You will have to discriminate whether the gaze of the portrait is directed to your left or to your right. If the portrait looks left, push the ‘z’ key; if the portrait looks right, push the ‘r’ key’. No time limits were fixed, and the picture remained on the screen until a response was given. A forced choice paradigm was used in order to avoid an influence of top-down preconscious perceptual processes on performance ŽFleminger, 1992.. For each subject, four practice trials were run before the experimental session, in order to assess comprehension of the instructions as well as the subject’s ability to detect the models’ eyes. 2.4. Data analysis For each trial, we recorded both the side of the response Žleft or right key. and the corresponding
Fig. 1. Representative example of a set of five portraits Ždirections of gaze: 308 left, 158 left, 08, 158 right, 308 right..
N. Franck et al. r Psychiatry Research 81 (1998) 67]75
response time. For the purpose of the analysis, the mean number of left responses for the five sets of six portraits was computed for each subject. Trials in which response times were faster than 200 ms Ž0.001% of total. or in which subjects stopped during the experiment for any reason Ž0.01%. were considered as errors and were excluded from analysis. Due to the small number of trials and to the peculiar nature of the analyzed variable, a nonparametric statistical approach was preferred. The number of left responses reported by schizophrenic patients for each gaze orientation was compared to that of control subjects by means of separate Mann]Whitney U-tests. Within the schizophrenic group, performance of patients experiencing paranoid symptoms Ž n s 11. was compared to that of undifferentiated and residual patients Ž n s 11.. As no time constraints were imposed for the response, a large variability was present in response time values. For the purpose of the analysis, response times were normalized by using logarithmic transformation. Transformed values were submitted to an ANOVA, whose factors were as follows: between-subjects factor } Group ŽPatients vs. Control subjects.; within-subjects factor } Gaze Orientation Žleft 308, left 158, 08, right 308, right 158.. 3. Results The mean numbers of left responses recorded for each direction of gaze did not significantly differ between patients and control subjects Žleft:
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308, Us 278.0, zs 1.89, Ps 0.059; 158, Us 324.5, z s 1.14, P s 0.25; right: 308, U s 326.0, z s y1.12, Ps 0.26; 158, Us 370.5, zs y0.41, Ps 0.68; center: 08, Us 358.5, z s 0.60, Ps 0.55; see Table 2 for numerical values .. That is, schizophrenic patients, as well as normal control subjects, correctly responded by pressing the right key for rightward gaze directions, and the left key for leftward directions. Due to the forced choice paradigm, responses were equally distributed between the left and the right keys in both groups when the portraits were looking straight ahead Ž08 condition.. This behavior was observed in both control subjects and schizophrenic patients ŽFig. 2.. The non-significant difference in the performance between patients and control subjects was clear for all but one condition Ž308 right.. Being an extreme direction, and likely an easy one, the slight trend toward significance was investigated, and a power analysis was run in order to exclude that the result was due to a sample effect. Effect size was estimated according to Cohen Ž1988. as a medium effect size Ž ds 0.68.. In order to reach a reliable power Ž1 y b s 0.8., a sample of 25 subjects in each group is required. Dealing with unequal groups, we computed the harmonic mean for our sample, which emerged to be slightly larger Ž27.5. than the required one. Therefore we feel rather confident that negative results were not due to sample size. Within the patients’ group, the performance of paranoid patients did not differ from that of undifferentiated and residual ones for all gaze orientations Žleft: 308, Us 46.0, z s y0.95, Ps 0.34; 158, Us 54.5, z s 0.39, Ps
Table 2 Percentages of left- and right-key responses for normal subjects and schizophrenic patients in the gaze discrimination task 308 Left
158 Left
08
158 Right
308 Right
Controls
Left-key responses Right-key responses S.D.
96.8 3.2 0.06
81.5 18.5 0.17
48.8 51.2 0.25
3.8 96.2 0.07
0.9 99.1 0.04
Patients
Left-key responses Right-key responses S.D.
92.1 7.9 0.08
75.2 24.8 0.20
46.6 53.4 0.28
6.2 93.8 0.12
4.7 95.3 0.09
N. Franck et al. r Psychiatry Research 81 (1998) 67]75
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Fig. 2. Percentages of left key responses observed for control subjects and schizophrenic patients for the five directions of gaze.
0.69; right: 308, Us 43.0, zs 1.14, Ps 0.25; 158, Us 51.0, z s 0.62, Ps 0.53; center: 08, Us 36.5, zs y1.57, Ps 0.11.. Response times were recorded. Means and variability data are reported in Table 3. Overall, schizophrenic patients were significantly slower than control subjects Žpatients 1649.8 ms, control subjects 1385.8 ms, F1,56 s 4.31; P- 0.04., but distribution of response times across conditions was similar in the two groups Žsee Fig. 3.. Indeed, the interaction between group and orientation was not significant in the ANOVA.
Table 3 Mean response times ŽS.D.. for controls ŽC. and schizophrenic patients ŽPt. in the gaze discrimination task Žscores in ms. 308 Left
158 Left
08
158 Right 308 Right
C 965 Ž339. 1818 Ž862. 1997 Ž1168. 1275 Ž615. 874 Ž227. Pt 1243 Ž497. 1938 Ž1066. 2350 Ž1371. 1466 Ž697. 1252 Ž611.
4. Discussion Rather surprisingly, schizophrenic patients are not impaired in the gaze discrimination task used in the present study. When the mean number of left responses is considered, no significant differences are found for the five directions of gaze between schizophrenic patients and normal control subjects. This finding seems to be at odds with data from Rosse et al. Ž1994.. These authors used a different type of discrimination task in which subjects were required to report whether portraits presented on a screen were looking at them or not. Rosse et al. demonstrated that schizophrenic patients presented significantly different performance profiles with respect to control subjects and produced different types of errors. Patients with schizophrenia, and among them especially those with paranoid symptoms, often reported the
N. Franck et al. r Psychiatry Research 81 (1998) 67]75
Fig. 3. Response times ŽS.D.. observed for control subjects and schizophrenic patients for the five directions of gaze.
portraits as looking at them even when in fact they were staring elsewhere. The authors hypothesized that the patients’ performance reflects more subtle insults to the human equivalent of the monkey STS than that found in neurological patients ŽCampbell et al., 1990.. It is possible that our results differ from those of Rosse et al. because a different experimental sample was tested. That is, the dysfunction in the gaze direction detection system may be specific for a peculiar subtype of schizophrenic patients. However, our sample, like those of Rosse et al., included both paranoid and non-paranoid patients; therefore we can exclude that the different sample composition is responsible for the different results. An alternative possibility is that the different pattern of results found in our experiment likely relies on two methodological differences in the paradigm. First, the task for the subjects differed in the two experiments: in Rosse’s experiment, subjects were required to decide whether the portrait on the screen was looking at them or not. On the contrary, in our task, subjects were simply required to state whether gaze was directed to the right or to the left. No explicit judgment was required as to whom or what the gaze was directed. Therefore we can assume that the present paradigm investigated the functioning of a more basic process than that tested by Rosse et al. The
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overlap between the pattern of response shown by patients and control subjects excludes that this process might be impaired in the former. Second, in Rosse’s experiment subjects answered the question as to whether the gaze of the portrait was directed towards them or not, and a bias towards the central direction was found. In our task, a ‘left vs. right’ forced choice was required, and no central key was provided for the response. Therefore if a bias exists for the central direction, it can be investigated only indirectly. That is, if patients experience the subjective impression of being looked at by the portraits, a bias towards the central direction should be expressed by a reduced number of correct responses in the conditions of left and right gaze orientations, and most likely, in the less extreme ones. Indeed, patients should respond to these directions with a similar hesitation to that experienced in the central one. This is clearly not the case: the number of errors reported for the lateral gaze orientations is very low, and does not differ from that of control subjects. In order to account for our and Rosse’s data, we suggest that the conscious feeling of being looked at and the more automatic process of gaze detection represent different functions Žlikely interdependent rather than independent. of the EDD module ŽBaron-Cohen, 1995.. We assume that the paradigm used in the present experiment activates the most basic function of the EDD system, which appears to be unimpaired in the patients. Interpretation of gaze as seeing has not presently been tested, and according to Rosse et al., might be more severely affected by schizophrenia. Indeed, if we assume the existence of a deficit in the gaze discrimination system in schizophrenic patients, we should find a difference in their response patterns with respect to control subjects in a task of simple eye-direction detection like the one used in the present experiment. Even though null results must be interpreted with caution, the overlap between the performance of the two groups suggests that the most basic functions of the EDD module are likely spared in schizophrenia. Undoubtedly, patients are slower than control subjects, but the behavior of the two groups is almost identical.
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Indeed, when no explicit discrimination as to whom the portrait is looking at is required, patients are unimpaired. This result is consistent with the observation by Rosse et al. Ž1994. that total gaze discrimination scores do not differ between groups Žalthough mean total gaze scores were lower in the schizophrenic patients than in the control subjects.. Patients with schizophrenia and control subjects did not differ significantly in the overall number of total correct responses. Furthermore, our data are consistent with those reporting that basic cognitive processes are unimpaired in schizophrenia, whereas explicit processes are extensively affected ŽCallaway and Naghdi, 1982; Dominey and Georgieff, 1997.. It has been recently suggested ŽGarety et al., 1991; Phillips and David, 1997. that schizophrenic patients often present a ‘jumping to conclusions’ style of information processing. In the present case, it can be assumed that whereas gaze direction detection is spared, interpretation of the meaning of such a direction is abnormal in the patients. According to Frith Ž1992., an impairment in interpreting other people’s mental states or intentions could be an important mechanism of schizophrenic symptoms. It has still to be defined whether this impairment derives from a deficit in the automatic processes involved in perception, as suggested by Frith Ž1992., or is a consequence of more specific deficits in conscious processes ŽDaprati et al., 1997.. Our results suggest that in schizophrenia an impairment is present in gaze interpretation rather than in gaze direction detection. Further studies on gaze discrimination could provide useful data on the role of elementary perceptive deficits Žif present. in the interpretation of other people’s mental states, and may cast light on the mechanisms responsible for symptoms like paranoia and delusions. Acknowledgements We thank James Intriligator for the photographic portraits, and Drs. T. d’Amato, J. Furtos, G. Burloux, J. Dubuis, A. Parriaud and B. Stalloni for referring the patients to us. We are grateful to T. Montoute, Dr. L. Craighero and Dr. L. Riggio
for comments on an earlier version of the manuscript. References American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th ed. American Psychiatric Press, Washington, DC. Andreasen, N.C., 1979. Thought, language, and communication disorders: I. Clinical assessment, definition of terms, and evaluation of their reliability. Archives of General Psychiatry 39, 1315]1321. Andreasen, N.C., 1983. The Scale for the Assessment of Negative Symptoms ŽSANS.. The University of Iowa, Iowa City, IA. Andreasen, N.C., 1984. The Scale for the Assessment of Positive Symptoms ŽSAPS.. The University of Iowa, Iowa City, IA. Baron-Cohen, S., 1995. Mindblindness. M.I.T. Press, Cambridge, MA. Baron-Cohen, S., Cross, P., 1992. Reading the eyes: evidence for the role of perception in the development of theory of mind. Mind and Language 6, 173]186. Campbell, R., Heywood, C.A., Cowey, A., Regard, M., Landis, T., 1990. Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation. Neuropsychologia 28, 1123]1142. Callaway, E., Naghdi, S., 1982. An information processing model for schizophrenia. Archives of General Psychiatry 39, 339]347. Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates, Hillsdale, NJ. Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, ´ J., Jeannerod, M., 1997. Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition 65, 71]96. Dominey, P.F., Georgieff, N., 1997. Schizophrenics learn surface but not abstract structure in a serial reaction time task. NeuroReport 8, 2877]2882. Fleminger, S., 1992. Seeing is believing: the role of ‘preconscious’ perceptual processing in delusional misidentification. British Journal of Psychiatry 160, 293]303. Frith, C.D., 1992. The Cognitive Neuropsychology of Schizophrenia. Lawrence Erlbaum Associates, Hillsdale, NJ. Frith, C.D., Corcoran, R., 1996. Exploring ‘theory of mind’ in people with schizophrenia. Psychological Medicine 26, 521]530. Garety, P.A., Hemsley, D.R., Wessely, S., 1991. Reasoning in deluded and paranoid patients. Biases in performance on a probabilistic inference task. Journal of Nervous and Mental Disease 179, 194]201. Gur, R.E., Pearlson, G.D., 1993. Neuroimaging in schizophrenia research. Schizophrenia Bulletin 19, 337]353. Hoffman, R.E., 1986. Verbal hallucinations and language pro-
N. Franck et al. r Psychiatry Research 81 (1998) 67]75 duction processes in schizophrenia. Behavioral and Brain Sciences 9, 503]548. Maurer, D., 1985. Infants’ perception of facedness. In: Field, T., Fox, N. ŽEds.., Social Perception in Infants. Ablex. McCarley, R.W., Shenton, M.E., O’Donnell, B.F., Faux, S.F., Kikinis, R., Nestor, P.G., Jolesz, F.A., 1993. Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. Archives of General Psychiatry 50, 190]197. Oldfield, R.C., 1971. The assessment and analysis of handedness. Neuropsychologia 9, 97]113. Overall, J.E., Gorham, D.R., 1962. The Brief Psychiatric Rating Scale. Psychological Reports 10, 799]812. Perrett, D.I., Smith, P.A.J., Potter, D.D., Mistlin, A.J., Head, A.S., Milner, A.D., Jeeves, M.A., 1985. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proceedings of the Royal Society of London B 223, 293]317. Perrett, D.I., Mistlin, A.J., Chitty, A.J., Harries, M., Newscombe, F., de Haan, E., 1988. Neuronal mechanisms of face perception and their pathology. In: Kennard, C., Clifford Rose, F. ŽEds.., Physiological Aspects of Clinical NeuroOphthalmology. Chapman and Hall, London, pp. 137]154.
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Perrett, D.I., Hietanen, M., Oram, M.W., Benson, P.J., 1992. Organization and functions of cells responsive to faces in the temporal cortex. Proceedings of the Royal Society of London B 335, 23]30. Phillips, M.L., David, A.S., 1997. Visual scan paths are abnormal in deluded schizophrenics. Neuropsychologia 35, 99]105. Rosse, R.B., Kendrick, K., Wyatt, R.J., Isaac, A., Deutsch, S.I., 1994. Gaze discrimination in patients with schizophrenia: preliminary report. American Journal of Psychiatry 151, 919]921. Salem, J.E., Kring, A.M., Kerr, S.L., 1996. More evidence for generalized poor performance in facial emotion perception in schizophrenia. Journal of Abnormal Psychology 105, 480]483. Sarfati, Y., Hardy-Bayle, ´ M.-C., Nadel, J., Chevalier, J.-F., Widlocher, D., 1997. Attribution of mental states to others ¨ by schizophrenic patients. Cognitive Neuropsychiatry 2, 1]17.
Gaze discrimination is unimpaired in schizophrenia Nicolas Franck a,U , Elena Daprati b , Franc¸ois Michel c , Mohamed Saoudd , Jean Dalery ´ d,e , Michel Marie-Cardine d,e , Nicolas Georgieff a,e a
Institut des Sciences Cogniti¨ es, CNRS UPR 9075, 67, Bd Pinel 69675 Bron cedex, France Institute of Human Physiology, Uni¨ ersity of Parma, Via Gramsci 14, 43100 Parma, Italy c INSERM U280, Lyon, France d Hopital Le Vinatier,Lyon, France ˆ e Jeune Equipe 1943, Uni¨ ersite´ Claude Bernard, Lyon, France
b
Received 30 December 1997; received in revised form 29 June 1998; accepted 12 July 1998
Abstract Interpersonal communication is largely dependent on interpretation of facial expression and emotion. Difficulties in face processing, and more specifically in gaze discrimination, have been described in schizophrenic patients. According to Baron-Cohen ŽMindblindness. M.I.T. Press, Cambridge, MA, 1995., gaze discrimination relies on the functioning of a specific cognitive module, the Eye Direction Detector ŽEDD.. It has been proposed wRosse et al. Ž1994. Gaze discrimination in patients with schizophrenia: preliminary report. American Journal of Psychiatry 151, 919]921x that an impairment in gaze discrimination is present in schizophrenia, and plays a fundamental role in inducing the paranoid symptoms reported by many patients. However, in the previous studies, gaze direction detection and interpretation of gaze have never been completely dissociated. The present experiment attempts to test the schizophrenics’ skill in a simple gaze direction detection task. A series of photographic portraits of models looking at different directions have been presented to 22 schizophrenic patients and 36 control subjects. For each portrait subjects were asked to determine whether gaze was directed to the right or to the left by pressing a keyboard key. A forced choice paradigm was used. No differences were reported between schizophrenic patients and control subjects. That is, in the present paradigm, schizophrenic patients did not show any specific impairment in detecting the direction of gaze of the portraits. The results are discussed according to the notion that a dissociation is present in schizophrenia between implicit and explicit processes. The present case illustrates how the more automatic elementary functions, such as the detection of gaze direction, may be spared in schizophrenic patients, whereas explicit cognitive functions are likely more affected. Q 1998 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Perception; Eye direction; Automatic processes; Facial expression; Paranoid symptoms; Vision
U
Corresponding author. Fax: q33 437 911210; e-mail: [email protected]
0165-1781r98r$ - see front matter Q 1998 Elsevier Science Ireland Ltd. All rights reserved. PII S0165-1781Ž98.00082-1
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1. Introduction It is well known that schizophrenic patients present a broad variety of communication problems ŽAndreasen, 1979., among which language ŽHoffman, 1986. and interaction disorders ŽFrith, 1992. have been largely studied. Several authors ŽFrith and Corcoran, 1996; Sarfati et al., 1997. have related such disturbances, as well as some of the positive symptoms of schizophrenia Že.g. delusions., to an impairment in the patients’ understanding of other people’s intentions. Most information about other people’s mental states is conveyed by facial expression and, very likely, by gaze direction ŽCampbell et al., 1990; Baron-Cohen, 1995.. Therefore a deficit at any of these levels might account for some of the patients’ communication disorders. Difficulties in face processing have been suggested for schizophrenic patients ŽSalem et al., 1996., as well as perception troubles responsible for an abnormal visual scan path in face observation ŽPhillips and David, 1997.. A specific deficit in gaze discrimination has also been hypothesized ŽRosse et al., 1994.. According to Baron-Cohen Ž1995., sensitivity to eye gaze relies on a specific cognitive module Ža specialized part of the human visual system., the Eye Direction Detector ŽEDD., which subserves three main functions. First, the EDD is involved in eyes detection. This capacity emerges very early, as demonstrated by the fact that infants approx. 2 months of age spend significantly more time looking at the eyes than at other parts of the face ŽMaurer, 1985.. Second, the EDD is used in order to establish direction of gaze, and especially to compute whether the eyes one is looking at are directed to the subject or somewhere else, an ability which is completely acquired by 3 years of age ŽBaron-Cohen and Cross, 1992.. Third, the EDD is implied in interpretation of gaze as seeing ŽBaron-Cohen, 1995.. That is, it intervenes in the interpretation of intentions of others, and allows us to establish what another person is interested in, wishes, or thinks when he or she looks at something or at somebody. Gaze discrimination processes have been linked to the activity of specific cells in the superior temporal sulcus ŽSTS., as suggested by clinical
data on prosopagnosic patients ŽPerrett et al., 1988; Campbell et al., 1990., and by neurophysiological evidence from monkey studies ŽPerrett et al., 1985; Perrett et al., 1992.. Neuroimaging studies ŽGur and Pearlson, 1993. and electrophysiological data ŽMcCarley et al., 1993. suggest that anomalies in the STS might be present in schizophrenic patients, thus accounting for disturbances in their gaze discrimination system. Rosse et al. Ž1994. tested subjective impressions concerning gaze discrimination in a group of schizophrenic patients. The authors presented them a series of slides showing portraits of a model, whose head position and gaze direction varied from trial to trial. Subjects were required to judge whether the portrait was looking at them or not. Schizophrenics reported the subjective impression of being looked at by the portraits significantly more often than control subjects. The authors concluded that a specific impairment in gaze detection, possibly linked to an anomaly in the STS, is present in the patients, and that it may be responsible for the paranoid symptoms often reported in schizophrenia. However, it is difficult to assert that a response bias in schizophrenics towards perceiving faces as looking at them results from the deficit of an elementary perceptual module responsible for the detection of eye direction. Rather we suspect such a bias to be the consequence of an impairment at the more complex level of mindreading, responsible for the interpretation of gaze as seeing in terms of mental states. As previously stated, in the model of Baron-Cohen Ž1995., the capacity to detect the direction of the eyes ŽEDD’s second basic function., and consequently to determine whether the eyes are directed towards the subject, is described as an automatic process which operates within very short delays during social interactions ŽPerrett et al., 1988., and which is not necessarily responsible for a conscious experience. On the other hand, interpreting gaze as seeing corresponds to reading gaze in terms of mental states, and should be mostly a conscious process ŽEDD’s third function.. The aim of the present experiment was to test in a more specific way the elementary gaze discrimination system. In other words, we were in-
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terested in reviewing whether the results by Rosse et al. Ž1994. in schizophrenics apply to the interpretation of gaze, or can be extended to the more basic automatic ability to detect direction of gaze. We predicted that this ability would not be impaired in schizophrenic patients, as most automatic processes are preserved in schizophrenia ŽCallaway and Naghdi, 1982; Dominey and Georgieff, 1997.. In order to test our hypothesis, we devised a simple experimental paradigm in which the analysis of gaze direction, rather than the subjective impression of being looked at, was investigated.
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Table 1 Characteristics of patients with schizophrenia and control subjects; means ŽS.D.. Schizophrenics Ž n s 22.
Normal controls Ž n s 36.
Age
31.5 Ž9.8.
27.7 Ž8.9.
Gender: Male Female
19 3
24 12
Educational level
10.4 Ž2.8.
13.3 Ž3.5.
Illness durationa
10.6 Ž9.1.
]
2.1. Participants
Typeb : Paranoid Undifferentiated Residual
11 9 2
] ] ]
Twenty-two patients and 36 control subjects participated in the study. All signed informed consent before testing.
Medicationc
2. Methods
2.2. Patients A total of 22 inpatients Žhospitalized in the Hospital Le Vinatier, Lyon., 19 males, three females, meeting DSM-IV ŽAmerican Psychiatric Association, 1994. criteria for schizophrenia, participated in the study Žsee Table 1.. Patients were screened for neurological and psychiatric conditions. Exclusion criteria were visual troubles, history of neurological illness or trauma, alcohol or drug dependence according to DSM-IV criteria, and aged over 65 years. The mean age of the schizophrenic patients was 31.5 ŽS.D., 9.8; range, 21]57.. They had a mean educational level of 10.4 years ŽS.D., 2.8; range, 5]16.. The mean average disease duration was 10.6 years ŽS.D., 9.1; range, 1]32.. All patients were receiving antipsychotic medication Žaverage daily chlorpromazine equivalent dose of 371 mg; S.D., 254; range, 0]1080., and were clinically stable at the time of testing. Eleven patients met DSM-IV criteria for paranoid schizophrenia, nine for undifferentiated schizophrenia, and two for residual schizophrenia. The patients’ symptomatology was quantified according to the Brief Psychiatric Rating Scale
371 Ž254.
]
B.P.R.S. score
53.0 Ž13.3.
]
S.A.P.S. score
31.2 Ž18.2.
]
S.A.N.S. score
47.2 Ž21.0.
]
a
Time elapsed since onset of psychotic symptoms. Schizophrenia subtypes ŽDSM-IV.. c Mean dose for the 3 last months Žchlorpromazine equivalents.. b
ŽB.P.R.S., Overall and Gorham, 1962., the Scale for the Assessment of Positive Symptoms ŽS.A.P.S., Andreasen, 1984., and the Scale for the Assessment of Negative Symptoms ŽS.A.N.S., Andreasen, 1983.. Mean scores were 53.0 for the B.P.R.S ŽS.D., 13.3; range, 30]77., 31.2 for the S.A.P.S. ŽS.D., 18.2; range, 6]67., and 47.2 for the S.A.N.S. ŽS.D., 21.0; range, 17]85.. All but two patients were right-handed according to the Edinburgh Inventory ŽOldfield, 1971.. 2.2.1. Control subjects Thirty-six control subjects were recruited from maintenance staff of the hospital, and from students of the Claude Bernard University ŽLyon, France.. There were 24 males and 12 females. Their mean age was 27.7 ŽS.D., 8.9; range, 19]63.,
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and their mean educational level was 13.3 years ŽS.D., 3.5; range, 5]18.. Control subjects were excluded if they met DSM-IV criteria for depressive or psychotic syndromes, alcohol or drug dependence, or reported a history of neurological illness or trauma. All but four subjects were right-handed according to the Edinburgh Inventory ŽOldfield, 1971.. In both groups, vision was normal or corrected to normal. A t-test performed on educational levels indicated a significant difference between patients and control subjects Ž Ps 0.002; t s 3.2.. However, no correlation was found between educational level and performance in the experimental test Ž r s 0.3; F s 0.1; Ps 0.1.. 2.3. Apparatus and procedure The experiment was run on a Macintosh 7600r132 computer, equipped with a 17-inch color computer monitor ŽSamsung Syncmaster 17 Gli.. Subjects sat in front of the monitor and positioned their right index finger on the ‘r’ key of the keyboard and their left index finger on the ‘z’ key. The head was not fixed and distance between the eyes and the screen was approx. 70 cm. Stimuli were 30 digitalized color photographic portraits of six models ŽFig. 1.. The models were four males and two females, aged from 20 to 25 years, with a neutral facial expression. All pictures were full-face portraits, regardless of the gaze direction. For each model, five pictures were shown, each presenting one of five different di-
rections of gaze Žy308, y158, 08, 158 and 308.. In other words, five sets of six portraits Žone set for each gaze direction. were shown. The size of each picture was 13 = 15 cm. Each picture was presented at the center of the screen, on a white background. The order of presentation of the 30 pictures was randomized for each subject. In each trial one portrait was presented. Subjects were asked to determine the direction of its gaze by pressing the left key if the portrait was looking to the left, and the right key if the portrait was looking to the right. The instructions for the participants were the following: ‘In each trial, you are going to see one portrait, looking either leftward or rightward. You will have to discriminate whether the gaze of the portrait is directed to your left or to your right. If the portrait looks left, push the ‘z’ key; if the portrait looks right, push the ‘r’ key’. No time limits were fixed, and the picture remained on the screen until a response was given. A forced choice paradigm was used in order to avoid an influence of top-down preconscious perceptual processes on performance ŽFleminger, 1992.. For each subject, four practice trials were run before the experimental session, in order to assess comprehension of the instructions as well as the subject’s ability to detect the models’ eyes. 2.4. Data analysis For each trial, we recorded both the side of the response Žleft or right key. and the corresponding
Fig. 1. Representative example of a set of five portraits Ždirections of gaze: 308 left, 158 left, 08, 158 right, 308 right..
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response time. For the purpose of the analysis, the mean number of left responses for the five sets of six portraits was computed for each subject. Trials in which response times were faster than 200 ms Ž0.001% of total. or in which subjects stopped during the experiment for any reason Ž0.01%. were considered as errors and were excluded from analysis. Due to the small number of trials and to the peculiar nature of the analyzed variable, a nonparametric statistical approach was preferred. The number of left responses reported by schizophrenic patients for each gaze orientation was compared to that of control subjects by means of separate Mann]Whitney U-tests. Within the schizophrenic group, performance of patients experiencing paranoid symptoms Ž n s 11. was compared to that of undifferentiated and residual patients Ž n s 11.. As no time constraints were imposed for the response, a large variability was present in response time values. For the purpose of the analysis, response times were normalized by using logarithmic transformation. Transformed values were submitted to an ANOVA, whose factors were as follows: between-subjects factor } Group ŽPatients vs. Control subjects.; within-subjects factor } Gaze Orientation Žleft 308, left 158, 08, right 308, right 158.. 3. Results The mean numbers of left responses recorded for each direction of gaze did not significantly differ between patients and control subjects Žleft:
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308, Us 278.0, zs 1.89, Ps 0.059; 158, Us 324.5, z s 1.14, P s 0.25; right: 308, U s 326.0, z s y1.12, Ps 0.26; 158, Us 370.5, zs y0.41, Ps 0.68; center: 08, Us 358.5, z s 0.60, Ps 0.55; see Table 2 for numerical values .. That is, schizophrenic patients, as well as normal control subjects, correctly responded by pressing the right key for rightward gaze directions, and the left key for leftward directions. Due to the forced choice paradigm, responses were equally distributed between the left and the right keys in both groups when the portraits were looking straight ahead Ž08 condition.. This behavior was observed in both control subjects and schizophrenic patients ŽFig. 2.. The non-significant difference in the performance between patients and control subjects was clear for all but one condition Ž308 right.. Being an extreme direction, and likely an easy one, the slight trend toward significance was investigated, and a power analysis was run in order to exclude that the result was due to a sample effect. Effect size was estimated according to Cohen Ž1988. as a medium effect size Ž ds 0.68.. In order to reach a reliable power Ž1 y b s 0.8., a sample of 25 subjects in each group is required. Dealing with unequal groups, we computed the harmonic mean for our sample, which emerged to be slightly larger Ž27.5. than the required one. Therefore we feel rather confident that negative results were not due to sample size. Within the patients’ group, the performance of paranoid patients did not differ from that of undifferentiated and residual ones for all gaze orientations Žleft: 308, Us 46.0, z s y0.95, Ps 0.34; 158, Us 54.5, z s 0.39, Ps
Table 2 Percentages of left- and right-key responses for normal subjects and schizophrenic patients in the gaze discrimination task 308 Left
158 Left
08
158 Right
308 Right
Controls
Left-key responses Right-key responses S.D.
96.8 3.2 0.06
81.5 18.5 0.17
48.8 51.2 0.25
3.8 96.2 0.07
0.9 99.1 0.04
Patients
Left-key responses Right-key responses S.D.
92.1 7.9 0.08
75.2 24.8 0.20
46.6 53.4 0.28
6.2 93.8 0.12
4.7 95.3 0.09
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Fig. 2. Percentages of left key responses observed for control subjects and schizophrenic patients for the five directions of gaze.
0.69; right: 308, Us 43.0, zs 1.14, Ps 0.25; 158, Us 51.0, z s 0.62, Ps 0.53; center: 08, Us 36.5, zs y1.57, Ps 0.11.. Response times were recorded. Means and variability data are reported in Table 3. Overall, schizophrenic patients were significantly slower than control subjects Žpatients 1649.8 ms, control subjects 1385.8 ms, F1,56 s 4.31; P- 0.04., but distribution of response times across conditions was similar in the two groups Žsee Fig. 3.. Indeed, the interaction between group and orientation was not significant in the ANOVA.
Table 3 Mean response times ŽS.D.. for controls ŽC. and schizophrenic patients ŽPt. in the gaze discrimination task Žscores in ms. 308 Left
158 Left
08
158 Right 308 Right
C 965 Ž339. 1818 Ž862. 1997 Ž1168. 1275 Ž615. 874 Ž227. Pt 1243 Ž497. 1938 Ž1066. 2350 Ž1371. 1466 Ž697. 1252 Ž611.
4. Discussion Rather surprisingly, schizophrenic patients are not impaired in the gaze discrimination task used in the present study. When the mean number of left responses is considered, no significant differences are found for the five directions of gaze between schizophrenic patients and normal control subjects. This finding seems to be at odds with data from Rosse et al. Ž1994.. These authors used a different type of discrimination task in which subjects were required to report whether portraits presented on a screen were looking at them or not. Rosse et al. demonstrated that schizophrenic patients presented significantly different performance profiles with respect to control subjects and produced different types of errors. Patients with schizophrenia, and among them especially those with paranoid symptoms, often reported the
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Fig. 3. Response times ŽS.D.. observed for control subjects and schizophrenic patients for the five directions of gaze.
portraits as looking at them even when in fact they were staring elsewhere. The authors hypothesized that the patients’ performance reflects more subtle insults to the human equivalent of the monkey STS than that found in neurological patients ŽCampbell et al., 1990.. It is possible that our results differ from those of Rosse et al. because a different experimental sample was tested. That is, the dysfunction in the gaze direction detection system may be specific for a peculiar subtype of schizophrenic patients. However, our sample, like those of Rosse et al., included both paranoid and non-paranoid patients; therefore we can exclude that the different sample composition is responsible for the different results. An alternative possibility is that the different pattern of results found in our experiment likely relies on two methodological differences in the paradigm. First, the task for the subjects differed in the two experiments: in Rosse’s experiment, subjects were required to decide whether the portrait on the screen was looking at them or not. On the contrary, in our task, subjects were simply required to state whether gaze was directed to the right or to the left. No explicit judgment was required as to whom or what the gaze was directed. Therefore we can assume that the present paradigm investigated the functioning of a more basic process than that tested by Rosse et al. The
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overlap between the pattern of response shown by patients and control subjects excludes that this process might be impaired in the former. Second, in Rosse’s experiment subjects answered the question as to whether the gaze of the portrait was directed towards them or not, and a bias towards the central direction was found. In our task, a ‘left vs. right’ forced choice was required, and no central key was provided for the response. Therefore if a bias exists for the central direction, it can be investigated only indirectly. That is, if patients experience the subjective impression of being looked at by the portraits, a bias towards the central direction should be expressed by a reduced number of correct responses in the conditions of left and right gaze orientations, and most likely, in the less extreme ones. Indeed, patients should respond to these directions with a similar hesitation to that experienced in the central one. This is clearly not the case: the number of errors reported for the lateral gaze orientations is very low, and does not differ from that of control subjects. In order to account for our and Rosse’s data, we suggest that the conscious feeling of being looked at and the more automatic process of gaze detection represent different functions Žlikely interdependent rather than independent. of the EDD module ŽBaron-Cohen, 1995.. We assume that the paradigm used in the present experiment activates the most basic function of the EDD system, which appears to be unimpaired in the patients. Interpretation of gaze as seeing has not presently been tested, and according to Rosse et al., might be more severely affected by schizophrenia. Indeed, if we assume the existence of a deficit in the gaze discrimination system in schizophrenic patients, we should find a difference in their response patterns with respect to control subjects in a task of simple eye-direction detection like the one used in the present experiment. Even though null results must be interpreted with caution, the overlap between the performance of the two groups suggests that the most basic functions of the EDD module are likely spared in schizophrenia. Undoubtedly, patients are slower than control subjects, but the behavior of the two groups is almost identical.
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Indeed, when no explicit discrimination as to whom the portrait is looking at is required, patients are unimpaired. This result is consistent with the observation by Rosse et al. Ž1994. that total gaze discrimination scores do not differ between groups Žalthough mean total gaze scores were lower in the schizophrenic patients than in the control subjects.. Patients with schizophrenia and control subjects did not differ significantly in the overall number of total correct responses. Furthermore, our data are consistent with those reporting that basic cognitive processes are unimpaired in schizophrenia, whereas explicit processes are extensively affected ŽCallaway and Naghdi, 1982; Dominey and Georgieff, 1997.. It has been recently suggested ŽGarety et al., 1991; Phillips and David, 1997. that schizophrenic patients often present a ‘jumping to conclusions’ style of information processing. In the present case, it can be assumed that whereas gaze direction detection is spared, interpretation of the meaning of such a direction is abnormal in the patients. According to Frith Ž1992., an impairment in interpreting other people’s mental states or intentions could be an important mechanism of schizophrenic symptoms. It has still to be defined whether this impairment derives from a deficit in the automatic processes involved in perception, as suggested by Frith Ž1992., or is a consequence of more specific deficits in conscious processes ŽDaprati et al., 1997.. Our results suggest that in schizophrenia an impairment is present in gaze interpretation rather than in gaze direction detection. Further studies on gaze discrimination could provide useful data on the role of elementary perceptive deficits Žif present. in the interpretation of other people’s mental states, and may cast light on the mechanisms responsible for symptoms like paranoia and delusions. Acknowledgements We thank James Intriligator for the photographic portraits, and Drs. T. d’Amato, J. Furtos, G. Burloux, J. Dubuis, A. Parriaud and B. Stalloni for referring the patients to us. We are grateful to T. Montoute, Dr. L. Craighero and Dr. L. Riggio
for comments on an earlier version of the manuscript. References American Psychiatric Association, 1994. Diagnostic and Statistical Manual of Mental Disorders, 4th ed. American Psychiatric Press, Washington, DC. Andreasen, N.C., 1979. Thought, language, and communication disorders: I. Clinical assessment, definition of terms, and evaluation of their reliability. Archives of General Psychiatry 39, 1315]1321. Andreasen, N.C., 1983. The Scale for the Assessment of Negative Symptoms ŽSANS.. The University of Iowa, Iowa City, IA. Andreasen, N.C., 1984. The Scale for the Assessment of Positive Symptoms ŽSAPS.. The University of Iowa, Iowa City, IA. Baron-Cohen, S., 1995. Mindblindness. M.I.T. Press, Cambridge, MA. Baron-Cohen, S., Cross, P., 1992. Reading the eyes: evidence for the role of perception in the development of theory of mind. Mind and Language 6, 173]186. Campbell, R., Heywood, C.A., Cowey, A., Regard, M., Landis, T., 1990. Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation. Neuropsychologia 28, 1123]1142. Callaway, E., Naghdi, S., 1982. An information processing model for schizophrenia. Archives of General Psychiatry 39, 339]347. Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates, Hillsdale, NJ. Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, ´ J., Jeannerod, M., 1997. Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition 65, 71]96. Dominey, P.F., Georgieff, N., 1997. Schizophrenics learn surface but not abstract structure in a serial reaction time task. NeuroReport 8, 2877]2882. Fleminger, S., 1992. Seeing is believing: the role of ‘preconscious’ perceptual processing in delusional misidentification. British Journal of Psychiatry 160, 293]303. Frith, C.D., 1992. The Cognitive Neuropsychology of Schizophrenia. Lawrence Erlbaum Associates, Hillsdale, NJ. Frith, C.D., Corcoran, R., 1996. Exploring ‘theory of mind’ in people with schizophrenia. Psychological Medicine 26, 521]530. Garety, P.A., Hemsley, D.R., Wessely, S., 1991. Reasoning in deluded and paranoid patients. Biases in performance on a probabilistic inference task. Journal of Nervous and Mental Disease 179, 194]201. Gur, R.E., Pearlson, G.D., 1993. Neuroimaging in schizophrenia research. Schizophrenia Bulletin 19, 337]353. Hoffman, R.E., 1986. Verbal hallucinations and language pro-
N. Franck et al. r Psychiatry Research 81 (1998) 67]75 duction processes in schizophrenia. Behavioral and Brain Sciences 9, 503]548. Maurer, D., 1985. Infants’ perception of facedness. In: Field, T., Fox, N. ŽEds.., Social Perception in Infants. Ablex. McCarley, R.W., Shenton, M.E., O’Donnell, B.F., Faux, S.F., Kikinis, R., Nestor, P.G., Jolesz, F.A., 1993. Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. Archives of General Psychiatry 50, 190]197. Oldfield, R.C., 1971. The assessment and analysis of handedness. Neuropsychologia 9, 97]113. Overall, J.E., Gorham, D.R., 1962. The Brief Psychiatric Rating Scale. Psychological Reports 10, 799]812. Perrett, D.I., Smith, P.A.J., Potter, D.D., Mistlin, A.J., Head, A.S., Milner, A.D., Jeeves, M.A., 1985. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proceedings of the Royal Society of London B 223, 293]317. Perrett, D.I., Mistlin, A.J., Chitty, A.J., Harries, M., Newscombe, F., de Haan, E., 1988. Neuronal mechanisms of face perception and their pathology. In: Kennard, C., Clifford Rose, F. ŽEds.., Physiological Aspects of Clinical NeuroOphthalmology. Chapman and Hall, London, pp. 137]154.
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Perrett, D.I., Hietanen, M., Oram, M.W., Benson, P.J., 1992. Organization and functions of cells responsive to faces in the temporal cortex. Proceedings of the Royal Society of London B 335, 23]30. Phillips, M.L., David, A.S., 1997. Visual scan paths are abnormal in deluded schizophrenics. Neuropsychologia 35, 99]105. Rosse, R.B., Kendrick, K., Wyatt, R.J., Isaac, A., Deutsch, S.I., 1994. Gaze discrimination in patients with schizophrenia: preliminary report. American Journal of Psychiatry 151, 919]921. Salem, J.E., Kring, A.M., Kerr, S.L., 1996. More evidence for generalized poor performance in facial emotion perception in schizophrenia. Journal of Abnormal Psychology 105, 480]483. Sarfati, Y., Hardy-Bayle, ´ M.-C., Nadel, J., Chevalier, J.-F., Widlocher, D., 1997. Attribution of mental states to others ¨ by schizophrenic patients. Cognitive Neuropsychiatry 2, 1]17.