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Treatment and diagnostic subtype in facial affect recognition in schizophrenia
I. psvchiat. Res., Vol, 29, No. I, pp. 5 1 I. 1995 Copyright ,(, 1995 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0022 395695 $ 9 5 0 + . 0 0
~ Pergamon 0022-3956(94)00033-6
T R E A T M E N T A N D D I A G N O S T I C SUBTYPE IN F A C I A L A F F E C T R E C O G N I T I O N IN S C H I Z O P H R E N I A S T E P H E N F. L E W I S * and D A V I D L. G A R V E R t * Department of Psychiatry, University of Arizona School of Medicine, Tucson VAMC, Tucson, AZ 85623, U.S.A.; and + Department of Psychiatry, Southwestern Medical School of the University of Texas, Schizophrenia Research Center, Dallas VAMC (116A), 4500 Lancaster Road, Dallas, TX 75216, U.S.A.
(ReceivedJbr publication 20 July 1994) Summary Patients with schizophrenia have been described as having deficits in the ability to recognize facial expressions of emotion. We report the results of a study on the effects of global psychopathology, positive and negative symptoms, diagnostic subtype, and antipsychotic medications, on the ability of subjects with schizophrenia to recognize facial affect. Eighteen SCID diagnosed patients with schizophrenia and ten matched controls were evaluated at a drug-free baseline for ability to identify facial expression expressed in a standardized series of photographs. with concurrent measures of global psychopathology, and positive and negative symptoms. At baseline patients were impaired in affect recognition relative to the normals, and impairment was not related to measures of psychopathology or positive or negative symptoms. Performance did not improve with antipsychotic treatment, and patients with paranoid schizophrenia had significantly better affect recognition abilities than non-paranoid patients. Introduction The ability to recognize expressions of facial affect appears to be universal a m o n g h u m a n s (Ekman, 1989, 1993), and m a y be innate in primates (Sackett, 1965). Patients with schizophrenia have been considered to be distinctive in part because o f " a deficit in the emotional r a p p o r t " (Bleuler, 1925), and an impaired ability to recognize facial affect might contribute to this deficit. Izard (1959) was the first to study responses to p h o t o g r a p h s o f facial expressions in subjects with schizophrenia and normal controls. Subjects with schizophrenia were found to be impaired in j u d g m e n t o f facial affect relative to normal controls in this and subsequent studies ( D o u g h e r t y et al., 1974). These early studies had vague diagnostic criteria, and subjects were frequently poorly characterized as to length o f hospitalization, medication status or diagnostic subtype. M o r e recent studies using standardized photographs of facial expression as stimulus material have expanded the n u m b e r o f control groups to include non-psychotic psychiatric patients (Archer et al., 1992; Cutting 1981, Feinberg et al., 1986, Walker et al., 1984); have added control tasks that use complex stimuli or faces to evaluate general visual processing deficits (Walker et al., 1984; Gessler et al., 1989; Kline et al., 1992; N o v i c et al., 1984: Heimberg et al., 1992); and have evaluated different age groups (Walker et al., 1980). Most studies have suggested that in schizophrenia there is indeed impairment in recognition o f facial expression, and when control tasks are Correspondence to: Stephen Lewis, Tucson VAMC, Tucson, AZ 85623, U.S.A~
6
s.F. Lewisand D. L. Garver
included there is a differential impairment in affect recognition (Cutting, 1981; Walker et al., 1980, 1984; Heimberg et al., 1992; Pilowsky & Basset, 1980; Gaebel & Wolwer, 1992). Other studies have been equivocal (Feinberg et al., 1986; Novic et al., 1984), and one study used questionable diagnostic criteria (Zuroff & Collussy, 1986). Two studies have not shown a differential impairment (Archer et al., 1992; Gessler et al., 1989). Despite improved study designs there has been little investigation of the relationship between impairments in facial affect recognition and other measures of psychopathology or treatment methods. One recent study examined the effect of diagnostic subtype on facial affect recognition (Kline et al., 1992) and found patients with paranoid schizophrenia superior to non-paranoid patients in ability to recognize facial expression. Another recent study examined medication effects on affect recognition (Gaebel et al., 1992), finding that impairments were relatively stable over 4 weeks. We hypothesized that patients with schizophrenia would be impaired relative to normal controls in affect recognition, that such impairments are relatively stable for each patient and independent of global psychopathology, that such deficits are related to measurements of negative symptoms, and that diagnostic subtype would be related to the ability to recognize affect. Method
Subjects All patients admitted to the Dallas VA over a 10-month period with complaints of symptoms of psychosis were screened for inclusion in this study. Subjects were required to have no history of head trauma predating onset of their illness, no substance abuse in the month prior to hospitalization, and no medical condition which might produce psychosis. All subjects were informed of the nature of the investigation and the procedures involved, and informed consent was obtained. All subjects with schizophrenia were diagnosed and subtyped using the SCID-P (Spitzer et al., 1988), and all patients included had demonstrated an ability to read a list of seven affects (anger, fear, sad, happy, disgust, surprise, neutral). Ten normal control subjects were recruited by advertisements from the housekeeping, maintenance, and volunteer staffs at the Dallas VAMC, and screened with the MiniSCID (Multi-Health Systems Inc. & American Psychiatric Association, 1990). Normals were also screened for family history of mental illness, or any medical condition which might impair brain functioning. Past histories of substance abuse did not exclude controls as such histories were present in some experimental subjects.
Procedure Stimulus material for testing facial affect recognition came from a set of photographs developed by Ekman and Friesen (1976) and shown to elicit reliable responses in normals. The six photographs in each category of basic affect (anger, fear, sad, happy, disgust, surprise) that had been most reliably identified by normals and four photographs of a neutral expression were selected. Each category of photographs was divided into two groups, so that two series of 20 photographs was produced. The photographs were presented as 5" × 7" prints in a fixed randomized order; with each photograph subjects were given a
Treatment in Facial Affect Recognition in Schizophrenia
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sheet with a checklist of the seven expressions listed above. Subjects were asked to check the word which best matched the expression on the photograph presented. Schizophrenic subjects were tested at a drug-free baseline with one photographic series, and BPRS (Overall & G o r h a m , 1962) and the PANSS (Kay et al., 1987) positive and negative scales were rated at the same time. After antipsychotic drug treatment patients were given the second series of photographs, and BPRS and PANSS ratings were again recorded. An attempt was made to reevaluate all patients after 2 weeks of medication treatment, and most patients were treated with 5-20 mg of haloperidol per day, but clinical necessity and involvement in other study protocols were accepted as grounds for a change in drug dose and time to retest. N o r m a l control subjects had the same test, retest, and rating scales, over similar intervals of time. Patients and controls were compared with independent t-tests (separate variances t or pooled variances t as appropriate); relationships between variables were measured using Pearson correlation coefficients with Bonferroni adjustments. Results A total of 18 patient subjects met inclusion criteria and gave informed consent to participate in the study, as did 10 normal controls. Patient and control groups did not differ in terms of age (mean = 38.9 years_+ 6.5SD, and 38.5 years + 7.2SD respectively: t -- 0.14 df= 17.1), education (mean = 12.6 years_+ 1.8SD, and 13.1 years+_l.6SD respectively; t = - 0 . 7 1 , df= 26) or race (each group 50% black and 50% white). The age of onset of illness ranged from 13 to 39 years (mean 22.5 y e a r s ± 3 . 2 S D ; non-paranoid 21.1 years_+ 7.5SD, paranoid 23.4 years + 7.5SD; t = --0.81, df = 9.0,). One of the patient subjects had no previous treatment with antipsychotic medications, all other subjects had been without antipsychotic medications for periods of 2-400 weeks (mean duration 48 weeks _+99.1SD). As predicted, schizophrenic subjects were significantly impaired in affect recognition relative to normal controls, as measured by number of errors on the recognition test at baseline (5.4_+3.4SD vs 2.6_+1.7SD errors respectively; t = 2.91, df= 26, p = 0.007). Though the schizophrenic subjects responded to daily doses of antipsychotic medications (mean BPRS baseline = 45.7 vs mean BPRS at second t e s t - - 4 0 . 2 , t = 2.83, df= 17.1, p = 0.011), the difference between schizophrenic and control performance in affect recognition remained at the time of the second test (5.2 ± 2.9SD vs 3.2_+ 2.0SD errors respectively; t = - 2.1, df = 24.4, p = 0.042). We found no significant correlation between global psychopathology as measured by the BPRS and performance in affect recognition testing in the schizophrenic group at drug-free baseline (r = - 0 . 1 3 , df = 15, p = NS) or during treatment with antipsychotic medications (r = 0.37, df= 15, p = NS). There was no relationship between the PANSS positive scales and affect recognition scores at baseline (r = 0.05, df= 15, p = NS) or during treatment (r = 0.32, df= 15, p = NS). We found a similar lack of correlation for the PANSS negative scale and affect recognition scores at both test 1 (r = 0.05, df= 15, p = NS) and test 2 (r = 0.39, df= 15, p = NS). Patients' age of onset of illness was not correlated with affect recognition scores at baseline (r = - 0 . 3 6 , df= 15, p = NS) or during treatment (r = - 0 . 0 7 , df= 15, p = NS), and duration of
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Figure 1. Performance of individual schizophrenics on a test of ability to recognizefacial affect displayed in photographs. (O) Scores of patients diagnosed as paranoid schizophrenic; (O) performance of non-paranoid schizophrenics. time since last treatment with antipsychotic medications was not correlated with affect recognition at test 1 or test 2 (r = 0.053, d f = 15,p = NS, and r = -0.316, d f = 15,p = NS respectively). There were differences among the patient subjects in the ability to recognize affect. Though baseline global psychopathology scores (BPRS) were similar for patients with both paranoid and non-paranoid schizophrenia (mean BPRS score 46.5 + 9.7SD vs 45.0 _+7.7SD respectively), subjects with the paranoid subtype clearly made fewer errors in affect recognition (2.5+ 1.OSD vs 7.7_+2.6SD respectively; t = 5.54, d f = 13.9, p < 0.001). These differences remained during antipsychotic treatment, with subjects with the paranoid subtype out-performing non-paranoid subjects (2.38 +_0.9SD vs 7.50_+ 1.6SD errors respectively; t = 8.60, df = 14.8, p < .001). Figure 1 illustrates these differences, and shows the stability of performance for each individual. Discussion We found a clear distinction between paranoid and non-paranoid patients in their ability to recognize facial expressions of affect. The only other study to examine the effects of diagnostic subtype on affect recognition (Kline et al., 1992) also found subjects with paranoid schizophrenia superior to those with non-paranoid schizophrenia. That same study also found that subjects with non-paranoid schizophrenia impaired in recognition memory for expressive faces and abstract figures. While this suggests the group of nonparanoid patients was more impaired in visual memory tasks than the paranoid and control subjects, it does not necessarily follow that memory impairments are responsible for deficits in affect recognition. Primate literature suggests that there are distinct face processing centers in the temporal lobe (Leonard et al., 1985; Hasselmo et al., 1989), with neurons in the superior temporal sulcus selective for facial expression, and neurons on the inferior temporal cortex specific for facial identity. Humans might also have distinct sites for
Treatment in FacialAffectRecognitionin Schizophrenia
9
processing facial identity and affect recognition, as suggested by human subjects with brain injury who have been shown to have dissociation of facial affect recognition and facial identity recognition (Trane et al., 1988; Parry et al, 1991; Humphreys et al., 1993). It may be that using facial identity and affect recognition memory tasks as control tests compares short-term recall functions (hippocampus) (Squire, 1992) with face processing tasks (superior and inferior temporal cortex). The results of Kline et al. (1992) may be due to neuropathologic processes that affect multiple temporal lobe regions, so that deficits in recognition memory tasks and facial affect recognition are independent expressions of a common pathologic process. The lack of correlation between impairments in expression recognition and negative symptoms is puzzling. Definitions of negative symptoms generally include impairments in emotional response (Kay et al., 1987; Andreason & Olsen, 1982; Crow, 1985). One other study has examined the relationship between negative symptom scales and affect recognition (Gaebel et al., 1992), and found that from the SANS (Andreasen, 1983) only alogia correlated with impairment in affect recognition. It may be that our use of negative symptoms as a group measure does not reflect the actual processes found in patients. Factor analysis of the PSE, SANS, and SAPS has suggested that there might actual be two or three separate clusters of symptoms instead of a single set of negative symptoms (Liddle et al., 1989; Dworkin, 1990; Keefe et al., 1992). Attempts to correlate affect recognition to one of these clusters might show a better relationship than we now see, but at present no similar factor analysis of the PANSS has been done. Alternatively, it may be that no current rating adequately measures impairment in affect recognition. This study has several important limitations. First, the sample size is not large. Enrollment was limited by recent substance abuse in the majority of potential patient subjects. Though the sample was sufficient for basic analysis, any real association between affect recognition and symptoms or treatment may have been obscured by the relatively modest number of subjects. Second, the amount of improvement associated with 2 weeks of antipsychotic drug treatment averaged only 12% and many patients remained quite psychotic. While we have shown that affect recognition in schizophrenia does not improve with short courses of antipsychotic treatment, it remains possible that longer treatment or reduction of symptoms to more mild levels of psychopathology might be associated with improved affect recognition. In our study antipsychotic medications and improvements in general measures of psychopathology did not appear to be associated with an improved ability to recognize facial expression. This was also reported in the one other study that examined medication effects (Gaebel, 1992), which showed deficits in affect recognition were relatively stable in schizophrenics but not in depressed subjects. In those schizophrenic patients who display affect recognition deficits, these deficits may represent a trait-like effect of specific underlying brain pathology. To determine if objectively measured deficits in facial affect recognition are a trait, pedigree and high-risk studies will be necessary. Future studies should include facial identity tasks as a control task, so any pattern of differential face processing impairment may be discerned. Such future studies should subtype psychotic patients to insure that deficits detected in one group are not also taken to be representative of schizophrenics as a whole. Appropriate structural imaging techniques might suggest correlation between temporal lobe pathology and expression recognition deficits.
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References Andreasen, N. C. (1983) The scalefor the assessment of negative symptoms (SANS). Iowa City: University of Iowa. Andreason, N. C. & Olsen, S. (1982). Negative versus positive schizophrenia: definition and validation. Archives of General Psychiatry, 39, 789-794. Archer, J., Hay, D. C. & Young, A. W. (1992). Face processing in psychiatric conditions. British Journal of Clinical Psychology, 31, 45-61. Bleuler, E. (1925). Textbook of psychiatry. New York: Arno Press, 1976. Crow, T. I. (1985). The two - - syndrome concept: origins and current status. SchizophreniaBulletin, 11,471-486. Cutting, J. C. (1981). Judgment of emotional expression in schizophrenia. British Journal of Psychiatry, 139, 1-6. Dougherty, E. E. Bartlett, E. S. & Izard, C. E. (1974). Responses of schizophrenics to expressions of fundamental emotions. Journal of Clinical Psychology, 30, 243-246. Dworkin, R. H. (1990). Patterns of sex differences in negative symptoms and social functioning consistent with separate dimensions of schizophrenic psychopathology. American Journal of Psychiatry, 147, 347 349. Ekman, P. (1993). Facial expression and emotion. American Psychologist, 48, 384-392. Ekman, P. (1989). The argument and evidence about universals in facial expressions of emotion. In H. Wagner & S. Smith (Eds.), Handbook ofsocialpsychophysiology (pp. 143-164). Chichester: Wiley. Ekman, P. & Friesen, W. V. (1976). Pictures offacial affect. Palo Alto: Consulting Psychologists Press. Feinberg, T. E., Rifkin, A., Schaffer, C. & Walker, E. (1986). Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry, 43, 276-279. Gaebel, W. & Wolwer, W. (1992). Facial expression and emotional face recognition in schizophrenia and depression. European Archives of Psychiatry and Clinical Neuroscience, 242, 46-52. Gessler, S., Cutting, J. Frith, C. D. & Weinman, J. (1989). Schizophrenic inability to judge facial emotion: a controlled study. British Journal of Clinical Psychology, 28, 19 29. Hasselmo, M. E. Rolls E. T. & Baylis, G. C. (1989). The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behavioral Brain Research, 32, 203-218. Heimberg, C., Gur, R. E., Erwin, J. R., Shastel, D. L. & Gur, R. C. (1992). Facial emotion discrimination: III. Behavioral findings in schizophrenia. Psychiatry Research, 42, 253 265. Humphreys, G. W., Donnelly, N. & Riddoch, M. J. (1993). Expression is computed separately from facial identity, and it is computed separately for moving and static faces: neuropsychological evidence. Neuropsychologia, 31, 173-181. Izard, C. E. (1959). Paranoid schizophrenic and normal subjects' perceptions of photographs of human faces. Journal of Consulting Psychology, 42, 253-265. Kay, S. R., Fiszbein, A. & Opler, I. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13, 261-275. Keefe, B. S. E., Harvey, P. D., Lenzenwagger, M. E., Davidson, M., Apter, S. H., Schmeidler, J., Mohs, R. C. & Davis, K. L. (1992). Empirical assessment of the factorial structure of clinical symptoms in schizophrenia: negative symptoms. Psychiatry Research, 44, 153 165. Kline, J. S., Smith J. E. & Ellis, H. C. (1992). Paranoid and non-paranoid schizophrenic processing of facially displayed affect. Journal of Psychiatric Research, 26, 169-182. Leonard, C. M., Rolls, E. T., Wilson, E. A. W. & Baylis, G. C. (1985). Neurons in the amygdala of the monkey with responses selective for faces. Behavioral Brain Research, 15, 159-176. Liddle, P. F., Barnes, T. R. E., Morris, D. & Haque, S. (1989). Three syndromes in chronic schizophrenia. British Journal of Psychiatry, 155 (Suppl. 7), 119-122. Mini-SCID (1990). Multi-Health Systems Inc. and American Psychiatric Association N. Tonawanda, NY. Novic, J., Luchins, D. J. & Perline, R. (1984). Facial affect recognition in schizophrenia. British Journal of Psychiatry, 144, 533-537. Overall, J. E. & Gorham, D. R. (1962). The brief psychiatric rating scale. PsychologicalReports, 10, 799 812. Parry, E. M., Young, A. W., Saul, J. S. M. & Moss, A. (1991). Dissociable face processing impairment after brain injury. Journal of Clinical and Experimental Neuropsychology, 13, 545-558. Pilowsky, I. & Basset, D. (1980). Schizophrenia and the response to facial emotions. Comprehensive Psychiatry, 21, 23(~244. Sackett, G. (1965). Monkeys reared in isolation with pictures as visual input: evidence for an innate releasing mechanism. Science, 154, 1468-1463. Spitzer, R. I., Williams, I. B. W., Gibbon, M. & First, M. B. (1988). Structured Clinical Interviewfor DSM-111-R (SCID). New York: New York State Psychiatric Institute. Squire L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195-231.
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Tranel, D., Damasio, A. R. & Damasio, H. (1988). Intact recognition of facial expression, gender, and age in patients with impaired recognition of face identity. Neurology, 38, 690-696. Walker, E., Marwit, S. I. & Emory, E. (1980). A cross-sectional study of emotion recognition in schizophrenics. Journal of Abnormal Psychology, 89, 428-436. Walker, E., Mcguire, M. & Bettes, B. (1984). Recognition and identification of facial stimuli by schizophrenics and patients with affective disorders. British Journal of Clinical Psychology, 23, 37-44, Zuroff, D. C. & Collussy, S. A. (1986). Emotion recognition in schizophrenic and depressed inpatients. Journal of Clinical Psychology, 42, 411-417.
~ Pergamon 0022-3956(94)00033-6
T R E A T M E N T A N D D I A G N O S T I C SUBTYPE IN F A C I A L A F F E C T R E C O G N I T I O N IN S C H I Z O P H R E N I A S T E P H E N F. L E W I S * and D A V I D L. G A R V E R t * Department of Psychiatry, University of Arizona School of Medicine, Tucson VAMC, Tucson, AZ 85623, U.S.A.; and + Department of Psychiatry, Southwestern Medical School of the University of Texas, Schizophrenia Research Center, Dallas VAMC (116A), 4500 Lancaster Road, Dallas, TX 75216, U.S.A.
(ReceivedJbr publication 20 July 1994) Summary Patients with schizophrenia have been described as having deficits in the ability to recognize facial expressions of emotion. We report the results of a study on the effects of global psychopathology, positive and negative symptoms, diagnostic subtype, and antipsychotic medications, on the ability of subjects with schizophrenia to recognize facial affect. Eighteen SCID diagnosed patients with schizophrenia and ten matched controls were evaluated at a drug-free baseline for ability to identify facial expression expressed in a standardized series of photographs. with concurrent measures of global psychopathology, and positive and negative symptoms. At baseline patients were impaired in affect recognition relative to the normals, and impairment was not related to measures of psychopathology or positive or negative symptoms. Performance did not improve with antipsychotic treatment, and patients with paranoid schizophrenia had significantly better affect recognition abilities than non-paranoid patients. Introduction The ability to recognize expressions of facial affect appears to be universal a m o n g h u m a n s (Ekman, 1989, 1993), and m a y be innate in primates (Sackett, 1965). Patients with schizophrenia have been considered to be distinctive in part because o f " a deficit in the emotional r a p p o r t " (Bleuler, 1925), and an impaired ability to recognize facial affect might contribute to this deficit. Izard (1959) was the first to study responses to p h o t o g r a p h s o f facial expressions in subjects with schizophrenia and normal controls. Subjects with schizophrenia were found to be impaired in j u d g m e n t o f facial affect relative to normal controls in this and subsequent studies ( D o u g h e r t y et al., 1974). These early studies had vague diagnostic criteria, and subjects were frequently poorly characterized as to length o f hospitalization, medication status or diagnostic subtype. M o r e recent studies using standardized photographs of facial expression as stimulus material have expanded the n u m b e r o f control groups to include non-psychotic psychiatric patients (Archer et al., 1992; Cutting 1981, Feinberg et al., 1986, Walker et al., 1984); have added control tasks that use complex stimuli or faces to evaluate general visual processing deficits (Walker et al., 1984; Gessler et al., 1989; Kline et al., 1992; N o v i c et al., 1984: Heimberg et al., 1992); and have evaluated different age groups (Walker et al., 1980). Most studies have suggested that in schizophrenia there is indeed impairment in recognition o f facial expression, and when control tasks are Correspondence to: Stephen Lewis, Tucson VAMC, Tucson, AZ 85623, U.S.A~
6
s.F. Lewisand D. L. Garver
included there is a differential impairment in affect recognition (Cutting, 1981; Walker et al., 1980, 1984; Heimberg et al., 1992; Pilowsky & Basset, 1980; Gaebel & Wolwer, 1992). Other studies have been equivocal (Feinberg et al., 1986; Novic et al., 1984), and one study used questionable diagnostic criteria (Zuroff & Collussy, 1986). Two studies have not shown a differential impairment (Archer et al., 1992; Gessler et al., 1989). Despite improved study designs there has been little investigation of the relationship between impairments in facial affect recognition and other measures of psychopathology or treatment methods. One recent study examined the effect of diagnostic subtype on facial affect recognition (Kline et al., 1992) and found patients with paranoid schizophrenia superior to non-paranoid patients in ability to recognize facial expression. Another recent study examined medication effects on affect recognition (Gaebel et al., 1992), finding that impairments were relatively stable over 4 weeks. We hypothesized that patients with schizophrenia would be impaired relative to normal controls in affect recognition, that such impairments are relatively stable for each patient and independent of global psychopathology, that such deficits are related to measurements of negative symptoms, and that diagnostic subtype would be related to the ability to recognize affect. Method
Subjects All patients admitted to the Dallas VA over a 10-month period with complaints of symptoms of psychosis were screened for inclusion in this study. Subjects were required to have no history of head trauma predating onset of their illness, no substance abuse in the month prior to hospitalization, and no medical condition which might produce psychosis. All subjects were informed of the nature of the investigation and the procedures involved, and informed consent was obtained. All subjects with schizophrenia were diagnosed and subtyped using the SCID-P (Spitzer et al., 1988), and all patients included had demonstrated an ability to read a list of seven affects (anger, fear, sad, happy, disgust, surprise, neutral). Ten normal control subjects were recruited by advertisements from the housekeeping, maintenance, and volunteer staffs at the Dallas VAMC, and screened with the MiniSCID (Multi-Health Systems Inc. & American Psychiatric Association, 1990). Normals were also screened for family history of mental illness, or any medical condition which might impair brain functioning. Past histories of substance abuse did not exclude controls as such histories were present in some experimental subjects.
Procedure Stimulus material for testing facial affect recognition came from a set of photographs developed by Ekman and Friesen (1976) and shown to elicit reliable responses in normals. The six photographs in each category of basic affect (anger, fear, sad, happy, disgust, surprise) that had been most reliably identified by normals and four photographs of a neutral expression were selected. Each category of photographs was divided into two groups, so that two series of 20 photographs was produced. The photographs were presented as 5" × 7" prints in a fixed randomized order; with each photograph subjects were given a
Treatment in Facial Affect Recognition in Schizophrenia
7
sheet with a checklist of the seven expressions listed above. Subjects were asked to check the word which best matched the expression on the photograph presented. Schizophrenic subjects were tested at a drug-free baseline with one photographic series, and BPRS (Overall & G o r h a m , 1962) and the PANSS (Kay et al., 1987) positive and negative scales were rated at the same time. After antipsychotic drug treatment patients were given the second series of photographs, and BPRS and PANSS ratings were again recorded. An attempt was made to reevaluate all patients after 2 weeks of medication treatment, and most patients were treated with 5-20 mg of haloperidol per day, but clinical necessity and involvement in other study protocols were accepted as grounds for a change in drug dose and time to retest. N o r m a l control subjects had the same test, retest, and rating scales, over similar intervals of time. Patients and controls were compared with independent t-tests (separate variances t or pooled variances t as appropriate); relationships between variables were measured using Pearson correlation coefficients with Bonferroni adjustments. Results A total of 18 patient subjects met inclusion criteria and gave informed consent to participate in the study, as did 10 normal controls. Patient and control groups did not differ in terms of age (mean = 38.9 years_+ 6.5SD, and 38.5 years + 7.2SD respectively: t -- 0.14 df= 17.1), education (mean = 12.6 years_+ 1.8SD, and 13.1 years+_l.6SD respectively; t = - 0 . 7 1 , df= 26) or race (each group 50% black and 50% white). The age of onset of illness ranged from 13 to 39 years (mean 22.5 y e a r s ± 3 . 2 S D ; non-paranoid 21.1 years_+ 7.5SD, paranoid 23.4 years + 7.5SD; t = --0.81, df = 9.0,). One of the patient subjects had no previous treatment with antipsychotic medications, all other subjects had been without antipsychotic medications for periods of 2-400 weeks (mean duration 48 weeks _+99.1SD). As predicted, schizophrenic subjects were significantly impaired in affect recognition relative to normal controls, as measured by number of errors on the recognition test at baseline (5.4_+3.4SD vs 2.6_+1.7SD errors respectively; t = 2.91, df= 26, p = 0.007). Though the schizophrenic subjects responded to daily doses of antipsychotic medications (mean BPRS baseline = 45.7 vs mean BPRS at second t e s t - - 4 0 . 2 , t = 2.83, df= 17.1, p = 0.011), the difference between schizophrenic and control performance in affect recognition remained at the time of the second test (5.2 ± 2.9SD vs 3.2_+ 2.0SD errors respectively; t = - 2.1, df = 24.4, p = 0.042). We found no significant correlation between global psychopathology as measured by the BPRS and performance in affect recognition testing in the schizophrenic group at drug-free baseline (r = - 0 . 1 3 , df = 15, p = NS) or during treatment with antipsychotic medications (r = 0.37, df= 15, p = NS). There was no relationship between the PANSS positive scales and affect recognition scores at baseline (r = 0.05, df= 15, p = NS) or during treatment (r = 0.32, df= 15, p = NS). We found a similar lack of correlation for the PANSS negative scale and affect recognition scores at both test 1 (r = 0.05, df= 15, p = NS) and test 2 (r = 0.39, df= 15, p = NS). Patients' age of onset of illness was not correlated with affect recognition scores at baseline (r = - 0 . 3 6 , df= 15, p = NS) or during treatment (r = - 0 . 0 7 , df= 15, p = NS), and duration of
S. F. Lewisand D. L. Garver 16 z 0 I,z 0 rO ku rr
=-,,o
10
Z 00 rr
0 r'r"
,,=,
5
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BASELINE
DURING TREATMENT
Figure 1. Performance of individual schizophrenics on a test of ability to recognizefacial affect displayed in photographs. (O) Scores of patients diagnosed as paranoid schizophrenic; (O) performance of non-paranoid schizophrenics. time since last treatment with antipsychotic medications was not correlated with affect recognition at test 1 or test 2 (r = 0.053, d f = 15,p = NS, and r = -0.316, d f = 15,p = NS respectively). There were differences among the patient subjects in the ability to recognize affect. Though baseline global psychopathology scores (BPRS) were similar for patients with both paranoid and non-paranoid schizophrenia (mean BPRS score 46.5 + 9.7SD vs 45.0 _+7.7SD respectively), subjects with the paranoid subtype clearly made fewer errors in affect recognition (2.5+ 1.OSD vs 7.7_+2.6SD respectively; t = 5.54, d f = 13.9, p < 0.001). These differences remained during antipsychotic treatment, with subjects with the paranoid subtype out-performing non-paranoid subjects (2.38 +_0.9SD vs 7.50_+ 1.6SD errors respectively; t = 8.60, df = 14.8, p < .001). Figure 1 illustrates these differences, and shows the stability of performance for each individual. Discussion We found a clear distinction between paranoid and non-paranoid patients in their ability to recognize facial expressions of affect. The only other study to examine the effects of diagnostic subtype on affect recognition (Kline et al., 1992) also found subjects with paranoid schizophrenia superior to those with non-paranoid schizophrenia. That same study also found that subjects with non-paranoid schizophrenia impaired in recognition memory for expressive faces and abstract figures. While this suggests the group of nonparanoid patients was more impaired in visual memory tasks than the paranoid and control subjects, it does not necessarily follow that memory impairments are responsible for deficits in affect recognition. Primate literature suggests that there are distinct face processing centers in the temporal lobe (Leonard et al., 1985; Hasselmo et al., 1989), with neurons in the superior temporal sulcus selective for facial expression, and neurons on the inferior temporal cortex specific for facial identity. Humans might also have distinct sites for
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processing facial identity and affect recognition, as suggested by human subjects with brain injury who have been shown to have dissociation of facial affect recognition and facial identity recognition (Trane et al., 1988; Parry et al, 1991; Humphreys et al., 1993). It may be that using facial identity and affect recognition memory tasks as control tests compares short-term recall functions (hippocampus) (Squire, 1992) with face processing tasks (superior and inferior temporal cortex). The results of Kline et al. (1992) may be due to neuropathologic processes that affect multiple temporal lobe regions, so that deficits in recognition memory tasks and facial affect recognition are independent expressions of a common pathologic process. The lack of correlation between impairments in expression recognition and negative symptoms is puzzling. Definitions of negative symptoms generally include impairments in emotional response (Kay et al., 1987; Andreason & Olsen, 1982; Crow, 1985). One other study has examined the relationship between negative symptom scales and affect recognition (Gaebel et al., 1992), and found that from the SANS (Andreasen, 1983) only alogia correlated with impairment in affect recognition. It may be that our use of negative symptoms as a group measure does not reflect the actual processes found in patients. Factor analysis of the PSE, SANS, and SAPS has suggested that there might actual be two or three separate clusters of symptoms instead of a single set of negative symptoms (Liddle et al., 1989; Dworkin, 1990; Keefe et al., 1992). Attempts to correlate affect recognition to one of these clusters might show a better relationship than we now see, but at present no similar factor analysis of the PANSS has been done. Alternatively, it may be that no current rating adequately measures impairment in affect recognition. This study has several important limitations. First, the sample size is not large. Enrollment was limited by recent substance abuse in the majority of potential patient subjects. Though the sample was sufficient for basic analysis, any real association between affect recognition and symptoms or treatment may have been obscured by the relatively modest number of subjects. Second, the amount of improvement associated with 2 weeks of antipsychotic drug treatment averaged only 12% and many patients remained quite psychotic. While we have shown that affect recognition in schizophrenia does not improve with short courses of antipsychotic treatment, it remains possible that longer treatment or reduction of symptoms to more mild levels of psychopathology might be associated with improved affect recognition. In our study antipsychotic medications and improvements in general measures of psychopathology did not appear to be associated with an improved ability to recognize facial expression. This was also reported in the one other study that examined medication effects (Gaebel, 1992), which showed deficits in affect recognition were relatively stable in schizophrenics but not in depressed subjects. In those schizophrenic patients who display affect recognition deficits, these deficits may represent a trait-like effect of specific underlying brain pathology. To determine if objectively measured deficits in facial affect recognition are a trait, pedigree and high-risk studies will be necessary. Future studies should include facial identity tasks as a control task, so any pattern of differential face processing impairment may be discerned. Such future studies should subtype psychotic patients to insure that deficits detected in one group are not also taken to be representative of schizophrenics as a whole. Appropriate structural imaging techniques might suggest correlation between temporal lobe pathology and expression recognition deficits.
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S.F. Lewis and D. L. Garver
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