253
Ps.vchiatry Research, 421253-265 Elsevier
Facial Emotion Schizophrenia
Discrimination:
Carolyn Heimberg, Ruben C. Gur
Raquel E. Gur, Roland J. Erwin,
Received
October
IS, 1991; revised
version
received
III. Behavioral
February
Findings
Derri L. Shtasel,
24, 1992; accepted
April
in
and
12, 1992.
Abstract. Emotional
discrimination was studied in patients with schizophrenia (n = 20) and matched controls. Performance of the emotion-discrimination tasks in the schizophrenic patients was impaired, relative to their performance of an age-discrimination task. Performance patterns in the patient group could also be reliably distinguished from those of normal controls. The impairment was associated with the severity of both emotional and nonemotional symptoms specific to schizophrenia, but not with the severity of nonspecific symptoms. The deficit associated with schizophrenia is more marked than that reported for depression (Gur et al., 1992), particularly for the emotion-discrimination tasks, and showed no difference between “happy” discrimination and “sad” discrimination. The main difficulty in patients with schizophrenia is the assignment of emotional valence to neutral faces. The magnitude of the deficit underscores the salience of emotional impairment in schizophrenia, and its relation to cognitive dysfunction in this disorder merits further scrutiny. Key Words. Affect recognition,
depression,
psychiatric
symptoms.
Although disturbed cognition has been considered the hallmark of schizophrenia, disturbed affect is also a recognized feature. Early descriptions included lack of relatedness (Kraepelin, 1919) and inappropriate and blunted affect (Bleuler, 1911/ 1950). Advances in the study of human emotions (e.g., Izard, 1971; Ekman et al., 1972) have provided tools to measure individual differences in the ability to recognize facial affect. This domain has gained interest with the growing understanding of the neuropsychology of emotions and has been applied to patients with schizophrenia. Despite methodologic heterogeneity in studies of affect recognition (Morrison et al., 1988) some consistent findings have emerged. Patients with schizophrenia perform less well than depressed patients, and both groups perform more poorly than normal controls (Cutting, 1981; Walker et al., 1984; Feinberg et al., 1986;
Carolyn Heimberg, M.D., is Postdoctoral Fellow; Raquel E. Gur, M.D., Ph.D., and Ruben C. Gur, Ph.D., are Professors; and Roland J. Erwin, Ph.D., and Derri L. Shtasel, M.D., are Assistant Professors, all in the Department of Psychiatry, University of Pennsylvania, Philadelphia, was submitted. (Reprint requests to Dr. R.E. Gur, Neuropsychiatry Program, Floor Gates Bldg., University of Pennsylvania, 3500 Spruce St., Philadelphia, 0165-1781/92/$05.00
@ 1992 Elsevier Scientific
Publishers
Ireland
Ltd.
PA, at the time this report Dept. of Psychiatry, 10th PA 19104-4283, USA.)
254 Zuroff and Colussy, 1986; Gessler et al., 1989). The performance deficit in psychiatric patients has been particularly marked in the detection of negative emotions (Dougherty et al., 1974; Muzekari and Bates, 1977; Novic et al., 1984). Chronicity is associated with relatively better affect discrimination than is seen in acute psychosis (Cutting, 1981; Gessler et al., 1989). Patients have usually performed well on control tasks, including age discrimination and facial identity (Cutting, 1981; Walker et al., 1984; Gessler et al., 1989). Finally, affect-recognition tasks are associated with better performance than affect-labeling tasks (Dougherty et al., 1974; Walker et al., 1984; Feinberg et al., 1986). Inconsistencies between studies relate to differences in both subject populations and procedures. Patients have received diagnoses under differing classification systems (e.g., DSM-III-R [American Psychiatric Association, 19871, the Structured Clinical Interview for DSM-III-R [SCID; Spitzer et al., 19861, and Research Diagnostic Criteria [Spitzer et al., 19751); have included those with schizoaffective illness (Walker et al., 1984); have had divergent courses of illness with variable or undocumented medication status; and in some cases have been limited to females (Dougherty et al., 1974; Zuroff and Colussy, 1986). Control groups have not always been studied, though more recent investigations have included patients with affective disorders as well as normal controls. Procedural variation exists in stimuli, task administration, and response mode. Most studies used a set of black and white stimulus photographs from the Izard or Ekman batteries (Izard, 1971; Ekman et al., 1972), but other stimuli (Muzekari and Bates, 1977; Cutting, 1981; Magaro and Chamrad, 1983) have also been used. Even among those investigators who used material from the batteries, there are procedural variations in supplementing stimuli, use of adjunctive tasks (Novic et al., 1984; Walker et al., 1984; Zuroff and Colussy, I986), types of response sought (Dougherty et al., 1974; Pilowsky and Bassett, 1980; Cutting, 1981; Zuroff and Colussy, 1986), and stimulus-display methods (Feinberg et al., 1986). Furthermore, in the few studies that controlled for stimulus-exposure interval, duration of exposure varied from 500 msec to 5 minutes (Muzekari and Bates, 1977; Walker et al., 1984; Zuroff and Colussy, 1986; Gessler et al., 1989). Only a few studies of affect recognition in schizophrenia also conducted analyses of symptomatology that had a greater scope than what was required for diagnosis and subtyping (Muzekari and Bates, 1977; Novic et al., 1984; Zuroff and Colussy, 1986). Where such ratings were discussed, no significant relationship between clinical characteristics and response accuracy was found (Muzekari and Bates, 1977; Novic et al., 1984). The purpose of the present study was to apply standard procedures examined in normal subjects and patients with affective illness to a sample of patients with schizophrenia. We hypothesized that patients with schizophrenia would be impaired in their ability to discriminate emotions accurately. The application of standard diagnostic procedures and rating scales (Gur et al., 1991) permitted us to examine the relationships between affect-relevant symptomatology and affect recognition. We expected to find an association between task performance and severity of symptoms, especially in the affective domain.
255
Methods Subjects. The sample consisted of 20 patients (10 men, 10 women) from our Mental Health Clinical Research Center who received DSM-III-R diagnoses of schizophrenia (see Table I). They underwent medical, neurologic, and structured psychiatric evaluations, and were free of any other axis I disorder including substance abuse (Gur et al., 1991). Other exclusionary criteria for patients were as follows: history of neurologic disease including head trauma with loss of consciousness, history of medical disorders that might affect central nervous system function, and inability to cooperate with testing (e.g., inability to understand the task or excessive agitation). Notably, 11 patients were neuroleptic-naive at the time of testing, while 8 of the remaining 9 patients had not received neuroleptics for 2 or more weeks. For 1 I patients, this was the first psychiatric hospitalization. The mean age of the schizophrenic patients was 27.5 (SD = 6.2; range = 18-39) years. Control subjects were healthy volunteers (10 men, 10 women) who were matched to the patients on race (7 black, 13 white), handedness (3 left-handed), and sociodemographic variables. The mean age of the controls was 29.5 (SD = 8.7; range = 19-49) years. Controls underwent assessment procedures as described above for patients (Shtasel et al., 1991). Exclusionary criteria for controls were the same as those for patients, with the following additional requirements: (I) absence of axis II diagnosis of schizoid or schizotypal personality disorder and (2) absence of a history of first degree relatives with diagnoses of schizophrenia or affective disorder. While controls and patients were not comparable in the number of years of education (controls: mean = 15.0, SD = 2.4; patients: mean = 12.8, SD = 1.7; r = 3.47, p < O.Ol), they were balanced for parental education (controls: mean = 13.3, SD = 2.8; patients: mean = 13.1, SD = 2.0; f = 0.25, NS). Since schizophrenia is a disease that affects educational attainment (the “matching fallacy”; Meehl [ 1970]), parental level of education was considered a more valid index of sociodemographic background. Assessment and Rating Scales. Patient assessments and ratings were performed by research psychiatrists from the Mental Health Clinical Research Center (C.H., D.S., and R.E.G.). On the basis of clinical interviews and the SCID (Spitzer et al., 1986), the following rating scales were completed: the Brief Psychiatric Rating Scale (BPRS; Overall and Gorham, 1980) the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen and Olsen, 1982), the Scale for the Assessment of Negative Symptoms (SANS; Andreasen, 1982; Andreasen and Olsen, 1982) and the Hamilton Rating Scale for Depression (HRSD; Hamilton, 1960). Interrater reliabilities ranged from intraclass correlations of 0.74 to 0.95. Gur et al. (1989) described a method for developing a symptom specificity index for schizophrenia. This procedure divided the 18-item BPRS into symptoms considered specific to schizophrenia (emotional withdrawal, conceptual disorganization, mannerisms and posturing, grandiosity, suspiciousness, hallucinatory behavior, unusual thought content, and blunted affect) and nonspecific symptoms (somatic concern, anxiety, guilt feelings, tension, depressive mood, hostility, motor retardation, uncooperativeness, excitement, and disorientation). To examine the relationship between affective symptoms and emotional discrimination, this approach was adapted to the BPRS, SANS, and SAPS. Items of the scales assessing affect were identified by the three research psychiatrists, and consensus was achieved. Our determination of which items were more “schizophrenia-affect specific” was based on the premise that the presence of these symptoms is more characteristic of schizophrenia than of other major psychiatric disorders. The affect-nonspecific items were considered more likely to exist in any axis I disorder (Table 2). Task Administration. The facial discrimination tasks fell neutral, and sad-neutral. Task development and application in part I of this series of reports (Erwin et al., 1992). In professionai actors who were instructed to express happy
into three categories: age, happyto normal subjects was described brief, photographs were made of and sad faces. For the emotion-
18 30 35 31 33 31 20 36 23
B
B
W
B
W
B
B
B
B
W
B
M
F
F
F
F
F
F
F
F
F
F
10
11
12
13
14
15
16
17
18
19
20
21
D
16
20
P
D
33 26
P
C
R
L
11
U
P
P
R R
U
R
19
21
36
20
22
P
R R
30
21
D
R
U
P
R
19
P
L R
17
17
P
R
R
19
P
L R
21
24
P U
L R
U
R 21
22
U
Age at onset
R
Subtype
R
14
11
12
12
12
16
12
14
12
12
13
10
15
16
14
16
14
12
12
Education Handedness (yr)
1. Number of weeks that patrents had not been recerving neuroleptrcs; N = drug-narve.
Note. U = undrfferentiated. D = drsorganized. P = paranoid. M = male. F = female. W = whrte. 8 = black. R = right. L = left
23
20
19
W
8
29
M
M
7
25
9
M
6
25
B
26
M
5
B
M
4
29
w w
33
39
M
M
3
w w
Age (yr)
24
M
Race
w w
M
1
Sex
2
Patient No.
Table 1. Patient characteristics
0
0
1
0
0
1
0
0
4
1
0
0
2
0
0
3
0
2
10
25
Number of hospitalizations
N
N
N
N
3
N
3
N
2
0
N
N
2
N
N
12
N
231
10
26
Drug free’ (wk)
257 discrimination tasks, neutral and target emotion slides were intermixed, while for, the agediscrimination task, neutral faces were used. Cues were given at regular intervals within each task for subjects to rate their own emotional states. Mood and anxiety were assessed before and after the study with the Positive and Negative Affect Scale (PANAS; Zevon and Tellegen, 1982) and the State-Trait Anxiety Inventory (STAI; Spielberger et al., 1970).
Table 2. Emotion ratings BPRS:
Affect-Schizophrenia
Affect-General
Emotional
Anxiety
withdrawal
Guilt feelings
Blunted affect
Tension Depressive mood Hostility Excitement
SANS:
Unchanging
facial expression
Paucity of expressive
Decreased
spontaneous
movements
gestures
Poor eye contact Affective nonresponsivity Inappropriate
affect
Lack of vocal inflections Intimacy/closeness
with family/
significant other’ Relationships
with friends/peers’
Note. BPRS = Brief Psychiatric Rating Scale. SANS = Scale for the Assessment of Negative Symptoms. No items from the Scale for the Assessment of Positive Symptoms were considered to be relevant measures of affect. SANS item scores for interpersonal skills (intimacy/closeness
and relationships) were averaged
Data Analysis. Quantitation of the performance data was described by Erwin et al. (1992). In brief, the number of true positives (i.e., response in the “happy”range for a happy slide in the happy discrimination task and in the “sad” range for a sad slide in the sad discrimination task), false positives (scores in the emotional range for neutral stimuli), true negatives (neutral responses to neutral faces), and false negatives (neutral responses to emotional faces) were computed for each task. Percent correct was computed for all tasks as lOO*(total number of correct responses/ total number of items completed). For the emotional tasks, four additional measures were computed: sensitivity and specificity for each task separately, and positive and negative bias across tasks. Sensitivity was defined as true positives/(true positives + false negatives). This is a measure of how “sensitive” subjects are to the presence of the correct emotion. Specificity was defined as true negatives/(true negatives + false positives). This is a measure of how well subjects discriminate neutral from emotional stimuli. Sensitivity and specificity measures were not available for the age-discrimination task. Positive bias across tasks was computed as (happy-neutral false positives i- sad-neutral false negatives)/(total attempted happy-neutral positives + total attempted sad-neutral negatives), and negative bias was computed as (happy-neutral false negatives i- sad-neutral false positives)/(total attempted happy-neutral negatives -I- total attempted sad-neutral positives). The formula 2*arc sine of the square root of the proportion, as recommended by Cohen (1988), was used to transform all proportions. The effects of normal aging, sex, and the age X sex interaction were removed by regression procedures described in part II (Cur et al., 1992). Thus, the performance data submitted for statistical analysis were not influenced by effects of age and sex on normal performance. Statistical analysis was aimed at testing the hypotheses, possible mood-inducing effects of
258 the tasks, the discriminatory power of the tasks, and differences between patients with schizophrenia and patients with depression. The hypotheses were evaluated as follows: (1) Percent correct, sensitivity and specificity, and bias scores were compared between patients and controls in mixed model repeated measures analyses of variance (ANOVAs; SAS Institute, 1985), with diagnosis as a grouping factor. The within-group (repeated measures) factors were task (age discrimination, happyneutral, and sad-neutral) for the percent correct measure, task (happy-neutral, sad-neutral), and measure (sensitivity and specificity) for analyses restricted to the emotion-discrimination tasks, and bias (positive and negative) for the bias measures. (2) The association between task performance and severity of symptoms in patients was tested by first dividing patients into high and low severity (median cutoff) for emotional-specific, emotional-nonspecific, nonemotional-specific and nonemotional-nonspecific symptoms (see detailed description above). High and low severity for each of these four dimensions served as a grouping factor in separate ANOVAs with measure (sensitivity and specificity across emotion-discrimination tasks) as the within-group (repeated measures) factor. Both main effects and interactions were examined. The possible mood-inducing effects of the emotion-discrimination tasks were examined by calculating mean mood self-ratings for the first and second half of responses during each activation task (the halfway point was determined by dividing the total number of ratings for each subject on each task by two). These mood rating data were analyzed by adding rating
period as a within-group (repeated measures) factor in the ANOVA. Kraemer’s Quality Receiver Operating Characteristic method (QROC; Kraemer, 1988) was applied to the percent correct, sensitivity, and specificity measures (as defined for the second hypothesis) to test which measure best discriminates patients from controls. The performance of patients with schizophrenia was compared to that of patients with depression (see Gur et al., 1992). The two patient groups are not directly comparable primarily because of age differences. Although scores were age-corrected within each group, this correction may not apply across the wider range. Therefore, to permit comparison of performance of patients with schizophrenia to that of patients with depression, the percent correct scores for each group were represented as z-score deviations from the respective control group. These were entered into an ANOVA design with diagnosis (schizophrenia, depression) as a between-group factor and task (age, happy, sad discrimination) as a withingroup (repeated measures) factor.
Results Hypothesis Testing. The analysis of the percent correct data across all tasks (including age discrimination) yielded a main effect for diagnosis (F= 21.69;df= 1, 38;p < O.OOl), with patients performing worse than controls, and a diagnosis X task interaction (F= 6.0;df= 1,38;p < 0.025;see Fig. 1). As in the first study on normal subjects (Erwin et al., 1992),the age-discrimination task was associated with lower performance than the emotion-discrimination tasks in controls, while patients performed relatively more poorly on the emotion-discrimination tasks than on the age-discrimination task compared with controls. The ANOVA of the sensitivity and specificity performance measures for the emotion-discrimination tasks yielded a main effect for diagnosis (F= 28.29;df= 1, 38;~ < O.OOl), with patients performing more poorly than controls, and a diagnosis X measure interaction (F = 9.06; df = 1, 38; p < 0.005; see Fig. 2). Patients had lower specificity than sensitivity relative to controls. Analyses of the negative and positive bias scores revealed main effects for diagnosis (F = 32.38; df = 1, 38; p < O.OOOl), with patients having higher bias scores,
259
Fig. 1. Means (fSEM) percent correct of patients with schizophrenia and normal controls for the three tasks
90-
es-
&
ki
au75 -
2 be
7O esLw-
. PATIENT3(N-20) o CONl=OU
SJ-
(N-20)
30-
AGE
HAP
SAD
TASK Fig. 2. Means (fSEM) for the sensitivity and specificity measures of patients and controls 1.0
I A-
0.9 -
w
0.a -
2 9 e
1 0.7 -
e %
OS-
‘\“‘:
I
0.5 -
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260 and for bias (F = 4.7 1; df = 1, 38; p < 0.05), with both patients and controls having higher positive than negative bias scores. Dividing patients into high and low severity groups (see Data Analysis section above) for each of the four clinical measures (emotional-nonemotional X specificnonspecific) yielded significant group effects for the two specific (emotional and nonemotional) divisions but not for either of the nonspecific divisions. For the emotional-specific division, a significant main effect for group was obtained (F = 6.45; df = 1, 18; p < 0.025). The high severity group had worse sensitivity and specificity. For the nonemotional-specific division, a significant group X measure interaction was obtained ( F= I 1.50; df = 1,38; p < 0.005). The high severity group in this case had lower specificity than sensitivity compared with the low severity group (see Fig. 3). Fig. 3. Means (fSEM) for the sensitivity and specificity measures of patients divided into high and low severity on the nonemotional specific symptoms
Mood-Inducing Effects of Tasks. The ANOVA on mood self-ratings obtained during task performance showed no significant effects or interactions. Patients and controls had mood ratings in the “mildly happy” range (3-3.5) and maintained this level throughout the study. Discrimination Power of Tasks. The seven performance scores (percent correct for age, happy-neutral, and sad-neutral discrimination and happy and sad sensitivity and specificity) were entered into the QROC analysis procedure (Kraemer, 1988).
261 The best discriminators between patients and controls were the percent correct scores for the happy-neutral task (point-biserial correlation = 0.64) and the sadneutral task (point-biserial correlation = 0.66). The best cutoff point was 92.8 for both scores. Of subjects scoring lower than this on the happy-neutral task, 84% were patients compared with only 19% of those scoring higher, yielding an odds ratio of 22.4. On the sad-neutral task, 88% of subjects scoring lower than 92.8 were patients compared with 22% of those scoring higher, for an odds ratio of 26. In contrast, for the age-discrimination task (point-biserial correlation of 0.40) the best cutoff was 79.4, and only 7lYo of subjects scoring lower were patients compared with 35% of those scoring higher, yielding an odds ratio of 4.5. Comparison with Depression. A diagnosis X task ANOVA showed a main effect of diagnosis (F = 15.41; df = 1, 32; p < O.OOl), with better performance characterizing the depression group, task (F = 13.06; df = 2, 64; p < O.OOl), and a diagnosis X task interaction (F = 9.76; df = 2, 64; p < 0.001; see Fig. 4). Schizophrenia is associated with greater decrement in the happy-neutral and sadneutral discrimination tasks relative to the age-discrimination task. Fig. 4. Means (+SEM) of the z-scores for the percent patients with schizophrenia and depression 1.0
,
0.5
-
0.0
_
T
-0.5
-
I
-1.0
Y
ii z
-2.5
s N’
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in
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correct
I
-3.0 -3.5 -4.0 /J
-4.5 -5.0 -I=;
,
:
i
-s.5 -6.0
AGE
T
D6PRCSSION P sauzm
HAPPY
SAD
TASK (N-14) @-EO)
Discussion The present schizophrenia
emotion-discrimination tasks revealed impairment in patients with compared with normal controls. As the QROC analysis indicated,
262 performance on the emotion-discrimination tasks clearly separates patients from controls. The performance deficit for the emotion-discrimination tasks was relatively greater than that for the age-discrimination task. This corroborates earlier reports of deficits in emotional discrimination in schizophrenia compared with cognitive control tasks (Cutting, 1981; Walker et al., 1984). Gessler et al. (1989), however, found that patients were as impaired on a happy-sad discrimination task as on an age-discrimination task. In our study, subjects were asked to make the more subtle discrimination of emotional from neutral faces. When signal-detection parameters were used to examine the subscores of the emotion-discrimination tasks, patients were found to be differentially impaired in specificity of discrimination. Thus, their emotion-discrimination performance was particularly impaired in the judgment of neutral faces as displaying emotion. Zuroff and Colussy (1986) similarly found that positive-neutral faces were more often rated by patients with schizophrenia as displaying negative affect. This is consistent with the clinical impression that some patients with schizophrenia may infuse emotional meaning into stimuli that appear neutral to normal subjects. As in other reports, the schizophrenic subjects had higher positive than negative bias scores in affect discrimination (Dougherty et al., 1974; Zuroff and Colussy, 1986; Gessler et al., 1989). This “Pollyanna tendency” (Boucher and Osgood, 1969) is also consistent with the “mildly happy” self-ratings of mood during task administration. However, unlike the patients in previous studies who had more difficulty in discriminating negative emotions (Dougherty et al., 1974; Muzekari and Bates, 1977), our patients showed similar levels of impairment in their ability to identify positive and negative emotions. This may reflect the comparable level of difficulty of our emotion-discrimination tasks (Chapman and Chapman, 1978). Levels of symptom severity were related to the performance patterns of patients. This was apparent for the symptoms judged to be specific to schizophrenia, whether emotional or nonemotional, but not for the nonspecific symptoms. Since our patients were acutely ill, the results can be seen as similar to those of Cutting (198 l), who reported that acutely psychotic patients perform less well on an emotional rating task than do chronically ill patients. Also, this finding underscores the hypothesis that a deficit in emotional discrimination is germane to the symptomatology of schizophrenia and may underlie some of its core features. Our data further suggest that, within the specific symptoms, distinct performance measures may differentially relate to emotional and nonemotional features. Both sensitivity and specificity for the emotion-discrimination tasks showed greater impairment in patients with severe emotional symptoms. For the nonemotional symptoms, while less severely ill patients had equal sensitivity and specificity in emotional discrimination, patients with more severe symptoms were differentially impaired in specificity. This suggests that the assignment of emotional meaning to neutral stimuli could be linked in schizophrenia to disturbed behavior in domains other than affect. Thus, while thought disorder is a core feature of schizophrenia, the present results are consistent with Bleuler’s emphasis on enduring features. Such affective or interpersonal symptoms could be, in part, manifestations of the emational processing deficit. It is noteworthy that a deficit in discriminating affect was observed in a patient
263
population with acute symptomatology and of generally recent onset. With two exceptions, no patients had more than four hospitalizations, and over half had never been hospitalized or treated with neuroleptics. This makes it less likely that our results merely reflect the effects of institutionalization, understimulating environments, and antipsychotic drugs (Carpenter et al., 1985). The comparison of schizophrenia with depression indicated that whereas patients with depression are specifically impaired in the discrimination of sad-neutral emotions, those with schizophrenia have deficits in both happy-neutral and sad-neutral discriminations. Thus, the performance of patients with schizophrenia showed greater impairment on the emotion-discrimination tasks than did that of patients with depression. Moreover, their disturbance in the emotion-discrimination tasks was relatively more severe than their deficit in the age-discrimination task. The interaction of cognitive and emotional domains in schizophrenia merits further investigation. The present results provide evidence for deficits in decoding affective connotations from faces. The effect is noticeable given the simplicity of the tasks (a limited number of emotions), which normal and depressed subjects were able to perform almost perfectly. By contrast, patients with schizophrenia were relatively less impaired on the age-discrimination task, which controls found more challenging. It is therefore unlikely that either task complexity or a generalized level of impairment accounts for the findings. Rather, it appears that schizophrenia is associated with serious difficulties in processing facial features that are associated with emotional expression. The integration of these findings with brain function in schizophrenia requires further research that may advance the understanding of its pathophysiology. Acknowedgments. We thank Maureen Mawhinney-Hee, R. E.E.G. T., Joseph Smailis, B.A., Fiona Gallacher, B.S., and Margaret Taleff, M.S., for assistance in phases of this project. We also thank Helena Kraemer, Ph.D., for statistical advice. This research is supported in part by the MacArthur Foundation Mental Health Research Network I and by National Institute of Mental Health grants MH-43880, MH-42191, lT32MH-19112, and Research Scientist Development Award MH-00586 (R.E.G.).
References Psychiatric Association. DSM-III-R: Diagnostic and Statistical Manual of Mental 3rd ed., revised. Washington, DC: American Psychiatric Press, 1987. Andreasen, N.C. Negative symptoms in schizophrenia. Archives of General Psychiatry,
American
Disorders.
34:784-788,
1982.
Andreasen, N.C., and Olsen, S. Negative vs. positive schizophrenia: Definition and validation. Archives of General Psychiatry, 39:789-794, 1982. Bleuler, E. Dementia Praecox or the Group of Schizophrenias. (1911) Translated by J. Zinkin. New York: International University Press, 1950. Boucher, J., and Osgood, C.E. The Pollyanna tendency. Journal of Verbal Learning and Verbal
Behaviour,
Carpenter, Schizophrenia
Chapman, Psychiatric
8: l-8, 1969.
W.T.;
Heinrichs, D.W.; and Alphs, L.D. Treatment of negative 111440-452, 1985. L.J., and Chapman, J.P. The measurement of differential deficits.
symptoms.
Bulletin,
Research,
14:303-311,
1978.
Journal
of
264 Cohen, J. Statistical Power Anal_vsi.s,fbr the Behavioral Sciences. 2nd ed. Hillside, NJ: Lawrence Erlbaum Associates, 1988. Cutting, J. Judgement of emotional expression in schizophrenics. British Journal of P.y_vchiatry, 139: l-6, I98 I. Dougherty, F.E.; Bartlett, E.S.; and Izard. C.E. Responses of schizophrenics to expressions of the fundamental emotions. Journal qf Clinical Psychology. 30:243-246, 1974. Ekman, P.; Friesen, W.V.; and Ellsworth, P. Emotions in the Human. Elmstead, NY: Pergamon Press. 1972. Erwin, R.J.; Cur. R.C.; Cur, R.E.; Skolnick, B.; Mawhinney-Hee, M.; and Smailis. J. Facial emotion discrimination: I. Task construction and behavioral findings in normal subjects. Psychiatry Research, 42123 I-240, 1992. Feinberg, T.E.; Rifkin, A.; Schaffer, C.; and Walker, E. Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Ps.vchiatry,
43:276-279,
1986.
Gessler, S.; Cutting, J.: Frith, C.D.; and Weinman, J. Schizophrenic inability to judge facial emotion: A controlled study. British Journal qf Clinical PLs_vchologv. 28: 19-29, 1989. Cur, R.C.; Erwin, R.J.; Cur, R.E.; Zwil, A.S.; Heimberg, C.: and Kraemer, H.C. Facial emotion discrimination: 11. Behavioral findings in depression. Ps_vchiutry Research, 42:241251,
1992.
Cur, R.E.; Mozley, D.; Resnick, S.M.; Levick. S.; Erwin, R.; Saykin. A.J.; and Cur, R.C. Relations among clinical scales in schizophrenia: Overlap and subtypes. American Journal qf Psychiatry,
148:472-478,
1991.
Cur, R.E.; Resnick. S.M.; and Cur, R.C. Laterality and frontality of cerebral blood flow and metabolism in schizophrenia: Relationship to symptom specificity. Ps.vchiatry Research, 27:325-334,
Hamilton,
1989.
M. A rating
scale for depression.
23:56-62. 1960. C.E. The Face ef Emotion.
Journal
of’ Neurology.
Neur0surger.v.
and
Psychiatry,
Izard, New York: Appleton-Century-Crofts, 197 I. Kraemer. H. Assessment of 2 X 2 associations: Generalization of signal-detection methodology. American Statistician. 42:37-49, 1988. Kraepelin, E. Dementia Praecox. Translated by R.M. Barclay. Edinburgh: E. & S. Livingstone, I9 19. Magaro, P.A., and Chamrad, D.L. Hemispheric preference of paranoid and nonparanoid schizophrenics. Biological Psychiatry, 18:1269-1285, 1983. Meehl, P.E. Nuisance variable and the ex post facto design. In: Radner, M., and Winokur, S., eds. Minnesota Studies in the Philosophy qf Science. Minneapolis: University of Minnesota Press, 1970. pp. 373-402. Morrison, R.L.; Bellack. A.S.; and Mueser, K.T. Deficits in facial-affect recognition and schizophrenia. Schizophrenia Bulletin, 14:67-83, 1988. Muzekari, L.H., and Bates, M.E. Judgement of emotion among chronic schizophrenics. Journal
of Clinical
Psychology.
33~662-666,
1977.
265 Novic, J.; Luchins, D.J.; and Perline, R. Facial affect recognition in schizophrenia: Is there a differential deficit? British Journal of Psychiatry, 144:533-537, 1984. Overall, J.R., and Gorham, D.R. The Brief Psychiatric Rating Scale. Journal of Operational Psychiatry, 11:48-64, 1980. Pilowsky, I., and Bassett, D. Schizophrenia and the response to facial emotions. Comprehensive Psychiatry, 21:236-244, 1980. SAS Institute. Statistical Analysis System. SAS, Inc., Box 800, Cat-y, NC, 1985. Shtasel, D.L.; Gur, R.E.; Mozley, P.D.; Richards, J.; Taleff, M.M.; Heimberg, C.; Gallacher, F.; and Gur, R.C. Volunteers for biomedical research: Recruitment and screening of normal controls. Archives of General Psychiatry, 48:1022-1025, 1991. Spielberger, C.D.; Gorsuch, R.L.; and Lushene, R.E. Manualfor the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press, 1970. Spitzer, R.L.; Endicott, J.; and Robins, E. Research Diagnostic Criteria. New York: New York State Psychiatric Institute, 1975. Spitzer, R.L.; Williams, J.B.W.; and Gibbon, M. Structured Clinical Interviewfor DSMIII-R-Patient Version @CID-P, 10/Z/86). New York: New York State Psychiatric Institute, 1986. Walker, E.; McGuire, M.; and Bettes, B. Recognition and identification of facial stimuli by schizophrenics and patients with affective disorders. British Journal of Clinical Psychology, 23:37-44, 1984. Zevon, M.A., and Tellegen, A. The structure of mood change: An idiographic/nomothetic analysis. Journal of Personality and Social Psychology, 43: 11l-122, 1982. Zuroff, D.C., and Colussy, S.A. Emotion recognition in schizophrenic and depressed patients. Journal of Clinical Psychology, 42:41 I-417, 1986.
Ps.vchiatry Research, 421253-265 Elsevier
Facial Emotion Schizophrenia
Discrimination:
Carolyn Heimberg, Ruben C. Gur
Raquel E. Gur, Roland J. Erwin,
Received
October
IS, 1991; revised
version
received
III. Behavioral
February
Findings
Derri L. Shtasel,
24, 1992; accepted
April
in
and
12, 1992.
Abstract. Emotional
discrimination was studied in patients with schizophrenia (n = 20) and matched controls. Performance of the emotion-discrimination tasks in the schizophrenic patients was impaired, relative to their performance of an age-discrimination task. Performance patterns in the patient group could also be reliably distinguished from those of normal controls. The impairment was associated with the severity of both emotional and nonemotional symptoms specific to schizophrenia, but not with the severity of nonspecific symptoms. The deficit associated with schizophrenia is more marked than that reported for depression (Gur et al., 1992), particularly for the emotion-discrimination tasks, and showed no difference between “happy” discrimination and “sad” discrimination. The main difficulty in patients with schizophrenia is the assignment of emotional valence to neutral faces. The magnitude of the deficit underscores the salience of emotional impairment in schizophrenia, and its relation to cognitive dysfunction in this disorder merits further scrutiny. Key Words. Affect recognition,
depression,
psychiatric
symptoms.
Although disturbed cognition has been considered the hallmark of schizophrenia, disturbed affect is also a recognized feature. Early descriptions included lack of relatedness (Kraepelin, 1919) and inappropriate and blunted affect (Bleuler, 1911/ 1950). Advances in the study of human emotions (e.g., Izard, 1971; Ekman et al., 1972) have provided tools to measure individual differences in the ability to recognize facial affect. This domain has gained interest with the growing understanding of the neuropsychology of emotions and has been applied to patients with schizophrenia. Despite methodologic heterogeneity in studies of affect recognition (Morrison et al., 1988) some consistent findings have emerged. Patients with schizophrenia perform less well than depressed patients, and both groups perform more poorly than normal controls (Cutting, 1981; Walker et al., 1984; Feinberg et al., 1986;
Carolyn Heimberg, M.D., is Postdoctoral Fellow; Raquel E. Gur, M.D., Ph.D., and Ruben C. Gur, Ph.D., are Professors; and Roland J. Erwin, Ph.D., and Derri L. Shtasel, M.D., are Assistant Professors, all in the Department of Psychiatry, University of Pennsylvania, Philadelphia, was submitted. (Reprint requests to Dr. R.E. Gur, Neuropsychiatry Program, Floor Gates Bldg., University of Pennsylvania, 3500 Spruce St., Philadelphia, 0165-1781/92/$05.00
@ 1992 Elsevier Scientific
Publishers
Ireland
Ltd.
PA, at the time this report Dept. of Psychiatry, 10th PA 19104-4283, USA.)
254 Zuroff and Colussy, 1986; Gessler et al., 1989). The performance deficit in psychiatric patients has been particularly marked in the detection of negative emotions (Dougherty et al., 1974; Muzekari and Bates, 1977; Novic et al., 1984). Chronicity is associated with relatively better affect discrimination than is seen in acute psychosis (Cutting, 1981; Gessler et al., 1989). Patients have usually performed well on control tasks, including age discrimination and facial identity (Cutting, 1981; Walker et al., 1984; Gessler et al., 1989). Finally, affect-recognition tasks are associated with better performance than affect-labeling tasks (Dougherty et al., 1974; Walker et al., 1984; Feinberg et al., 1986). Inconsistencies between studies relate to differences in both subject populations and procedures. Patients have received diagnoses under differing classification systems (e.g., DSM-III-R [American Psychiatric Association, 19871, the Structured Clinical Interview for DSM-III-R [SCID; Spitzer et al., 19861, and Research Diagnostic Criteria [Spitzer et al., 19751); have included those with schizoaffective illness (Walker et al., 1984); have had divergent courses of illness with variable or undocumented medication status; and in some cases have been limited to females (Dougherty et al., 1974; Zuroff and Colussy, 1986). Control groups have not always been studied, though more recent investigations have included patients with affective disorders as well as normal controls. Procedural variation exists in stimuli, task administration, and response mode. Most studies used a set of black and white stimulus photographs from the Izard or Ekman batteries (Izard, 1971; Ekman et al., 1972), but other stimuli (Muzekari and Bates, 1977; Cutting, 1981; Magaro and Chamrad, 1983) have also been used. Even among those investigators who used material from the batteries, there are procedural variations in supplementing stimuli, use of adjunctive tasks (Novic et al., 1984; Walker et al., 1984; Zuroff and Colussy, I986), types of response sought (Dougherty et al., 1974; Pilowsky and Bassett, 1980; Cutting, 1981; Zuroff and Colussy, 1986), and stimulus-display methods (Feinberg et al., 1986). Furthermore, in the few studies that controlled for stimulus-exposure interval, duration of exposure varied from 500 msec to 5 minutes (Muzekari and Bates, 1977; Walker et al., 1984; Zuroff and Colussy, 1986; Gessler et al., 1989). Only a few studies of affect recognition in schizophrenia also conducted analyses of symptomatology that had a greater scope than what was required for diagnosis and subtyping (Muzekari and Bates, 1977; Novic et al., 1984; Zuroff and Colussy, 1986). Where such ratings were discussed, no significant relationship between clinical characteristics and response accuracy was found (Muzekari and Bates, 1977; Novic et al., 1984). The purpose of the present study was to apply standard procedures examined in normal subjects and patients with affective illness to a sample of patients with schizophrenia. We hypothesized that patients with schizophrenia would be impaired in their ability to discriminate emotions accurately. The application of standard diagnostic procedures and rating scales (Gur et al., 1991) permitted us to examine the relationships between affect-relevant symptomatology and affect recognition. We expected to find an association between task performance and severity of symptoms, especially in the affective domain.
255
Methods Subjects. The sample consisted of 20 patients (10 men, 10 women) from our Mental Health Clinical Research Center who received DSM-III-R diagnoses of schizophrenia (see Table I). They underwent medical, neurologic, and structured psychiatric evaluations, and were free of any other axis I disorder including substance abuse (Gur et al., 1991). Other exclusionary criteria for patients were as follows: history of neurologic disease including head trauma with loss of consciousness, history of medical disorders that might affect central nervous system function, and inability to cooperate with testing (e.g., inability to understand the task or excessive agitation). Notably, 11 patients were neuroleptic-naive at the time of testing, while 8 of the remaining 9 patients had not received neuroleptics for 2 or more weeks. For 1 I patients, this was the first psychiatric hospitalization. The mean age of the schizophrenic patients was 27.5 (SD = 6.2; range = 18-39) years. Control subjects were healthy volunteers (10 men, 10 women) who were matched to the patients on race (7 black, 13 white), handedness (3 left-handed), and sociodemographic variables. The mean age of the controls was 29.5 (SD = 8.7; range = 19-49) years. Controls underwent assessment procedures as described above for patients (Shtasel et al., 1991). Exclusionary criteria for controls were the same as those for patients, with the following additional requirements: (I) absence of axis II diagnosis of schizoid or schizotypal personality disorder and (2) absence of a history of first degree relatives with diagnoses of schizophrenia or affective disorder. While controls and patients were not comparable in the number of years of education (controls: mean = 15.0, SD = 2.4; patients: mean = 12.8, SD = 1.7; r = 3.47, p < O.Ol), they were balanced for parental education (controls: mean = 13.3, SD = 2.8; patients: mean = 13.1, SD = 2.0; f = 0.25, NS). Since schizophrenia is a disease that affects educational attainment (the “matching fallacy”; Meehl [ 1970]), parental level of education was considered a more valid index of sociodemographic background. Assessment and Rating Scales. Patient assessments and ratings were performed by research psychiatrists from the Mental Health Clinical Research Center (C.H., D.S., and R.E.G.). On the basis of clinical interviews and the SCID (Spitzer et al., 1986), the following rating scales were completed: the Brief Psychiatric Rating Scale (BPRS; Overall and Gorham, 1980) the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen and Olsen, 1982), the Scale for the Assessment of Negative Symptoms (SANS; Andreasen, 1982; Andreasen and Olsen, 1982) and the Hamilton Rating Scale for Depression (HRSD; Hamilton, 1960). Interrater reliabilities ranged from intraclass correlations of 0.74 to 0.95. Gur et al. (1989) described a method for developing a symptom specificity index for schizophrenia. This procedure divided the 18-item BPRS into symptoms considered specific to schizophrenia (emotional withdrawal, conceptual disorganization, mannerisms and posturing, grandiosity, suspiciousness, hallucinatory behavior, unusual thought content, and blunted affect) and nonspecific symptoms (somatic concern, anxiety, guilt feelings, tension, depressive mood, hostility, motor retardation, uncooperativeness, excitement, and disorientation). To examine the relationship between affective symptoms and emotional discrimination, this approach was adapted to the BPRS, SANS, and SAPS. Items of the scales assessing affect were identified by the three research psychiatrists, and consensus was achieved. Our determination of which items were more “schizophrenia-affect specific” was based on the premise that the presence of these symptoms is more characteristic of schizophrenia than of other major psychiatric disorders. The affect-nonspecific items were considered more likely to exist in any axis I disorder (Table 2). Task Administration. The facial discrimination tasks fell neutral, and sad-neutral. Task development and application in part I of this series of reports (Erwin et al., 1992). In professionai actors who were instructed to express happy
into three categories: age, happyto normal subjects was described brief, photographs were made of and sad faces. For the emotion-
18 30 35 31 33 31 20 36 23
B
B
W
B
W
B
B
B
B
W
B
M
F
F
F
F
F
F
F
F
F
F
10
11
12
13
14
15
16
17
18
19
20
21
D
16
20
P
D
33 26
P
C
R
L
11
U
P
P
R R
U
R
19
21
36
20
22
P
R R
30
21
D
R
U
P
R
19
P
L R
17
17
P
R
R
19
P
L R
21
24
P U
L R
U
R 21
22
U
Age at onset
R
Subtype
R
14
11
12
12
12
16
12
14
12
12
13
10
15
16
14
16
14
12
12
Education Handedness (yr)
1. Number of weeks that patrents had not been recerving neuroleptrcs; N = drug-narve.
Note. U = undrfferentiated. D = drsorganized. P = paranoid. M = male. F = female. W = whrte. 8 = black. R = right. L = left
23
20
19
W
8
29
M
M
7
25
9
M
6
25
B
26
M
5
B
M
4
29
w w
33
39
M
M
3
w w
Age (yr)
24
M
Race
w w
M
1
Sex
2
Patient No.
Table 1. Patient characteristics
0
0
1
0
0
1
0
0
4
1
0
0
2
0
0
3
0
2
10
25
Number of hospitalizations
N
N
N
N
3
N
3
N
2
0
N
N
2
N
N
12
N
231
10
26
Drug free’ (wk)
257 discrimination tasks, neutral and target emotion slides were intermixed, while for, the agediscrimination task, neutral faces were used. Cues were given at regular intervals within each task for subjects to rate their own emotional states. Mood and anxiety were assessed before and after the study with the Positive and Negative Affect Scale (PANAS; Zevon and Tellegen, 1982) and the State-Trait Anxiety Inventory (STAI; Spielberger et al., 1970).
Table 2. Emotion ratings BPRS:
Affect-Schizophrenia
Affect-General
Emotional
Anxiety
withdrawal
Guilt feelings
Blunted affect
Tension Depressive mood Hostility Excitement
SANS:
Unchanging
facial expression
Paucity of expressive
Decreased
spontaneous
movements
gestures
Poor eye contact Affective nonresponsivity Inappropriate
affect
Lack of vocal inflections Intimacy/closeness
with family/
significant other’ Relationships
with friends/peers’
Note. BPRS = Brief Psychiatric Rating Scale. SANS = Scale for the Assessment of Negative Symptoms. No items from the Scale for the Assessment of Positive Symptoms were considered to be relevant measures of affect. SANS item scores for interpersonal skills (intimacy/closeness
and relationships) were averaged
Data Analysis. Quantitation of the performance data was described by Erwin et al. (1992). In brief, the number of true positives (i.e., response in the “happy”range for a happy slide in the happy discrimination task and in the “sad” range for a sad slide in the sad discrimination task), false positives (scores in the emotional range for neutral stimuli), true negatives (neutral responses to neutral faces), and false negatives (neutral responses to emotional faces) were computed for each task. Percent correct was computed for all tasks as lOO*(total number of correct responses/ total number of items completed). For the emotional tasks, four additional measures were computed: sensitivity and specificity for each task separately, and positive and negative bias across tasks. Sensitivity was defined as true positives/(true positives + false negatives). This is a measure of how “sensitive” subjects are to the presence of the correct emotion. Specificity was defined as true negatives/(true negatives + false positives). This is a measure of how well subjects discriminate neutral from emotional stimuli. Sensitivity and specificity measures were not available for the age-discrimination task. Positive bias across tasks was computed as (happy-neutral false positives i- sad-neutral false negatives)/(total attempted happy-neutral positives + total attempted sad-neutral negatives), and negative bias was computed as (happy-neutral false negatives i- sad-neutral false positives)/(total attempted happy-neutral negatives -I- total attempted sad-neutral positives). The formula 2*arc sine of the square root of the proportion, as recommended by Cohen (1988), was used to transform all proportions. The effects of normal aging, sex, and the age X sex interaction were removed by regression procedures described in part II (Cur et al., 1992). Thus, the performance data submitted for statistical analysis were not influenced by effects of age and sex on normal performance. Statistical analysis was aimed at testing the hypotheses, possible mood-inducing effects of
258 the tasks, the discriminatory power of the tasks, and differences between patients with schizophrenia and patients with depression. The hypotheses were evaluated as follows: (1) Percent correct, sensitivity and specificity, and bias scores were compared between patients and controls in mixed model repeated measures analyses of variance (ANOVAs; SAS Institute, 1985), with diagnosis as a grouping factor. The within-group (repeated measures) factors were task (age discrimination, happyneutral, and sad-neutral) for the percent correct measure, task (happy-neutral, sad-neutral), and measure (sensitivity and specificity) for analyses restricted to the emotion-discrimination tasks, and bias (positive and negative) for the bias measures. (2) The association between task performance and severity of symptoms in patients was tested by first dividing patients into high and low severity (median cutoff) for emotional-specific, emotional-nonspecific, nonemotional-specific and nonemotional-nonspecific symptoms (see detailed description above). High and low severity for each of these four dimensions served as a grouping factor in separate ANOVAs with measure (sensitivity and specificity across emotion-discrimination tasks) as the within-group (repeated measures) factor. Both main effects and interactions were examined. The possible mood-inducing effects of the emotion-discrimination tasks were examined by calculating mean mood self-ratings for the first and second half of responses during each activation task (the halfway point was determined by dividing the total number of ratings for each subject on each task by two). These mood rating data were analyzed by adding rating
period as a within-group (repeated measures) factor in the ANOVA. Kraemer’s Quality Receiver Operating Characteristic method (QROC; Kraemer, 1988) was applied to the percent correct, sensitivity, and specificity measures (as defined for the second hypothesis) to test which measure best discriminates patients from controls. The performance of patients with schizophrenia was compared to that of patients with depression (see Gur et al., 1992). The two patient groups are not directly comparable primarily because of age differences. Although scores were age-corrected within each group, this correction may not apply across the wider range. Therefore, to permit comparison of performance of patients with schizophrenia to that of patients with depression, the percent correct scores for each group were represented as z-score deviations from the respective control group. These were entered into an ANOVA design with diagnosis (schizophrenia, depression) as a between-group factor and task (age, happy, sad discrimination) as a withingroup (repeated measures) factor.
Results Hypothesis Testing. The analysis of the percent correct data across all tasks (including age discrimination) yielded a main effect for diagnosis (F= 21.69;df= 1, 38;p < O.OOl), with patients performing worse than controls, and a diagnosis X task interaction (F= 6.0;df= 1,38;p < 0.025;see Fig. 1). As in the first study on normal subjects (Erwin et al., 1992),the age-discrimination task was associated with lower performance than the emotion-discrimination tasks in controls, while patients performed relatively more poorly on the emotion-discrimination tasks than on the age-discrimination task compared with controls. The ANOVA of the sensitivity and specificity performance measures for the emotion-discrimination tasks yielded a main effect for diagnosis (F= 28.29;df= 1, 38;~ < O.OOl), with patients performing more poorly than controls, and a diagnosis X measure interaction (F = 9.06; df = 1, 38; p < 0.005; see Fig. 2). Patients had lower specificity than sensitivity relative to controls. Analyses of the negative and positive bias scores revealed main effects for diagnosis (F = 32.38; df = 1, 38; p < O.OOOl), with patients having higher bias scores,
259
Fig. 1. Means (fSEM) percent correct of patients with schizophrenia and normal controls for the three tasks
90-
es-
&
ki
au75 -
2 be
7O esLw-
. PATIENT3(N-20) o CONl=OU
SJ-
(N-20)
30-
AGE
HAP
SAD
TASK Fig. 2. Means (fSEM) for the sensitivity and specificity measures of patients and controls 1.0
I A-
0.9 -
w
0.a -
2 9 e
1 0.7 -
e %
OS-
‘\“‘:
I
0.5 -
0.4
SENSITlVlW v rwnmls@20) ACOBTROIBR(-ZO)
BPECIPICITI
!
260 and for bias (F = 4.7 1; df = 1, 38; p < 0.05), with both patients and controls having higher positive than negative bias scores. Dividing patients into high and low severity groups (see Data Analysis section above) for each of the four clinical measures (emotional-nonemotional X specificnonspecific) yielded significant group effects for the two specific (emotional and nonemotional) divisions but not for either of the nonspecific divisions. For the emotional-specific division, a significant main effect for group was obtained (F = 6.45; df = 1, 18; p < 0.025). The high severity group had worse sensitivity and specificity. For the nonemotional-specific division, a significant group X measure interaction was obtained ( F= I 1.50; df = 1,38; p < 0.005). The high severity group in this case had lower specificity than sensitivity compared with the low severity group (see Fig. 3). Fig. 3. Means (fSEM) for the sensitivity and specificity measures of patients divided into high and low severity on the nonemotional specific symptoms
Mood-Inducing Effects of Tasks. The ANOVA on mood self-ratings obtained during task performance showed no significant effects or interactions. Patients and controls had mood ratings in the “mildly happy” range (3-3.5) and maintained this level throughout the study. Discrimination Power of Tasks. The seven performance scores (percent correct for age, happy-neutral, and sad-neutral discrimination and happy and sad sensitivity and specificity) were entered into the QROC analysis procedure (Kraemer, 1988).
261 The best discriminators between patients and controls were the percent correct scores for the happy-neutral task (point-biserial correlation = 0.64) and the sadneutral task (point-biserial correlation = 0.66). The best cutoff point was 92.8 for both scores. Of subjects scoring lower than this on the happy-neutral task, 84% were patients compared with only 19% of those scoring higher, yielding an odds ratio of 22.4. On the sad-neutral task, 88% of subjects scoring lower than 92.8 were patients compared with 22% of those scoring higher, for an odds ratio of 26. In contrast, for the age-discrimination task (point-biserial correlation of 0.40) the best cutoff was 79.4, and only 7lYo of subjects scoring lower were patients compared with 35% of those scoring higher, yielding an odds ratio of 4.5. Comparison with Depression. A diagnosis X task ANOVA showed a main effect of diagnosis (F = 15.41; df = 1, 32; p < O.OOl), with better performance characterizing the depression group, task (F = 13.06; df = 2, 64; p < O.OOl), and a diagnosis X task interaction (F = 9.76; df = 2, 64; p < 0.001; see Fig. 4). Schizophrenia is associated with greater decrement in the happy-neutral and sadneutral discrimination tasks relative to the age-discrimination task. Fig. 4. Means (+SEM) of the z-scores for the percent patients with schizophrenia and depression 1.0
,
0.5
-
0.0
_
T
-0.5
-
I
-1.0
Y
ii z
-2.5
s N’
measures
in
I
L -2.0
correct
I
-3.0 -3.5 -4.0 /J
-4.5 -5.0 -I=;
,
:
i
-s.5 -6.0
AGE
T
D6PRCSSION P sauzm
HAPPY
SAD
TASK (N-14) @-EO)
Discussion The present schizophrenia
emotion-discrimination tasks revealed impairment in patients with compared with normal controls. As the QROC analysis indicated,
262 performance on the emotion-discrimination tasks clearly separates patients from controls. The performance deficit for the emotion-discrimination tasks was relatively greater than that for the age-discrimination task. This corroborates earlier reports of deficits in emotional discrimination in schizophrenia compared with cognitive control tasks (Cutting, 1981; Walker et al., 1984). Gessler et al. (1989), however, found that patients were as impaired on a happy-sad discrimination task as on an age-discrimination task. In our study, subjects were asked to make the more subtle discrimination of emotional from neutral faces. When signal-detection parameters were used to examine the subscores of the emotion-discrimination tasks, patients were found to be differentially impaired in specificity of discrimination. Thus, their emotion-discrimination performance was particularly impaired in the judgment of neutral faces as displaying emotion. Zuroff and Colussy (1986) similarly found that positive-neutral faces were more often rated by patients with schizophrenia as displaying negative affect. This is consistent with the clinical impression that some patients with schizophrenia may infuse emotional meaning into stimuli that appear neutral to normal subjects. As in other reports, the schizophrenic subjects had higher positive than negative bias scores in affect discrimination (Dougherty et al., 1974; Zuroff and Colussy, 1986; Gessler et al., 1989). This “Pollyanna tendency” (Boucher and Osgood, 1969) is also consistent with the “mildly happy” self-ratings of mood during task administration. However, unlike the patients in previous studies who had more difficulty in discriminating negative emotions (Dougherty et al., 1974; Muzekari and Bates, 1977), our patients showed similar levels of impairment in their ability to identify positive and negative emotions. This may reflect the comparable level of difficulty of our emotion-discrimination tasks (Chapman and Chapman, 1978). Levels of symptom severity were related to the performance patterns of patients. This was apparent for the symptoms judged to be specific to schizophrenia, whether emotional or nonemotional, but not for the nonspecific symptoms. Since our patients were acutely ill, the results can be seen as similar to those of Cutting (198 l), who reported that acutely psychotic patients perform less well on an emotional rating task than do chronically ill patients. Also, this finding underscores the hypothesis that a deficit in emotional discrimination is germane to the symptomatology of schizophrenia and may underlie some of its core features. Our data further suggest that, within the specific symptoms, distinct performance measures may differentially relate to emotional and nonemotional features. Both sensitivity and specificity for the emotion-discrimination tasks showed greater impairment in patients with severe emotional symptoms. For the nonemotional symptoms, while less severely ill patients had equal sensitivity and specificity in emotional discrimination, patients with more severe symptoms were differentially impaired in specificity. This suggests that the assignment of emotional meaning to neutral stimuli could be linked in schizophrenia to disturbed behavior in domains other than affect. Thus, while thought disorder is a core feature of schizophrenia, the present results are consistent with Bleuler’s emphasis on enduring features. Such affective or interpersonal symptoms could be, in part, manifestations of the emational processing deficit. It is noteworthy that a deficit in discriminating affect was observed in a patient
263
population with acute symptomatology and of generally recent onset. With two exceptions, no patients had more than four hospitalizations, and over half had never been hospitalized or treated with neuroleptics. This makes it less likely that our results merely reflect the effects of institutionalization, understimulating environments, and antipsychotic drugs (Carpenter et al., 1985). The comparison of schizophrenia with depression indicated that whereas patients with depression are specifically impaired in the discrimination of sad-neutral emotions, those with schizophrenia have deficits in both happy-neutral and sad-neutral discriminations. Thus, the performance of patients with schizophrenia showed greater impairment on the emotion-discrimination tasks than did that of patients with depression. Moreover, their disturbance in the emotion-discrimination tasks was relatively more severe than their deficit in the age-discrimination task. The interaction of cognitive and emotional domains in schizophrenia merits further investigation. The present results provide evidence for deficits in decoding affective connotations from faces. The effect is noticeable given the simplicity of the tasks (a limited number of emotions), which normal and depressed subjects were able to perform almost perfectly. By contrast, patients with schizophrenia were relatively less impaired on the age-discrimination task, which controls found more challenging. It is therefore unlikely that either task complexity or a generalized level of impairment accounts for the findings. Rather, it appears that schizophrenia is associated with serious difficulties in processing facial features that are associated with emotional expression. The integration of these findings with brain function in schizophrenia requires further research that may advance the understanding of its pathophysiology. Acknowedgments. We thank Maureen Mawhinney-Hee, R. E.E.G. T., Joseph Smailis, B.A., Fiona Gallacher, B.S., and Margaret Taleff, M.S., for assistance in phases of this project. We also thank Helena Kraemer, Ph.D., for statistical advice. This research is supported in part by the MacArthur Foundation Mental Health Research Network I and by National Institute of Mental Health grants MH-43880, MH-42191, lT32MH-19112, and Research Scientist Development Award MH-00586 (R.E.G.).
References Psychiatric Association. DSM-III-R: Diagnostic and Statistical Manual of Mental 3rd ed., revised. Washington, DC: American Psychiatric Press, 1987. Andreasen, N.C. Negative symptoms in schizophrenia. Archives of General Psychiatry,
American
Disorders.
34:784-788,
1982.
Andreasen, N.C., and Olsen, S. Negative vs. positive schizophrenia: Definition and validation. Archives of General Psychiatry, 39:789-794, 1982. Bleuler, E. Dementia Praecox or the Group of Schizophrenias. (1911) Translated by J. Zinkin. New York: International University Press, 1950. Boucher, J., and Osgood, C.E. The Pollyanna tendency. Journal of Verbal Learning and Verbal
Behaviour,
Carpenter, Schizophrenia
Chapman, Psychiatric
8: l-8, 1969.
W.T.;
Heinrichs, D.W.; and Alphs, L.D. Treatment of negative 111440-452, 1985. L.J., and Chapman, J.P. The measurement of differential deficits.
symptoms.
Bulletin,
Research,
14:303-311,
1978.
Journal
of
264 Cohen, J. Statistical Power Anal_vsi.s,fbr the Behavioral Sciences. 2nd ed. Hillside, NJ: Lawrence Erlbaum Associates, 1988. Cutting, J. Judgement of emotional expression in schizophrenics. British Journal of P.y_vchiatry, 139: l-6, I98 I. Dougherty, F.E.; Bartlett, E.S.; and Izard. C.E. Responses of schizophrenics to expressions of the fundamental emotions. Journal qf Clinical Psychology. 30:243-246, 1974. Ekman, P.; Friesen, W.V.; and Ellsworth, P. Emotions in the Human. Elmstead, NY: Pergamon Press. 1972. Erwin, R.J.; Cur. R.C.; Cur, R.E.; Skolnick, B.; Mawhinney-Hee, M.; and Smailis. J. Facial emotion discrimination: I. Task construction and behavioral findings in normal subjects. Psychiatry Research, 42123 I-240, 1992. Feinberg, T.E.; Rifkin, A.; Schaffer, C.; and Walker, E. Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Ps.vchiatry,
43:276-279,
1986.
Gessler, S.; Cutting, J.: Frith, C.D.; and Weinman, J. Schizophrenic inability to judge facial emotion: A controlled study. British Journal qf Clinical PLs_vchologv. 28: 19-29, 1989. Cur, R.C.; Erwin, R.J.; Cur, R.E.; Zwil, A.S.; Heimberg, C.: and Kraemer, H.C. Facial emotion discrimination: 11. Behavioral findings in depression. Ps_vchiutry Research, 42:241251,
1992.
Cur, R.E.; Mozley, D.; Resnick, S.M.; Levick. S.; Erwin, R.; Saykin. A.J.; and Cur, R.C. Relations among clinical scales in schizophrenia: Overlap and subtypes. American Journal qf Psychiatry,
148:472-478,
1991.
Cur, R.E.; Resnick. S.M.; and Cur, R.C. Laterality and frontality of cerebral blood flow and metabolism in schizophrenia: Relationship to symptom specificity. Ps.vchiatry Research, 27:325-334,
Hamilton,
1989.
M. A rating
scale for depression.
23:56-62. 1960. C.E. The Face ef Emotion.
Journal
of’ Neurology.
Neur0surger.v.
and
Psychiatry,
Izard, New York: Appleton-Century-Crofts, 197 I. Kraemer. H. Assessment of 2 X 2 associations: Generalization of signal-detection methodology. American Statistician. 42:37-49, 1988. Kraepelin, E. Dementia Praecox. Translated by R.M. Barclay. Edinburgh: E. & S. Livingstone, I9 19. Magaro, P.A., and Chamrad, D.L. Hemispheric preference of paranoid and nonparanoid schizophrenics. Biological Psychiatry, 18:1269-1285, 1983. Meehl, P.E. Nuisance variable and the ex post facto design. In: Radner, M., and Winokur, S., eds. Minnesota Studies in the Philosophy qf Science. Minneapolis: University of Minnesota Press, 1970. pp. 373-402. Morrison, R.L.; Bellack. A.S.; and Mueser, K.T. Deficits in facial-affect recognition and schizophrenia. Schizophrenia Bulletin, 14:67-83, 1988. Muzekari, L.H., and Bates, M.E. Judgement of emotion among chronic schizophrenics. Journal
of Clinical
Psychology.
33~662-666,
1977.
265 Novic, J.; Luchins, D.J.; and Perline, R. Facial affect recognition in schizophrenia: Is there a differential deficit? British Journal of Psychiatry, 144:533-537, 1984. Overall, J.R., and Gorham, D.R. The Brief Psychiatric Rating Scale. Journal of Operational Psychiatry, 11:48-64, 1980. Pilowsky, I., and Bassett, D. Schizophrenia and the response to facial emotions. Comprehensive Psychiatry, 21:236-244, 1980. SAS Institute. Statistical Analysis System. SAS, Inc., Box 800, Cat-y, NC, 1985. Shtasel, D.L.; Gur, R.E.; Mozley, P.D.; Richards, J.; Taleff, M.M.; Heimberg, C.; Gallacher, F.; and Gur, R.C. Volunteers for biomedical research: Recruitment and screening of normal controls. Archives of General Psychiatry, 48:1022-1025, 1991. Spielberger, C.D.; Gorsuch, R.L.; and Lushene, R.E. Manualfor the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press, 1970. Spitzer, R.L.; Endicott, J.; and Robins, E. Research Diagnostic Criteria. New York: New York State Psychiatric Institute, 1975. Spitzer, R.L.; Williams, J.B.W.; and Gibbon, M. Structured Clinical Interviewfor DSMIII-R-Patient Version @CID-P, 10/Z/86). New York: New York State Psychiatric Institute, 1986. Walker, E.; McGuire, M.; and Bettes, B. Recognition and identification of facial stimuli by schizophrenics and patients with affective disorders. British Journal of Clinical Psychology, 23:37-44, 1984. Zevon, M.A., and Tellegen, A. The structure of mood change: An idiographic/nomothetic analysis. Journal of Personality and Social Psychology, 43: 11l-122, 1982. Zuroff, D.C., and Colussy, S.A. Emotion recognition in schizophrenic and depressed patients. Journal of Clinical Psychology, 42:41 I-417, 1986.
