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Association with Symptomatology and Cognition

Christian G. Kohler, Warren Bilker, Michael Hagendoorn, Raquel E. Gur, and

Ruben C. Gur

Background:Previous investigations have found impaired recognition of facial affect in schizophrenia. Controversy exists as to whether this impairment represents a specific emotion recognition deficit when compared with other face recognition control tasks. Regardless of whether the emotion processing deficit is differential, it may uniquely influence other manifestations of schizophrenia. We compared patients and healthy control subjects on computerized tasks of emo-tion and age recogniemo-tion. Performances on emoemo-tion and age recognition tasks were correlated with cognitive functioning and with symptomatology.

Methods:Thirty-five patients with schizophrenia and 45 healthy people underwent computerized testing for emo-tion and age recogniemo-tion. Participants were assessed neuropsychologically, and patients were rated for positive and negative symptoms.

Results:The patients with schizophrenia performed worse than control subjects on emotion and age recognition without differential deficit. In both groups, we found higher error rates for identification of emotion in female faces and for identification of sad versus happy faces. In schizophrenic patients, emotion but not age recognition correlated with severity of negative and positive symp-toms. In healthy control subjects, neither task correlated with cognitive functions. In schizophrenic patients, emo-tion but not age recogniemo-tion correlated with attenemo-tion, verbal and spatial memory, and language abilities. Conclusions:This study did not reveal a specific deficit for emotion recognition in schizophrenia; however, our findings lend support to the concept that emotion recognition is uniquely associated in schizophrenia with core symptomatol-ogy and cognitive domains. Biol Psychiatry 2000;48: 127–136 ©2000 Society of Biological Psychiatry

Key Words:Emotion recognition, schizophrenia, gender, cognition

Introduction

P

rocessing of affect is an important component of social interaction (Anthony 1978; Charlesworth 1982; Izard 1971) and is supported by distributed neural systems (Damasio 1998; Heilman and Gilmore 1998; Lang et al 1998; Leventhal and Tomarken 1986; Mesulam 1998). Impaired processing of emotion has been noted in a range of disorders, including focal brain lesions (Adolphs et al 1994, 1996; Blonder et al 1991; Borod et al 1993; Bowers et al 1991; Sackeim et al 1982), Huntington’s Disease (Jacobs et al 1995), Parkinson’s Disease (Adolphs et al 1998), and neuro-psychiatric disorders (Feinberg et al 1986; Gur et al 1992; Mikhailova et al 1996; Walker et al 1984). The study of emotion processing domains, including recognition, experi-ence and expression, has benefitted from the use of standard-ized facial stimuli (Ekman et al 1972).

Abnormalities in emotional expression and experience have been reported since the earliest descriptions of schizophrenia (Bleuler 1911). More recently, deficits in facial-affect recognition also have been noted; however, an issue has been raised as to whether a differential deficit can be demonstrated against the more general impairment in facial processing (Kerr and Neale 1993; Salem et al 1996). Some studies support a differential deficit. Cutting (1981) reported that acutely ill schizophrenic patients performed poorly relative to patients in remission and patients with psychotic depression on an affect discrimi-nation task, which compared “friendliness” and “mean-ness,” but not on color discrimination and age perception tasks. Walker et al (1984) studied patients with chronic schizophrenia, affective disorder, and healthy control sub-jects. Three emotional tasks of 16 faces each were used to probe emotion discrimination, emotion labeling, and mul-tiple choice assignment of six different emotional valences (happiness, anger, fear, sadness, surprise, and shame) but not neutral faces. Although patients with schizophrenia performed as well as control subjects on the Benton Facial Recognition Test (Benton and Van Allen 1968), their performance on recognition of affect was significantly below the level of both control subjects and patients with affective disorders. Heimberg et al (1992) likewise

re-From the Schizophrenia Research Center, Neuropsychiatry Section, Department of Psychiatry (CGK, MH, REG, RCG) and the Department of Biostatistics and Epidemiology (WB), University of Pennsylvania School of Medicine, Philadelphia.

Address reprint requests to Christian G. Kohler, M.D., Mental Health Clinical Research Center, 3400 Spruce Street, Department of Psychiatry, 10 Gates Bldg, Philadelphia PA 19104.

Received June 14, 1999; revised December 7, 1999; accepted February 15, 2000.

© 2000 Society of Biological Psychiatry 0006-3223/00/$20.00

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ported differential impairment in discrimination of happy and sad facial expression relative to age discrimination using a set of neutral, happy, and sad faces. Patients performed worse on emotion than on age recognition, whereas healthy subjects performed comparably on these tasks. Using the same testing paradigm (which included 254 faces, enabling comparison of happy versus neutral and sad versus neutral in a blocked design), Gur et al (1992) found that the deficit associated with schizophrenia was more marked compared with the performance of patients with depression. The large number of facial stimuli used, which permitted blocking sad and happy discrimination, enabled separate determination of false positive and negative rates for each emotion; however, the interspersed stimulus presentation of the other investiga-tions is more naturalistic. Borod et al (1993) administered facial emotion identification and discrimination tasks of six different emotions and neutral, ranging from 21 to 32 facial stimuli to patients with schizophrenia, patients with right-brain damage, and healthy control subjects and found that both patient groups were impaired. When perfor-mances on the Benton Facial Recognition Test and a visuospatial task were used as covariates, this effect disappeared in both groups for the emotion discrimination, but not for the more difficult identification task.

In contrast, other studies indicate a generalized facial processing deficit in schizophrenia. Novic et al (1984) reported that patients performed more poorly than control subjects on a task requiring participants to match pictures with identical emotions, but when they controlled for performance on the Benton Facial Recognition Test, the difference became insignificant. The validity of the results is limited by the small number of presented stimuli (six out of 16) used in the analysis. Likewise, Feinberg et al (1986) found that schizophrenic patients were impaired on emo-tion matching and labeling tasks, but not on facial recog-nition tasks relative to depressed patients. Patients with schizophrenia were also impaired on emotion and facial recognition tasks compared with healthy control subjects. Archer et al (1992) reported that patients with schizophre-nia were as impaired on facial expression recognition of six different emotions as they were on two facial recog-nition tasks, relative to patients with major depression and normal control subjects. For patient and control groups, performances on the tasks ranged between 89 –98%, indi-cating that the experimental tasks may have been too easy to detect differences between the tasks. Schneider et al (1995) described similar results in that patients with schizophrenia were impaired relative to healthy control subjects on identification of happy, sad, and neutral expressions, as well as assessment of age; however, this study did not evaluate whether the deficit was generalized or specific. Kerr and Neale (1993) utilized a differential

deficit design based on the requirements put forth by Chapman and Chapman (1978) as described below. This study compared a group of institutionalized and unmedi-cated with patients with chronic schizophrenia with a control group on tests of perception and discrimination of different emotions (happiness, sadness, fear, anger, shame, and surprise) and Benton’s Facial Recognition Test. Schizophrenic patients performed worse on all tasks with-out a differential deficit, indicating that they display impaired facial processing, rather than a specific emotion recognition deficit. Performance data were not presented. Using an abbreviated test design, Salem et al (1996) replicated these findings in a group of 23 medicated, male, chronic schizophrenia patients compared with a male control group. Although the differences in performance between patient and control groups reached significance, the magnitude of differences between tasks may not have been large enough to detect differential deficits for emo-tion recogniemo-tion.

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Gender differences have been reported in the clinical presentation and course of schizophrenia. Men tend to have an earlier age of onset (Beratis et al 1994; Jayaswal et al 1987; Vazquez-Barquero et al 1995), poorer premor-bid adjustment (Shtasel et al 1992), lower level of daily functioning, and worse negative symptomatology (Gold-stein et al 1989; Salem and Kring 1998; Shtasel et al 1992) than women. No previous study has addressed the issue of gender differences in emotion perception in schizophrenia. In healthy subjects, women performed better than men (reviewed in Kring and Gordon 1998). Erwin et al (1992) reported an interaction of gender of poser with the gender of observer: women were more sensitive to male faces, whereas men showed a lack of sensitivity to sad expres-sions in women.

In our study, patients completed computerized emotion and age recognition tasks, along with ratings of symptom-atology and neuropsychologic testing. The computerized tasks consisted of male and female faces with randomized neutral, sad, and happy affect. This was modified from our previous blocked stimulus design to allow for a more natu-ralistic methodology and better comparability with other studies. The control task used the same type of stimuli and differed only in the requirement to rate age rather than affect. The goals of the present study were to measure the severity of emotion recognition deficits in schizophrenia compared with age recognition performance. We also evaluated whether schizophrenic patients exhibit gender-related differ-ences in emotion recognition similar to healthy subjects. Finally, we examined the association of emotion and age recognition performance with clinical and neurocognitive manifestations of schizophrenia.

We hypothesized the following: 1) Emotion and age recognition would be impaired in schizophrenia compared with healthy control subjects. 2) Male patients would exhibit a greater deficit than female patients. This finding would be consistent with worse symptomatology in men. 3) Impaired emotion, rather than age recognition, would be associated with severity of positive and negative symptoms. 4) Emotion recognition performance correlates with different cognitive functions than age discrimination performance. Support for hypotheses 3 and 4 would indicate that the emotion recognition deficit in schizophre-nia relates uniquely to core features of the disorder.

Methods and Materials

Subjects

The sample consisted of 45 healthy people (25 men, 20 women) and 35 people with schizophrenia (20 men, 15 women). Recruit-ment of participants followed established procedures (Gur et al 1991; Shtasel et al 1991). Patients underwent diagnostic exam-ination using the Structured Clinical Interview for DSM-IV

(SCID-P; First et al 1995a) and met criteria for schizophrenia or schizophreniform disorder. Patients with the initial diagnosis of schizophreniform disorder (n57) were followed longitudinally and met criteria for schizophrenia. Patients with the diagnosis of schizoaffective disorder, any concomitant Axis I disorder, or history of any other disorder affecting brain function were excluded. Testing of age and emotion recognition and symptom and cognitive assessments were performed in patients who were symptomatic but clinically stable at the time of evaluation. At the time of emotion recognition testing, 31 patients were treated with standard neuroleptic medication, whereas four patients were medication naive (diagnosis schizophrenia:schizophreniform53: 1). Patients were treated with typical neuroleptics (n 5 22), atypical neuroleptics (n 5 4) or both (n 5 5) at an average dose of 454 chlorpromazine equivalents per day. Medication exposure ranged from 1 week to 14.8 years. Healthy control subjects underwent comprehensive assessment including Struc-tured Clinical Interview for DSM-IV nonpatient version (SCID-NP; First et al 1995b), physical examination, and laboratory tests to exclude concurrent psychiatric or other medical illness. Those with a family history of schizophrenia or affective illness were excluded. Sociodemographic data are presented in Table 1. Male and female control subjects did not differ in age, education, ethnicity, and handedness. Likewise, male and female patients did not differ in these variables. Clinically, they differed in age of onset of disease with men (20.6 years64.7) having an earlier onset than women (25.3 years 6 7.9). They did not differ in number of hospitalizations. Patient and control groups differed in ethnicity, handedness, and education. As expected, patients attained fewer years of education than control subjects but did not differ in parental education.

Procedures

EMOTION RECOGNITION TASK. A computerized task,

consisting of emotion and age identification subtests, was con-structed using Authorware Professional 2.0 (Macromedia, San Francisco). The test is a computerized version of the emotion discrimination task developed in our laboratory (Erwin et al 1992). In the emotion discrimination condition, participants were presented with 40 faces displaying happy (five male, five female), sad (five male, six female), or neutral (nine male, 10 female) expressions (Figure 1). The age perception task included 40 faces of the same people with similar distribution of happy (eight male, six female), sad (five male, five female), or neutral (eight male, eight female) expressions. The order of stimuli was randomized but fixed across subjects.

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were administered by a trained neuropsychologic tester, and participants were provided with a demonstration of tasks and time to practice.

SYMPTOM RATINGS. Symptom severity ratings were

per-formed by trained investigators (ICC. .85) and included the Scale for the Assessment of Negative Symptoms (SANS; An-dreasen 1984a), the Scale for the Assessment of Positive Symp-toms (SAPS; Andreasen 1984b), and the 21-item Hamilton Depression Rating Scale (HDRS; Hamilton 1960). Ratings were obtained within 3 months of testing in 27 of the 35 patients and within 8 months for the remaining patients. Patients remained clinically stable during this period.

NEUROPSYCHOLOGIC BATTERY. A standardized,

previ-ously detailed (Saykin et al 1991, 1994) neuropsychologic battery was administered to participants. Briefly, the battery consisted of tests evaluating eight functional domains:

1) Abstraction–flexibility: Wisconsin Card Sorting Test (Heaton 1981)

2) Attention-vigilance: Continuous Performance Test (Gor-don 1986), Seashore Rhythm Test (Halstead-Reitan Neu-ropsychological Test Battery HRB] Reitan and Wolfson 1985), letter and symbol cancellation (Mesulam 1985) 3) Verbal memory: story recall (Wechsler Memory Scale,

Wechsler 1945; Wechsler Memory Scale-Revised, Wech-sler 1987), California Verbal Learning Test (Delis et al 1983)

4) Spatial memory: design reproduction (Wechsler Memory Scale, Wechsler 1945; Wechsler Memory Scale-Revised, Wechsler 1987), Benton Facial Recognition (Benton and Van Allen 1968), Continuous Visual Memory Test Trahan and Larrabee 1988)

5) Verbal intelligence and language function: vocabulary (Wechsler Adult Intelligence Scale-Revised [WAIS-R], Wechsler 1981), controlled oral word association (Multi-lingual Aphasia Examination [MAE], Benton and Ham-sher 1976), animal naming (Boston Diagnostic Aphasia Exam [BDAE], Goodglas and Kaplan 1983), MAE Visual Naming (Benton and Hamsher 1976), Reading Sentences and Paragraphs subtest from the BDAE (Goodglass and Kaplan 1983)

6) Spatial abilities: Benton Judgment of Line Orientation (Benton et al 1978), block design (WAIS-R, Wechsler 1981)

7) Sensory: stereognosis (Luria-Nebraska Neuropsychologi-cal Battery, Golden et al 1980)

8) Fine manual motor functions: finger tapping (HRB, Reitan and Wolfson 1985).

The battery was administered by trained neuropsychologic technicians, who are supervised by neuropsychologists, and is scored according to the established procedures for each test. For 18 of the 35 patients and 23 of the 45 control subjects, the battery was administered within 3 months of the facial recognition tasks. For the remaining subjects, the battery was administered within a year.

Table 1. Sociodemographic Characteristics

Healthy group Schizophrenic group Significance

Gender (men/women) 25/20 20/15 ns

Age 27.568.5 30.669.5 ns

Handedness Right: 42 Right: 26 x254.59

Left: 3 Left: 8 p5.03

Ethnicity White: 32 White: 16 x254.65

African American: 12 African American: 19 p5.02 Asian: 1

Subject education 14.962.0 13.462.4 t53.1

p5.003 Parental education (paternal1

maternal:2)

11.761.8 12.562.5 n.s.

Age at onset

men — 20.664.7 t52.1

women — 25.367.9 p5.05

Duration (years) — 5.667.8 —

No. of hospitalizations — 1.456.51 —

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Data Analysis

EMOTION AND AGE RECOGNITION. The dependent

mea-sure for performance was error rate defined as percentage of responses that are more than one point away from the correct response on the seven-point scale. In the emotion discrimination task, the correct response was defined by the mean of the normative sample used to validate the stimuli (Erwin et al 1992). For the age discrimination task, birth dates were available for each poser. These percentages were determined separately for male and female faces. To satisfy normality assumptions for the repeated measures multivariate analysis of variance (MANOVA), these percentages were transformed using the arcsin transformation. The model used was a repeated measures MANOVA, with error rates (for emotion and age discrimination tasks) as outcome measures, diagnosis (patients, control sub-jects), and gender of the observer as between-group factors, and gender of facial stimuli as the within-group factor. Handedness, ethnicity, and education were considered as covariates in our model. Additionally, a model was fit to the patient group to assess the impact of duration.

SYMPTOM RATINGS. Spearman correlation coefficients were computed for emotion and age recognition errors (arcsine transformed for normality), and the SANS, SAPS, and HDRS ratings. For SANS, we used the global ratings for affective flattening, alogia, avolition, and anhedonia; for SAPS, we used the global ratings for hallucinations, delusions, bizarre behavior, and thought disorder; for HDRS we used the total score.

NEUROPSYCHOLOGICAL PERFORMANCE. Spearman

correlation coefficients were computed for emotion and age recognition errors (arcsine transformed for normality) and for cognitive domains of abstraction-flexibility, attention, verbal and spatial memory, language and spatial abilities, and motor and sensory abilities. For the neuropsychologic battery, raw test scores were transformed to standard equivalents (zscores) using the means and SEM of the normal control group, as previously described (Saykin et al 1991, 1994).

Results

Emotion and Age Recognition

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both diagnosis [F(1,76) 5 10.95, p 5 .001] and gender [F(1,76)5 4.78,p5.03], with women having fewer errors.

A MANOVA breaking the scores by poser’s gender showed a task3 poser gender interaction, [F(1,76) 5 4.39, p , .05], reflecting increased error rate for judging emotional displays of female posers in contrast to equal error rate on age discrimination. To test this hypoth-esis more directly, we calculated an opposite-gender emotion detection index, defined as same-gender errors minus opposite-gender errors. As predicted, this score was negative for men [20.04 6 0.06, t(23) 5 2.95, p , .01] and positive for women [0.05 6 0.07, t(18) 5 2.59, p , .01] in the healthy group (between group difference was significant, t 5 3.92, p , .001). The effect was absent in men with schizophrenia [20.02 6 0.03, t(18) 5 0.46, p 5 .65] and not significant in women with schizophrenia [0.04 6 0.03, t(13) 5 1.41, p 5 .18] probably attributable to low power (because the effect size is similar to that of the healthy women).

The inclusion of handedness, education, and ethnicity as covariates did not alter our findings. Additionally, in a separate model including only patients, when duration was added as a covariate, none of these findings were altered. A MANOVA contrasting emotion discrimination per-formance for happy with sad faces showed a main effect of emotional valence, with more errors for sad than happy

faces [F 5 44.07, df 5 1,76, p , .001]. When

performance was examined separately for happy and sad expressions, we found different effects for the two tasks depending on diagnosis and gender. Patients performed more poorly than control subjects on recognition of happy faces [F 5 8.16; df 5 1,76; p 5 .005], whereas the effect is weaker for sad faces [F 5 4.54, df 5 1,76;

p5 .036]. Men performed more poorly on identification of sad faces regardless of diagnosis [F 5 5.84; df 5 1,76; p 5 .018]. Whereas fewer errors were made across groups in identifying happy faces than identifying sad faces, men across groups identified sad female expres-sions most poorly [F 5 12.15;df 5 1,76;p , .001].

Emotion and Age Recognition and Symptomatology

Overall, age recognition performance did not correlate with severity of symptoms. In contrast, errors on the emotion recognition task were associated with greater severity of alogia [r(33) 5 .46, p , .01] from the SANS, and hallucinations [r(33) 5 .29, p , .05] and thought disorder [r(33) 5.48,p,.01] from the SAPS in the whole group of patients and the patients who completed testing of age and emotion recognition and symptom ratings within 3 months. Severity of depressive

symptoms was not associated with emotion or age recog-nition performance. Results for subjects who completed emotion and symptom ratings within 3 months and more than 3 months apart were similar for negative, but not positive symptoms. In the group that completed testing and ratings within 3 to 8 months, similar correlations were found for alogia, but not for hallucinations and thought disorder, indicating relative stability of negative and not positive symptoms over time.

Emotion and Age Recognition and Cognition

Results for subjects who completed emotions and neuro-psychologic testing within 3 months and more than 3 months apart were similar and are reported for whole patient and control groups. In healthy control subjects, neither emotion nor age recognition performances showed significant correlations with any neuropsychologic domain (Figure 3). In patients, age recognition performance was not correlated with neurocognitive performance, but better emotion recognition performance was correlated specifi-cally with better abstraction-flexibility [r 5 .36, df 5 33, p, .05], attention [r5 .60,df5 33,p, .001], verbal [r 5 .59, df 5 33, p , .001], and spatial memory [r 5 .65, df 5 33, p , .001], and language abilities [r 5 .55, df 5 33, p , .001].

Discussion

Patients performed more poorly than control subjects on both facial processing tasks, without an indication of differential impairment. Chapman and Chapman (1978) proposed that to probe for the presence of a differential deficit, performance of an experimental task needs to be compared with performance on a psychometrically matched control task. Over the past 15 years, studies that have used a differential deficit design have yielded find-ings both supporting (Borod et al 1993; Heimberg et al 1992; Walker et al 1984) and failing to support (Archer et al 1992; Feinberg et al 1986; Kerr and Neale 1993; Novic et al 1984; Salem et al 1996) the presence of such a differential or specific emotion recognition impairment. We reported differential deficit in an earlier study (Heim-berg et al 1992), which used a larger set of the same facial stimuli but presented them in a blocked rather than interspersed or randomized design as was done here. Whether blocked presentation makes the task more sensi-tive to differential impairment in schizophrenia merits further study.

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recogni-tion of happy and sad faces, these effects too were moderated by the observers’ gender and diagnosis. All groups had fewer errors for happy than for sad discrimi-nation, replicating our earlier reports (Erwin et al 1992; Heimberg et al 1992). Also replicating an earlier finding (Erwin et al 1992), women were more accurate in discrim-inating emotions on male than on female faces, whereas men did not show the corollary effect. This result could be interpreted to suggest that women are less facially expres-sive, but recent evidence indicates that women are more facially expressive in their emotions (Kring and Gordon 1998); however, this finding is consistent with the “hunter-gatherer” hypothesis (Cherney and Ryalls 1999; Hill 1984; Lee 1974). This hypothesis stipulates that from an evolu-tionary standpoint, it was much more important for indi-viduals of both genders to interpret emotional displays of the physically powerful and socially dominant male than to detect emotional expression in females. It is noteworthy that both male and female patients made more errors than control subjects in recognizing happy expressions. For sad expressions, men but not women with schizophrenia showed impairment relative to control subjects.

Beyond the question of differential deficits, the aim of this study was to examine whether emotion processing deficits are uniquely associated with neurocognitive per-formance and symptom severity. The results supported this notion. Although neither symptom severity nor neu-ropsychologic performance was associated with age rec-ognition errors, both were associated with errors in

emo-tion discriminaemo-tion. The correlaemo-tions with symptoms were significant for the negative symptoms of alogia and for the positive symptoms of hallucinations and thought disorder. Positive symptoms (Barta et al 1990; Shenton et al 1992) have been linked to neural circuitry of the temporal lobes, whereas negative symptoms have been associated with frontal (Buchanan et al 1994) and to a lesser extent temporal (Turetsky et al 1995) structures. It was surprising to find that the emotion processing deficit was associated with alogia, rather than other negative symptoms such as affective flattening, avolition, or anhedonia. This suggests that emotion recognition has at least partially independent effects on symptomatology that do not necessarily relate to disturbed affect and psychosocial functioning. Further-more, the association of emotion recognition, but not age recognition, with core symptoms of schizophrenia offers indirect evidence that emotion recognition may help ex-amine temporolimbic features of schizophrenia. Longitu-dinal designs are needed to establish whether change in performance on emotion discrimination tasks is predictive of symptomatic improvement.

The were no correlations between performance on either age discrimination or emotion discrimination and neuropsychologic domains for the healthy participants. This is unusual because most cognitive tasks share com-mon variance related to sensory input, attention to the task, facial processing, and linguistic ability (the “g factor”). Nonetheless, there is increased evidence that face process-ing has distinct neural substrates (see review in Mesulam

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1998). In patients, although there were no correlations between age discrimination and neuropsychologic perfor-mance, significant and large correlations were observed between performance on emotion discrimination and sev-eral neurocognitive domains. These were specific to ab-straction and mental flexibility, attention, memory (verbal and spatial), and language, all related to frontal and temporal functioning. Several studies have indicated dif-ferential deficits in verbal memory in patients with schizo-phrenia, superimposed on generally lower cognitive per-formance (Saykin et al 1991, 1994). Thus, the correlations suggest that the impairment in frontotemporal functions extends to limbic regions related to emotional processing. Our study is limited in sample size and the cross-sectional design; it does not offer correlations between emotion processing and regional brain function. Based on our findings, however, we propose that emotion recognition, as a primarily temporal lobe function, is impaired in schizophrenia and contributes to the deficit load of pa-tients suffering from this disorder. Even though the deficit is not more severe for emotion recognition than for age recognition, the emotion processing deficit is uniquely associated with symptom severity and neurocognitive deficits and therefore merits further scrutiny.

Our study has several limitations related to the task and patient sample. Compared with our previous study of emotion and age recognition in schizophrenia, the present study uses only 40 stimuli, which may yield insufficient statistical power to probe for differential impairment regarding positive and negative emotions. The age recog-nition task, although carefully constructed to serve as a control task that differs only in the component of recog-nition, may represent another limitation. Facial display of emotions may influence the assessment of age. Further-more, the requirement to assess emotional faces for age rather than affect could be distracting to the subjects. The number of moderately emotional faces in the age recog-nition task was insufficient to probe for this effect. These test-related limitations may have contributed to the failure to establish a differential deficit for emotion recognition. On the other hand, the association of emotion recognition, but not age recognition, with severity of symptoms and to a lesser extent with cognitive impairment, can be consid-ered as indirectly supporting the presence of specific associations for the emotion processing deficit. Limita-tions regarding the patient group included patients being at different stages of the illness, the use of different neuro-leptics, and relating experimental measures that were not performed at the same time. Patients were tested at different times of illness, including seven patients with schizophreniform disorder who were later diagnosed with schizophrenia. Testing of age and emotion recognition and symptom and cognitive assessments were performed in

patients who were symptomatic but clinically stable at the time of evaluation. Unfortunately, the sample of patients with first onset of schizophrenia was too small to allow for comparison with more chronically ill patients. The use of different medications, including atypical, typical, and combined typical and atypical neuroleptics, as well as the presence of neuroleptic-naive patients, precluded compar-ison of medication effects. It is noteworthy that comparing the patients who underwent symptom rating within 3 months of testing to those with larger intervals were remarkably similar. Nonetheless, it would have been preferable if all assessments had been be performed within shorter intervals.

Comparison of patients with schizophrenia with those who have depression or mania with psychotic features may help elucidate the disease specificity of deficits in emotion recognition. Comparison of schizophrenia with patients suffering from temporal lobe epilepsy would yield information regarding emotional processing associated with impairment in temporolimbic processing. To study the effects of medication and stage of illness, we need to assess emotion recognition longitudinally in the setting of standardized neuroleptic medication treatment. Evaluation of emotion recognition using functional imaging will help delineate the extent of neuronal impairment related to emotional processing that may contribute the pathophysi-ology of schizophrenia.

This research was supported by the National Institute of Health Grants Nos. MH-43880, MH-42191, MH-01336, and MO1RR0040.

References

Adolphs R, Damasio H, Tranel D, Damasio AR (1996): Cortical systems for the recognition of emotion in facial expressions.

J Neurosci16:7678 – 687.

Adolphs R, Schul R, Tranel D (1998): Intact recognition of facial emotion in Parkinson’s disease. Neuropsychology 12:253– 258.

Adolphs R, Tranel D, Damasio H, Damasio A (1994): Impaired recognition of emotion in facial expressions following bilat-eral damage to the human amygdala.Nature372:669 – 672. Andreasen NC (1984a):The Scale for the Assessment of Negative

Symptoms (SANS).Iowa City: The University of Iowa. Andreasen NC (1984b):The Scale for the Assessment of Positive

Symptoms (SAPS).Iowa City: The University of Iowa. Anthony BJ (1978): Piagetian egocentrism, empathy, and affect

discrimination in children at high risk for psychosis. In: Anthony EJ, Koupernik C, Chiland C, editors.The Child and His Family: Vulnerable Children,Vol 4. New York: Wiley, 359 –379.

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Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE (1990): Auditory hallucinations and smaller superior tempo-ral gytempo-ral volume in schizophrenia. Am J Psychiatry 147: 1457–1462.

Benton AL, Hamsher K (1976):Multilingual Aphasia Examina-tion.Iowa City, Iowa: AJA Associates.

Benton AL, Hamsher KD, Varney NR, Spreen O (1983):

Contributions to Neuropsychological Assessment. New York: Oxford University Press.

Benton AL, Van Allen MW (1968): Impairment in facial recogni-tion in patients with cerebral disease.Cortex4:344 –358. Benton AL, Varney NR, Hamsher K (1978): Visuospatial

judge-ment: A clinical test.Arch Neurol35:364 –367.

Beratis S, Gabriel J, Hoidas S (1994): Age at onset in subtypes of schizophrenic disorders.Schizophr Bull20:287–296. Bleuler E (1911):Dementia Praeox oder die Gruppe der

Schizo-phrenien,Aschaffenburgs Handbuch. Leipzig: Deutike. Blonder LX, Bowers D, Heilman KM (1991): The role of the

right hemisphere in emotional communication. Brain 114: 1115–1127.

Borod JC, Martin CC, Alpert M, Brozgold A, Welkowitz J (1993): Perception of facial emotion in schizophrenic and right-brain damaged patients.J Nerv Ment Dis181:494 –502. Bowers D, Blonder LX, Feinberg T, Heilman KM (1991): Differential impact of right and left hemisphere lesions on facial emotion and object imagery.Brain114:2593–2609. Buchanan RW, Strauss ME, Kirkpatrick B, Holstein C, Breier A,

Carpenter WT (1994): Neuropsychological impairments in deficit vs nondeficit forms of schizophrenia. Arch Gen Psychiatry51:804 – 811.

Chapman LJ, Chapman JP (1978): The measurement of differ-ential deficit.J Psychiatr Res14:303–311.

Charlesworth WR (1982): An ethological approach to research on facial expressions. In: Izard CE, editor.Measuring Emo-tions in Infants and Children.New York: Cambridge Univer-sity Press, 317–334.

Cherney ID, Ryalls BO (1999): Gender-linked differences in the incidental memory of children and adults. J Exp Child Psychol72:305–328.

Cutting J (1981): Judgment of emotional expression in schizo-phrenics.Br J Psychiatry139:1– 6.

Damasio AR (1998): Emotion in the perspective of an integrated nervous system.Brain Res Brain Res Rev26:83– 86. Delis C, Kramer JH, Kaplan E, Ober BA (1983): California

Verbal Learning Test, Research Edition.Cleveland: Psycho-logical Corp.

Ekman P, Friesen WV, Ellsworth P (1972): Emotion in the Human Face: Guidelines for Research and an Integration of Findings.New York: Pergamon.

Erwin RJ, Gur RC, Gur RE, Skolnick BE, Mawhinney-Hee M, Smailis J (1992): Facial emotion discrimination: I. Task construction and behavioral findings in normals. Psychiatry Res42:231–240.

Feinberg TE, Rifkin A, Schaffer C, Walker E (1986): Facial discrimination and emotional recognition in schizophrenia and affective disorders.Arch Gen Psychiatry43:276 –279. First MG, Spitzer RL, Gibbon M, Williams JB (1995a):

Struc-tured Clinical Interview for DSM-IV Patient Edition

(SCID-P).New York: New York State Psychiatric Institute, Biometrics Research Department.

First MB, Spitzer RL, Gibbon M, Williams JBW (1995b):

Structured Clinical Interview for DSM-IV Axis I Disorders, Non-Patient Edition (SCID-NP).New York: New York State Psychiatric Institute, Biometrics Research Department. Golden CJ, Hammeke TA, Puritsch AD (1980):Luria-Nebraska

Neuropsychological Battery, Manual.Los Angeles: Western Psychological Services.

Goldstein JM, Tsuang MT, Faraone SV (1989): Gender and schizophrenia: Implications for understanding the heteroge-neity of the illness.Psychiatry Res28:243–253.

Goodglass H, Kaplan E (1983):The Assessment of Aphasia and Related Disorders,2nd ed. Philadelphia: Lea and Febiger. Gordon M (1986): Manual, Gordon Diagnostic System. New

York: Gordon Diagnostic Systems.

Gur RC, Erwin RJ, Gur RE, Zwil AS, Heimberg C, Kraemer HC (1992): Facial emotion discrimination: II. Behavioral findings in depression.Psychiatry Res42:241–251.

Gur RE, Mozley PD, Resnick SM, Levick S, Erwin R, Saykin AJ, Gur RC (1991): Relations among clinical scales in schizophre-nia: Overlap and subtypes.Am J Psychiatry148:472– 478. Hamilton M (1960): A rating scale for depression. J Neurol

Neurosurg Psychiatry23:56 – 62.

Heaton RK (1981): Wisconsin Card Sorting Test, Manual.

Odessa, FL: Psychological Assessment Resources.

Heilman KM, Gilmore RL (1998): Cortical influences in emo-tion.J Clin Neurophysiol15:409 – 423.

Heimberg C, Gur RE, Erwin RJ, Shtasel DL, Gur RC (1992): Facial emotion discrimination: III. Behavioral findings in schizophrenia.Psychiatry Res42:253–265.

Hill J (1984): Prestige and reproductive success in man.Ethol Sociobiol5:77–95.

Izard CE (1971): The Face of Emotion.New York: Appleton-Century.

Jacobs DH, Shuren J, Heilman KH (1995): Impaired perception of facial identity and facial affect in Huntington’s disease.

Neurology45:1217–1218.

Jayaswal SK, Paraveenlal K, Khandelwal SK, Mohan D (1987): Sex difference in the age at symptom onset in schizophrenia.

Indian J Psychol Med10:68 –74.

Kerr SL, Neale JM (1993): Emotion perception in schizophrenia: Specific deficit or further evidence of generalized poor performance?J Abnorm Psychol102:312–318.

Kring AM, Gordon AH (1998): Sex differences in emotion: Expression, experience, and physiology.J Pers Soc Psychol

74:686 –703.

Kring AM, Neale JM (1996): Do schizophrenia patients show a disjunctive relationship among expressive, experiential, and psychophysiological components of emotion?J Abnorm Psy-chol105:249 –257.

Lang PJ, Bradley MM, Cuthbert BN (1998): Emotion, motiva-tion, and anxiety: brain mechanisms and psychophysiology.

Biol Psychiatry44:1248 –1263.

Lee RB (1974): Male-female residence arrangements and polit-ical power in human hunter-gatherers. Arch Sex Behav

3:167–173.

Leventhal H, Tomarken AJ (1986): Emotions; today’s problems.

(10)

Lezak MD (1995): Perception, 3rd ed. Oxford, UK: Oxford University Press.

Mesulam M (1985):Principles of Behavioral Neurology. Phila-delphia: F.A. Davis.

Mesulam MM (1998): From sensation to cognition. Brain

121:1013–1052.

Mikhailova ES, Vladimirova TV, Iznack AF, Tsusulkovskaya EJ, Sushko NV (1996): Abnormal recognition of facial expression of emotions in depressed patients with major depression disorder and schizotypal personality disorder.Biol Psychiatry40:697–705.

Novic J, Luchins DJ, Perline R (1984): Facial affect recognition in schizophrenia. Is there a differential deficit?Br J Psychi-atry144:533–537.

Reitan RM, Wolfson D (1985):The Halstead Reitan Neuropsy-chological Test Battery: Theory and Clinical Interpretation.

Tucson: Neuropsychology Press.

Sackeim HA, Greenberg M, Weiman A, Gur RC, Hungerbuhler J, Geschwind N (1982): Hemispheric asymmetry in the expression of positive and negative emotions. Neurologic evidence.Arch Neurol39:210 –218.

Salem JE, Kring AM (1998): The role of gender differences in the reduction of etiologic heterogeneity in schizophrenia.Clin Psychol Rev18:795– 819.

Salem JE, Kring AM, Kerr SL (1996): More evidence for generalized poor performance in facial emotion perception in schizophrenia.J Abnorm Psychol105:480 – 483.

Saykin AJ, Gur RC, Gur RE, Mozley D, Mozley LH, Resnick SM, et al (1991): Neuropsychological function in schizophre-nia: selective impairment in memory and learning.Arch Gen Psychiatry48:618 – 624.

Saykin AJ, Shtasel DL, Gur RE, Kester DB, Mozley LH, Stafiniak P, Gur RC (1994): Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia.

Arch Gen Psychiatry51:124 –131.

Schneider F, Gur RC, Gur RE, Shtasel DL (1995): Emotional processing in schizophrenia: Neurobehavioral probes in rela-tion to psychopathology.Schizophr Res17:67–75.

Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, et al (1992): Abnormalities of the left temporal lobe and thought disorder in schizophrenia: a quantitative magnetic resonance imaging study.N Engl J Med327:604 – 612. Shtasel DL, Gur RE, Gallacher F, Heimberg C (1992): Gender

differences in the clinical expression of schizophrenia.

Schizophr Res7:225–231.

Shtasel DL, Gur RE, Mozley PD, Richards J, Taleff MM, Heimberg C, et al (1991): Volunteers for biomedical research: Recruitment and screening of normal controls. Arch Gen Psychiatry48:1022–1025.

Trahan DE, Larrabee GJ (1988): Continuous Visual Memory Test: Professional Manual. Odessa, FL: Psychological As-sessment Resources.

Turetsky BT, Cowell PE, Gur RC, Grossman RI, Shtasel DL, Gur RE (1995): Frontal and temporal lobe brain volumes in schizophrenia: Relationship to symptomatology and clinical subtype.Arch Gen Psychiatry52:1061–1070.

Vazquez-Barquero JL, Cuesta Nunez MJ, De La Varga M, Herrera Castanedo S (1995): The Cantabria first episode schizophrenia study: A summary of general findings. Acta Psychiatr Scand9:156 –162.

Walker E, McGuire M, Bettes B (1984): Recognition and identification of facial stimuli by schizophrenics and patients with affective disorders.Br J Clin Psychol23:37– 44. Wechsler D (1945): A standardized memory scale for clinical

use.J Psychol19:87–95.

Wechsler D (1981):Wechsler Adult Intelligence Scale-Revised, Manual.Cleveland: Psychological Corp.

Wechsler D (1987):Wechsler Memory Scale-Revised, Manual.

Gambar

Table 1. Sociodemographic Characteristics
Figure 2. Means of error rates for the age discrimination and emotion discrimination tasks for male and female posers (facial stimuli)in men (CNT_M) and women (CNT_F) who are healthy and in men (SCH_M) and women (SCH_F) who are ill with schizophrenia.
Figure 3. Spearman correlation coefficients between age (shaded columns) and emotion (solid columns) recognition errors inschizophrenia subjects

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