Original articleEmotion recognition deficit in schizophrenia: association with symptomatology and cognition
Introduction
Processing 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, Adolphs et al 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 neuropsychiatric 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, experience and expression, has benefitted from the use of standardized 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 discrimination task, which compared “friendliness” and “meanness,” but not on color discrimination and age perception tasks. Walker et al (1984) studied patients with chronic schizophrenia, affective disorder, and healthy control subjects. Three emotional tasks of 16 faces each were used to probe emotion discrimination, emotion labeling, and multiple 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 reported 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 investigations 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 performances 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 emotion matching and labeling tasks, but not on facial recognition 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 schizophrenia were as impaired on facial expression recognition of six different emotions as they were on two facial recognition tasks, relative to patients with major depression and normal control subjects. For patient and control groups, performances on the tasks ranged between 89–98%, indicating 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 unmedicated 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 without 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 emotion recognition.
The lack of consensus on whether a generalized face processing deficit can account for the affect recognition deficit may have several reasons. Except for the last two studies mentioned, all investigators utilized different emotion recognition paradigms. The use of different facial control tasks may further have contributed to the disparity of findings; however, many studies utilized the Test of Facial Recognition as the control task. This test, in an original 54-face (Benton and Van Allen 1968) and shortened 27-face (Benton et al 1983) version, measures the ability to recognize faces without a memory component. Performance relies on visuospatial and linguistic processing and is impaired in patients with right parietal lesions, aphasia, and dementias (Lezak 1995). Most emotion recognition studies attempted to conform to the Chapman and Chapman (1978) differential deficit design. To establish differential deficit, the target and control tasks should be equated for difficulty and true score variance in healthy people; however, the methodologically important question of generalized face processing versus specific affect recognition deficit should be considered within the context of efforts to elucidate the pathophysiology of schizophrenia and treatment of its behavioral manifestations. Impaired emotion recognition has considerable impact on a person’s abilities to communicate and comprehend nonverbal cues. As such, impaired emotion recognition in the person with schizophrenia may exert adverse effects on psychosocial functioning independent of the presence and severity of positive and negative symptoms and cognitive difficulties. Although this issue was not explored in our present study, we believe emotion recognition is relevant for interpersonal and social adjustment and has impact regardless of its severity relative to cognitive deficits that serve as a control task.
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 premorbid adjustment (Shtasel et al 1992), lower level of daily functioning, and worse negative symptomatology Goldstein 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 expressions in women.
In our study, patients completed computerized emotion and age recognition tasks, along with ratings of symptomatology 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 naturalistic 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 differences 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 schizophrenia relates uniquely to core features of the disorder.
Section snippets
Subjects
The sample consisted of 45 healthy people (25 men, 20 women) and 35 people with schizophrenia (20 men, 15 women). Recruitment of participants followed established procedures Gur et al 1991, Shtasel et al 1991. Patients underwent diagnostic examination 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 (n = 7) were followed longitudinally
Emotion and age recognition
The mean error rates for male and female faces in patients and controls (Figure 2) indicate impaired performance in schizophrenia that is moderated by gender of poser and gender of subject. The MANOVA comparing error rates in the age and emotion discrimination tasks showed that patients performed worse than comparison participants across tasks [F(1,76) = 24.00, p < .001]; however, there was no task × diagnosis interaction [F(1,76) = 1.30, p = .25]. Thus, the hypothesis of differential deficit
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 findings both supporting Borod et al 1993, Heimberg et al 1992
Acknowledgements
This research was supported by the National Institute of Health Grants Nos. MH-43880, MH-42191, MH-01336, and MO1RR0040.
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