Social perception and early visual processing in schizophrenia

Social perception and early visual processing in schizophrenia

Schizophrenia Research 59 (2002) 233 – 241 www.elsevier.com/locate/schres Social perception and early visual processing in schizophrenia Mark J. Serg...

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Schizophrenia Research 59 (2002) 233 – 241 www.elsevier.com/locate/schres

Social perception and early visual processing in schizophrenia Mark J. Sergi a,b,*, Michael F. Green b,c b

a Department of Psychology, California State University, Northridge, CA, USA Department of Veterans Affairs VISN-22 Mental Illness Research Education Clinical Center, Los Angeles, CA, USA c Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA

Received 14 May 2001; received in revised form 14 November 2001; accepted 19 November 2001

Abstract Persons with schizophrenia experience deficits in social cognition — the cognitive processes involved in how people perceive and interpret information about themselves, others, and social situations. These deficits may be related to the neurocognitive impairments often experienced by persons with schizophrenia. Our primary objective was to examine associations between social perception and early visual processing in schizophrenia. Our secondary objective was to examine whether outpatients with schizophrenia and healthy persons differ in social perception. Forty outpatients with schizophrenia and 30 healthy persons completed a measure of social perception (the Half-Profile of Nonverbal Sensitivity), visual masking procedures, and ratings of positive and negative symptoms. Within patients, performance on visual masking procedures was related to performance on the Half-Profile of Nonverbal Sensitivity. Patients with schizophrenia and the healthy persons differed significantly in their performance on the Half-Profile of Nonverbal Sensitivity, but this difference became nonsignificant when education was a covariate. These findings suggest that social perception in schizophrenia is related to very early aspects of visual processing. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Schizophrenia; Social cognition; Neurocognition; Social perception; Masking; Early visual processing

Deficits in social cognition—the cognitive processes involved in how people perceive, interpret, and process information about themselves, others, and social situations—are common in persons with schizophrenia (Penn et al., 1997) and may contribute to impairments in social functioning (Corrigan and Toomey, 1995; Penn et al., 1996). One aspect of social cognition that has direct relevance for social functioning involves one’s perception of social cues (including * Corresponding author. Department of Psychology, California State University, 18111 Nordhoff Street, Northridge, CA 913308255, USA. Tel.: +1-818-677-7352; fax: +1-818-677-2829. E-mail address: [email protected] (M.J. Sergi).

facial expressions, gestures, situational context, and voice tone). This aspect has been studied in schizophrenia in two distinct ways. Measures of emotion perception require participants to label or select the emotion conveyed by the social cue. Measures of social perception include similar social cues, but they differ from measures of emotion perception in the responses expected. In social perception tasks, individuals label or select the situational context that gave rise to the social cues (e.g., talking to a lost child, talking about the death of a friend). A second distinction between measures of emotion perception and measures of social perception concerns the breadth of the interpersonal areas addressed. While measures of

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emotion perception focus only on mood state, measures of social perception may address varied interpersonal areas such as intimacy, veracity, mood state, and status. Since the study of emotion perception in persons with schizophrenia began over 40 years ago, many studies have demonstrated that persons with schizophrenia are impaired in their ability to recognize emotions from static facial expressions (e.g., Cutting, 1981; Izard, 1959; Pollard et al., 1995), dynamic facial expressions (e.g., Archer et al., 1994; Hellewell et al., 1994), and voice intonation (e.g., Murphy and Cutting, 1990; Turner, 1964). Conversely, relatively few studies have examined social perception in schizophrenia. Four studies using videotape-based assessments of social perception have examined differences between inpatients with schizophrenia and healthy persons. Two of these studies found that inpatients were impaired on the Profile of Nonverbal Sensitivity (PONS; Rosenthal et al., 1979), which requires participants to assign situational labels to brief videotape scenes of facial expressions, gestures, and/or voice intonation (Monti and Fingeret, 1987; Toomey et al., in press). Two other studies found that inpatients were impaired on the Social Cue Recognition Test (SCRT; Corrigan and Green, 1993a,b), which requires participants to identify the cues present in videotaped scenes of social situations (Corrigan et al., 1990; Corrigan and Green, 1993a,b). Although the origins of social cognitive deficits in schizophrenia are not well understood, problems in this area may be related to impairments in neurocognition. Emotion perception in schizophrenia has been found to be related to early visual processing as measured by the Span of Apprehension Test (SPAN; Addington and Addington, 1998; Kee et al., 1998), visual attention as measured by the Continuous Performance Test (Addington and Addington, 1998; Bryson et al., 1997), and executive functioning as measured by the Wisconsin Card Sorting Test (Bryson et al., 1997). In a previous study from our laboratory (Kee et al., 1998), we found that associations between early visual processing as measured by the SPAN and emotion perception were significantly stronger than those involving other neurocognitive measures. This pattern of correlations suggests that early perception (in this case, visual perception) has an especially close link to emotion perception. It appears that this tight

association with early perceptual processing applies to social perception as well: Corrigan et al. (1994) found that 65% of the variance in social perception, assessed by the SCRT, was explained by two neurocognitive variables: early visual processing as measured by the SPAN and verbal recognition memory as measured by the Rey Auditory Verbal Learning Test. While the SPAN strongly suggests the importance of early perceptual processes, other perceptual techniques, such as visual masking procedures, offer interpretive advantages. The SPAN involves scanning of a visual array and read-out from the icon. In visual masking, a target is presented for a very brief interval and the presence of a mask disrupts the processing of the target. Hence, the test assesses the sensory components involved in the formation of a percept, not scanning or read-out. Measures of visual masking assess the earliest aspects of visual processing and have consistently shown performance deficits in schizophrenia (e.g., Green and Walker, 1986; Saccuzzo and Braff, 1981, 1986). Because there are reasonably well-established neural models of visual masking, these procedures allow one to make inferences about neural mechanisms. The different masking conditions used in this paper (location, high-energy, and low-energy) involve different masking mechanisms (see Green et al., 1994a for discussion). Visual masking is likely based on the interactions of sustained and transient channels (Breitmeyer, 1984). Although used much less often in psychopathology research, forward masking is of interest because it is thought to rely mainly on sustained channels, whereas backward masking depends on both transient and sustained channels. We have previously suggested that visual masking deficits are mainly due to overactive transient channels (Green et al., 1994b). If there is a relationship between early visual processing and social perception, we would expect it to be more prominent in backward masking. Our main objective for this paper was to test the hypothesis that social perception will be related to visual perception in schizophrenia. While previous studies suggest a strong relationship between early visual processing and social cognition, more specialized visual masking procedures provide a strong test of this possibility. Our secondary objective was to test whether stabilized outpatients with schizophrenia would display social perception deficits relative to

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healthy persons because there have been very few studies in this area.

1. Method 1.1. Participants Forty outpatients with schizophrenia (39 males and 1 female) and 30 healthy control participants (20 males and 10 females) were recruited from a larger study of early visual processing (Early Visual Processing in Schizophrenia; M.F. Green, P.I.). Participating outpatients were recruited from the treatment clinics of the VA Greater Los Angeles Healthcare System, which explains the high proportion of males. All patients met the criteria for schizophrenia based upon an interview with the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID; First et al., 1997). In addition, patients were excluded for mental retardation, an identifiable neurological condition, and substance dependence within the last 6 months. All potential healthy control participants were administered the SCID and selected sections of the Structured Clinical Interview for DSM-IV Axis II Disorders (SCID-II; First et al., 1996). Potential healthy control participants were excluded if they had a history of any psychotic disorder, recurrent

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depression, bipolar disorder, substance dependence, or if they met the criteria for any of the following Axis II disorders: Avoidant, Borderline, Paranoid, Schizoid, and Schizotypal. All SCID interviewers were trained to administer the SCID in the Diagnosis and Psychopathology Unit of the UCLA Intervention Research Center. All SCID interviewers demonstrated the agreement between their ratings and the consensus ratings of the Center diagnosticians (minimum Kappa coefficient of 0.80). Written informed consent was obtained from all participants in the study. Table 1 shows the age and education of the patients and healthy control participants. Participants were administered measures of social perception, visual masking, and psychiatric symptoms during a period of assessment that lasted approximately 2.5 h. 1.2. Measures 1.2.1. Social perception Participants were administered the Half-PONS (Ambady et al., 1995), which consists of the first 110 scenes of the Profile of Nonverbal Sensitivity (PONS, Rosenthal et al., 1979). The internal consistency of the PONS ranges from 0.86 to 0.92 and its median test – retest reliability is 0.69 (Ambady et al., 1995). Scenes of this videotape-based measure last 2 s and contain the facial expressions, voice intonations,

Table 1 Age, education, social perception skill, and symptom ratings (means and standard deviations)

Age Years of education Half-PONS (total score percentage) BPRS subscales Thinking disturbance Anxiety/depression Withdrawal/retardation Hostile/suspicious SANS global ratings Affective flattening Alogia Avolition Anhedonia Inattention

Outpatients with schizophrenia (n = 40)

All healthy controls (n = 30)

Male healthy controls (n = 20)

Female healthy controls (n = 10)

43.18 (9.59) 12.75 (1.43) 72.23 (7.80)

37.27 (8.67) 13.70 (1.24) 75.48 (4.91)

36.50 (9.34) 13.70 (1.22) 75.09 (4.99)

38.80 (7.33) 13.70 (1.34) 76.27 (4.91)

2.63 2.61 2.08 1.89

(1.35) (1.03) (0.88) (0.80)

1.78 0.73 2.20 2.23 1.98

(1.19) (0.97) (1.09) (1.17) (1.51)

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and bodily gestures of a Caucasian female. That is, some scenes contain only one of these social cues, others contain two social cues, and others contain all three social cues. After watching each scene, participants were asked to select from two labels (e.g., saying a prayer, talking to a lost child) the label that best described a situation that would give rise to the social cue(s) observed. As in prior studies that have used the PONS to assess social perception in persons with schizophrenia (e.g., Monti and Fingeret, 1987; Toomey et al., 1997), the administration procedure was modified to reduce the measure’s demands on sustained attention and reading comprehension. Prior to each scene, the videotape was paused as the experimenter read the two possible labels aloud and the participant read the labels silently from a 4  6 in. index card. To ensure that the participants understood the task, a practice sample of five scenes was randomly selected from the second 110 items of the PONS and administered prior to the scored scenes. We selected the PONS to measure social perception because: (1) it has been used frequently in previous nonclinical studies of social perception, (2) it has been used successfully in studies of social perception in schizophrenia (e.g., Monti and Fingeret, 1987; Toomey et al., in press), and (3) the nonverbal nature of the test made it appropriate for a study of visual perception. The Half-PONS can yield separate scores for facial expressions, gestures, and voice intonation alone, but for this study, we focused on the total score. 1.2.2. Visual masking Early visual processing was assessed with measures of visual masking that have been described in more detail elsewhere (Green et al., 1994a,b, 1997, submitted for publication). The masking conditions were adapted for computerized presentation and are described here briefly. In visual masking, a brief visual masking stimulus either precedes (forward masking) or follows (backward masking) a brief visual target stimulus (Breitmeyer, 1984). In the present study, the target was a square with a gap on one of the three sides (up, down, or left) that could appear in one of the four locations (upper left, upper right, lower left, lower right) on the computer screen. In two of the conditions, subjects indicated what the target was; in one condition, they indicated where it appeared. The target was presented for 13 ms (2 screen sweeps). The

masking stimulus consisted of squares that occupied every possible target location. An initial psychophysical procedure determined the target threshold for each subject. The threshold was set so that each subject performed at 83% accuracy with an unmasked target. For the masking conditions, 12 trials were presented for each stimulus onset asynchrony (SOA; the interval between the onset of the target stimulus and the onset of the masking stimulus), which allowed us to counterbalance the three targets and four locations. Three masking conditions were used. Separate forward and backward masking scores were derived for each condition, yielding a total of six masking summary scores. Briefly, the masking conditions included the following. (a) Target location with a high-energy mask: in this condition, subjects indicated where the target appeared (one of the four locations). The energy of the mask was twice that of the target (4 screen sweeps (27 ms) for the mask; 2 screen sweeps for the target). The term ‘‘energy’’ here refers to the duration times intensity of a stimulus. This condition typically yields a monotonic masking function in which performance is lowest at SOA = 0. (b) Target identification with a high-energy mask: in this condition, subjects identified a target (gap up, down, or left). The energy of the mask was twice the energy of the target (4 screen sweeps for the mask; 2 for the target). This condition, like the location condition, typically yields a monotonic masking function. (c) Target identification with a low-energy mask: in this condition, subjects identified a target when the energy of the mask was half the energy of the target (1 screen sweep for the mask (7 ms); 2 for the target). This type of condition typically generates a nonmonotonic masking function (i.e., a U-shaped function). 1.2.3. Psychiatric symptoms Symptoms were measured only in the patient group. They were administered with two interviewbased measures of symptomatology: the Brief Psychiatric Rating Scale (BPRS; Ventura et al., 1993) and the Scale for the Assessment of Negative Symptoms (SANS; Andreasen, 1984). Raters who conducted the interviews had been trained to minimum intraclass correlation coefficients of 0.80 for the BPRS and 0.75

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for the SANS. BPRS ratings range from 1 (not present) to 7 (extremely severe). SANS ratings range from 0 (not at all) to 5 (severe). For the statistical analyses, the thinking disturbance subscale of the BPRS (Overall, 1974) was used as an index of positive symptoms and the sum of the global ratings on the SANS was used as an index of negative symptoms. 1.3. Statistical analyses All 40 patients completed the Half-PONS and were available for the comparison of patients and controls, but 5 patients (4 males and 1 female) did not complete the masking procedures because they were unable to complete the psychophysical procedure for setting the initial target threshold. Thus, 35 male patients were available for the analyses of the association between social perception and early visual processing. For these analyses, separate 2 (high versus low social perception)  2 (forward/backward) factorial analyses of covariance were conducted on each of the three conditions of early visual processing. Social perception (dichotomized by a median split of the patient’s total score on the Half-PONS) was a between-groups factor and forward versus backward masking was a within-subject factor. The measures of positive symptoms and negative symptoms were covariates. Patient/

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control differences in social perception skill (total score on the Half-PONS) were assessed with an analysis of covariance with education as the covariate. Given the many concerns about using analyses of covariance (Miller and Chapman, 2001), we also examined group differences in social perception with a twotailed t-test after equalizing the education of the groups by dropping patients with less than 12 years of education. When group variances differed significantly, Satterthwaite’s (1946) approximation for the degrees of freedom was used. This procedure usually results in fractional degrees of freedom.

2. Results 2.1. Social perception and early visual processing in schizophrenia The raw data from the visual masking tasks administered to the patients are shown in Figs. 1, 2, and 3. Percentage correct on the masking tasks is shown on the y-axis and stimulus onset asynchrony (SOA) between target and mask is shown on the x-axis. Forward masking trials are on the left and backward masking trials on the right. The median split of patients by social perception skill (percentage correct

Fig. 1. Target location task with high-energy masking.

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Fig. 2. Target identification task with high-energy masking.

on the Half-PONS) yielded two distinctly different groups [patients with high social perception (n = 17): mean percentage = 78.7 (3.5); patients with low social perception (n = 18): mean percentage = 67.7 (6.1)]. On the target location task with high-energy masking, patients with better social perception skill displayed better visual masking performance across

SOAs ( F(1,31) = 7.66, p < 0.01). Also, patients were more accurate in reporting target location in forward masking trials than in backward masking trials ( F(1,31) = 23.13, p < 0.0001). On the target identification task with high-energy masking, patients with better social perception skill showed better visual masking performance across

Fig. 3. Target identification task with low-energy masking.

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SOAs ( F(1,31) = 4.50, p < 0.05). Patients performed better on the backward masking trials than on the forward masking trials ( F(1,31) = 6.30, p < 0.02). On the target identification task with low-energy masking, an interaction between social perception and forward –backward masking was observed ( F(1,31) = 5.69, p < 0.03). In backward masking trials, patients with better social perception skill were more accurate than those with poor social perception skill. However, patients with high and low social perception skills did not differ in forward masking. 2.2. Group differences in social perception Table 1 shows the symptom ratings of the patients and the percentage correct on all items of the HalfPONS for patients and healthy controls. Importantly, both the positive and negative symptoms of the patients were mild. As the healthy males and females did not differ in their total scores on the Half-PONS [t (28) = 0.61, p = 0.54], they were combined in the analyses. An initial t-test indicated that the patients’ total scores on the Half-PONS were lower than those of the healthy control participants (t(66.3) = 2.14, p < 0.05). However, because the groups were not fully matched on the level of education, we treated education as a covariate. In this analysis of covariance, the patients and healthy control participants did not differ significantly in social perception ( F(1,69) = 1.21, ns). Given concerns about using analyses of covariance (Miller and Chapman, 2001), we also examined group differences in social perception with a two-tailed t-test after equalizing the education of the groups by dropping patients with less than 12 years of education. Again, the patients and healthy control participants did not differ significantly in social perception skill (t (55) = 1.00, ns).

3. Discussion This study indicates that the early visual processing assessed with visual masking procedures is associated with social perception in schizophrenia. Three previous studies reported the associations between performance on measures of social perception or emotion perception and early visual processing assessed with the Span of Apprehension Test (SPAN), a measure of

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visual scanning and iconic read out. In the present study, better social perception was significantly associated with better masking performance in all three visual masking conditions. The present findings support the hypothesis that social perception in schizophrenia is related to very early aspects of visual processing. We had further suggested that social perception may be especially related to deficits on backward, as opposed to forward, masking. This suggestion was based on the theory that backward (but not forward) masking involves transient visual channels, and we have previously suggested that these channels are aberrant in schizophrenia. One of the masking conditions (identification with low energy masking) showed this predicted pattern. The other two conditions were not consistent with this pattern because social perception was equally related to both forward and backward masking. The influence of early visual processing on social perception in schizophrenia is readily understandable when one considers the speed with which social cues are emitted. The social cues (e.g., expressive facial movements, bodily gestures) that suggest the type and intensity of another person’s emotional experience or the type or quality of the relationship between two individuals rarely last as long as those emitted by soap opera actors. For example, in one scene of the HalfPONS, the actress looks moderately upset for about 1.5 s and then suddenly thrusts her extended index finger downward in a movement that lasts a fraction of a second. The patient who is impaired in early visual processing is less likely to fully perceive the thrusting finger, less likely to appreciate the intensity of the women’s upset, and, importantly, less likely to emit an appropriate social response. Although we have a particular interest in early visual processing based on our previous findings, it is entirely possible that other neurocognitive abilities are involved with social perception. For example, vigilance and verbal memory deficits are common in schizophrenia. Persons impaired in vigilance will have difficulty accurately distinguishing relevant from irrelevant social cues over an extended period of time. Similarly, verbal memory may influence the interpretation of social cues. Persons impaired in their ability to recall recent statements during a conversation will have difficulty interpreting more ambiguous social

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cues that require verbal context for accurate interpretation. Outpatients with schizophrenia and healthy persons did not differ in their social perception skill when education was covaried. The lack of significant group difference in social perception may reflect near normal social perception in stabilized outpatients when they are presented dynamic social cues (i.e., videotaped scenes). Although deficits in social perception in schizophrenia outpatients have been observed (Corrigan et al., 1996), it is not a consistent finding. For example, several studies of emotion perception for dynamic social cues found no significant differences between stabilized outpatients and healthy persons (Bellack et al., 1996; Joseph et al., 1992; Morrison et al., 1988), suggesting that existing tests may not be optimally sensitive to diagnostic group differences. The groups were significantly different on the Half-PONS before, but not after, education was covaried. This finding may have been the result of relatively small sample sizes and a modest effect size. Curiously, the effect size of the group difference in social perception within patients (good versus poor on visual masking = 0.65) was greater than the effect size between diagnostic groups (patients versus controls = 0.37). Moreover, the limited sensitivity to diagnostic differences may have been the result of modifications to the Profile of Nonverbal Sensitivity (PONS). We may have lost some sensitivity when we reduced the total number of items (administering the first 110 of the 220 items) out of concern about possible fatigue. Likewise, the procedures (e.g., use of cards and verbal prompting) were intentionally designed to limit the influence of vigilance and verbal memory on test performance. These procedures, however, may have restricted group differences. Green and Nuechterlein (1999) recently proposed that deficits in social cognition may mediate the commonly observed relationship between neurocognition and social functioning in schizophrenia (Green, 1996). Support for this view requires the evidence of association between social cognition and neurocognition and evidence of association between social cognition and social functioning. The current study adds support for an association between social cognition (social and/or emotion perception) and neurocognition in schizophrenia (e.g., Addington and Addington, 1998; Corrigan et al., 1994; Kee et al., 1998). Support

for relationships between social cognition and social functioning in schizophrenia is not as strong, but is encouraging (Corrigan and Toomey, 1995; Penn et al., 1996). More studies — especially those examining social cognition, neurocognition, and social functioning in a single sample —are needed to examine the potential role of social cognition as an intervening variable between neurocognition and social functioning in schizophrenia.

Acknowledgements This research was supported by Dr. Sergi’s Young Investigator Award from the National Alliance for Research in Schizophrenia and Depression (NARSAD #019503) and Dr. Green’s grant from the National Institute of Mental Health (NIMH #MH43292). The authors wish to thank Kimmy Kee, PhD, Mary Jane Robertson, MS, Mark McGee, BA, Liam Zaidel, BA, Debbie Doran, BA, and Robert Holaway, BA for their assistance with the collection and coding of data. Data analyses were conducted by Sun Hwang, MS, M.P.H., Jim Mintz, PhD, and Mel Widawski, MS of the Methodological and Statistical Support Unit of the UCLA Clinical Research Center for Schizophrenia and Psychiatric Rehabilitation.

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