Running head: PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA

People with schizophrenia have problems with social functioning, and it may be related to deficits in processing social information. This study investigated how people with schizophrenia process eye gaze, a form of self-referential social information, and whether it is related to paranoia symptoms in schizophrenia. Twenty-one participants with schizophrenia and 26 healthy controls were shown facial stimuli that differed on three dimensions: eye gaze direction, head orientation, and emotion. The participants chose whether they thought the person was looking at them or away from them. Their accuracy, response time, and event-related potentials (ERPs) were recorded. Although participants with schizophrenia did not differ from controls in accuracy, they had a longer reaction time compared to controls. N170 amplitudes in schizophrenia participants were comparable to controls’, but were affected by eye gaze direction and facial emotion in an opposite direction than in controls. Patients had an overall reduction in the P300 amplitude compared to controls, and they failed to show enlarged P300 to fearful faces relative to neutral faces as controls did. However, these processes were not significantly correlated with paranoia symptoms. These findings suggest that schizophrenia is characterized by abnormal modulation by emotion and gaze direction in facial structure encoding and reduced mental resources for memory update for salient information when they process self-referential and emotional social information. Limitations of this study and directions for future research were discussed. PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA 3 Psychophysiological Processing of Emotional and Self-Referential Information in Schizophrenia Schizophrenia can cause people with the disorder to be severely affected in their everyday lives. For example, people with schizophrenia can have trouble interpreting abstract social signals, such as other people’s facial expressions and intentions (Corrigan & Green, 1993). This difficulty in social cognition can affect social and occupational functioning (Addington, Saeedi, & Addington, 2006). Paranoia is a major symptom of schizophrenia in which people mistakenly believe that people are directing their intentions toward them even if they are not, including thoughts such as “They are staring at me” or “They are out to get me”. These paranoid thoughts are related to self-referential processing because they are misinterpretations of information directed at the self. It has been shown that people with schizophrenia exhibit abnormal patterns of brain activity during theory of mindrelated tasks (Park et al., 2011); however, instead of investigating general theory of mind, investigating self-directed social information processing can provide more evidence into the symptom of paranoia. Understanding the neurocognitive functions related to self-referential information processing can offer insight into the social difficulties in schizophrenia and may inform treatment options. Below I will review research in gaze processing in schizophrenia and two other factors, emotion and head orientation, that potentially influence gaze processing in schizophrenia. Eye Gaze Processing in Schizophrenia Eye contact is generally maintained throughout a social interaction by both parties and it is independent of other social cues (Kleinke, 1986). People spend more time looking at internal facial features, especially eyes, than at other facial features. Eye gaze during interactions between people can show several crucial social signals, including attention, synchronization and social control (see Itier & Batty, 2009 for review). Because eye gaze is crucial to social PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA 4 interactions and is used in interpreting others’ intentions and goals, eye gaze is a good example of self-referential signals. A study by Choi et al. (2010) explored the nature of eye gaze in patients with schizophrenia during emotional social situations. This study used a virtual reality system to place patients and controls in virtual social situations that were either positive or negative. The participant’s gaze was detected and measured during the interaction. The patients with schizophrenia had reduced eye gaze directed at the virtual person with whom they were interacting compared to controls, particularly in negative social situations, suggesting differences in receiving social input, especially in negative situations. In addition to differences in directing their own eye gaze, several studies propose a tendency for patients to think people are looking at them even if they are not. Rosse, Kendrick, Wyatt, and Isaac (1994) suggested that people with schizophrenia were more likely than controls to perceive a face looking at them even when it was looking away from them. A study by Hooker and Park (2005) supports these findings. Patients with schizophrenia and controls were briefly shown a face and were instructed to decide if the person was looking at them. They were also presented with a geometric control task in which they were shown a black box inside a rectangle and they needed to determine if the box was in the center of the rectangle. The people with schizophrenia judged that the person was looking at them significantly more than controls even when the gaze was actually averted; however they had no differences from controls in the geometric control task. Therefore, the authors concluded that the patients with schizophrenia had a direct gaze bias which is not solely due to general perceptual difficulties. However, some studies conflicted with these results and found that people with schizophrenia do not have deficits in gaze processing. When patients with schizophrenia and PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA 5 controls chose whether gaze was directed to the right or the left, no impairment in schizophrenia was found (Franck et al., 1998). Another study investigated both deciding between left or right gaze and whether or not the face is looking at you. The study found that people with schizophrenia did not have a difference from controls in distinguishing the correct gaze direction (Franck et al., 2002). If this is the case, delusions may be a result of higher level processing rather than eye gaze. This is supported by a study which found that although people with schizophrenia had no differences from controls in determining the eye gaze of a face, they had different brain activation patterns in the frontal and temporal regions than controls (Kohler et al., 2008). The different brain activation may suggest higher level processing involved in the schizophrenia symptoms. Because of the methodological variations in these studies, further study is needed to clarify whether gaze processing is impaired and what role it plays in schizophrenia. Emotional Processing in Schizophrenia Abnormal emotional processing has been widely reported in schizophrenia. The negative symptoms of schizophrenia have been a focus of emotion research in schizophrenia due to their broad effects to diminish emotional experience. For example, patients with schizophrenia reported more negative reactions to both positive and neutral stimuli compared to controls (see Cohen, Minor, & Najolia, 2010 for review). Another difference in schizophrenia from controls is disruptions in sustained attentional processing of emotional stimuli. While individuals with schizophrenia did not differ from controls in the initial sensory processing of positive stimuli, they had trouble sustaining the pleasurable feelings (Horan, Wynn, Kring, Simons, & Green, 2010). This may affect social interactions, because positive interactions with others may be forgotten or not fully processed. PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA 6 People with schizophrenia have also shown impairment in emotional recognition (Kee, Horan, Wynn, Mintz, & Green, 2006; Kohler, Walker, Martin, Healey, & Moberg, 2010). A recent event-related potential (ERP) study showed that the P3a component during an identity recognition task of emotional faces was also lower for schizophrenic patients than controls, implying difficulty focusing on emotional cues and attending on emotional recognition (RamosLoyo, Gonzalez-Garrido, Sanchez-Loyo, Medina, & Basar-Eroglu, 2009). Difficulty in emotional processing in schizophrenia may be due to problems with early facial recognition. Patients with schizophrenia have been shown to have impairments in early facial recognition and encoding as suggested by reduced P1 (sensory stage) and N170 (perceptual stage) amplitudes (Caharel et al., 2007). Turetsky et al. (2007) examined how this deficit in early facial encoding affects emotional processing. In their study of 16 participants with schizophrenia and 16 controls, the participants were shown pictures of faces with different emotions (e.g., very sad, somewhat sad, neutral, somewhat happy, or very happy) that were briefly presented for 100 ms, and they were asked to identify the emotions. The behavioral results showed that participants with schizophrenia were less accurate than controls in recognizing emotions. The ERP showed that the participants with schizophrenia showed deficits in early facial processing, quantified by the reduced amplitude of the N170 component, which represents early structural encoding of faces. This suggests that the difficulties in schizophrenia with emotional recognition may be attributed to problems with initial processing of faces. Another study also showed an N170 deficit in schizophrenia, supporting that the impaired emotional processing abilities in people with schizophrenia is related to impairment in early visual recognition. Bediou et al. (2007) asked 10 healthy controls and 10 patients with schizophrenia to identify the emotions of faces displayed to them. The results showed that the early processing component, N170, of the facial PSYCHOPHYSIOLOGICAL PROCESSING IN SCHIZOPHRENIA 7 structure encoding was lower in people with schizophrenia compared to controls during the emotional recognition task. They suggested that this difference may explain the disruption in the later processes of emotional recognition. People with schizophrenia have been shown to have difficulty with processing early facial and emotional components, but few studies have examined this in relation to specific symptoms in the disorder. A study by Herrmann, Reif, Jabs, Jacob and Fallgatter (2006) showed that participants with schizophrenia with paranoid symptoms have over-activation of the brain as measured with ERP (P300 and P400) to neutral faces in comparison to participants with schizophrenia without paranoid symptoms. The paranoid subgroup showed higher activation than the non-paranoid subgroup during the neutral facial expressions, which may be interpreted as the tendency for schizophrenia patients high in paranoid symptoms to misread neutral situations as salient. This study provided preliminary evidence for the relationship between emotion processing and specific schizophrenia symptoms, and further investigation is warranted to confirm this relationship.