Social cognition over time in individuals at clinical high risk for psychosis: Findings from the NAPLS-2 cohort

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Abstract

Deficits in social cognition are well established in schizophrenia and have been observed prior to the illness onset. Compared to healthy controls (HCs), individuals at clinical high risk of psychosis (CHR) are said to show deficits in social cognition similar to those observed in patients experiencing a first episode of psychosis. These deficits have been observed in several domains of social cognition, such as theory of mind (ToM), emotion perception and social perception. In the current study, the stability of three domains of social cognition (ToM, social perception and facial emotion perception) was assessed over time along and their association with both clinical symptoms and the later development of psychosis. Six hundred and seventy-five CHR individuals and 264 HC participants completed four tests of social cognition at baseline. Of those, 160 CHR and 155 HC participants completed assessments at all three time points (baseline, 1 year and 2 years) as part of their participation in the North American Prodrome Longitudinal Study. The CHR group performed poorer on all tests of social cognition across all time points compared to HCs. Social cognition was not associated with attenuated positive symptoms at any time point in the study. CHR individuals who developed a psychotic disorder during the course of the study did not differ in social cognition compared to those who did not develop psychosis. This longitudinal study demonstrated mild to moderate, but persistent ToM and social perception impairments in those at CHR for psychosis compared to HCs.

Introduction

The NIMH Workshop of Social Cognition in Schizophrenia defines social cognition as a function that involves the perception, interpretation and processing of information that underlies social interactions. Because of the emphasis on a direct association with social behavior and a number of real world outcomes, social cognition has become one of the major areas of interest in schizophrenia (Pinkham et al., 2014). This is not accidental or surprising given overwhelming reports of poor social and role functioning in schizophrenia. The Social Cognition Psychometric Evaluation (SCOPE) study (Pinkham et al., 2014), which was designed to achieve a consensus on the key domains of social cognition in schizophrenia based on the expert advice, identified four major domains of social cognition: 1) theory of mind (ToM) or the ability to attribute beliefs and intentions to oneself and others; 2) emotion perception (both prosodic and facial) or the ability to recognize other people's feelings from either facial expressions or vocal inflections and use them to guide behaviors; 3) social perception and knowledge or the ability to judge and be aware of cues and rules that occur in social situations; and 4) attributional style or bias, which refers to an individual's tendency to attribute the cause of an event to either oneself, others or the environment. Deficits in social cognition are well evidenced in schizophrenia, both in the established illness (Penn et al., 2008) and prior to the illness onset (Barbato et al., 2015, Green et al., 2012) suggesting that they are relatively stable (Horan et al., 2012).

Recent progress in risk identification methodology has made it possible to identify individuals who are at clinical high risk of developing psychosis (CHR) based on clinical phenomenology, in particular sub-threshold psychotic symptoms (Addington and Heinssen, 2012). In the past decade, there has been a surge of studies examining social cognition in CHR populations compared to healthy controls (HCs) and patients with psychosis. Although the findings from these studies are mixed, the majority report quantifiable deficits in social cognition in CHR populations relative to healthy controls. Furthermore, the severity of those deficits is often similar to patients with psychotic disorders (Green et al., 2012, Thompson et al., 2011). Two recent meta-analyses of social cognition in CHR, reported deficits in all domains of social cognition (Lee et al., 2015, van Donkersgoed et al., 2015). The largest cumulative deficits have been observed in attributional bias and ToM, with somewhat smaller effects for emotion perception and social perception. The overall magnitude of social cognitive deficits in those at CHR fell between that of schizophrenia patients and their non-affected relatives (Lee et al., 2015). However, despite relatively consistent findings of social cognitive deficits in CHR samples, some reports support (Bora et al., 2008, Healey et al., 2013) and others deny (Lee et al., 2015, van Donkersgoed et al., 2015) whether social cognitive deficits predict conversion to psychosis.

Most studies that have examined social cognition in CHR to date have been based on small samples and have examined only one or two social cognitive domains at a time. The North American Prodrome Longitudinal Study (NAPLS 2) group recently published baseline data on social cognition and its association with symptoms in a large group of CHR participants assessing three different domains: ToM, social perception and facial emotion perception. At study entry, the CHR group showed deficits in all domains of social cognition compared to age and gender matched HCs. These deficits however, were not related to attenuated positive and negative symptom severity (Barbato et al., 2015). The aim of the current paper is to examine: first, the stability of social cognition over time; secondly, the cross-sectional correlations between social cognition and clinical symptoms at each time point; and thirdly to examine whether there are differences in social cognition between those who develop psychosis and those who do not in the NAPLS 2 sample.

Section snippets

Participants

Participants were recruited as part of the multi-site NIMH funded NAPLS 2 that consisted of 764 CHR individuals (436 males, 328 females) and 280 HCs (141 males, 139 females) recruited across the eight NAPLS 2 sites. The majority, 743 CHR subjects, met the Criteria of Prodromal Syndromes (COPS) (McGlashan et al., 2010), however 21 CHR subjects were considered high risk due to presence of schizotypal features and age less than 18. Participants were excluded if they met criteria for any current or

Results

Six hundred and seventy-five CHR individuals (389 males and 286 females) and 264 HCs completed the social cognition assessments at baseline. Of those 675 CHR participants, 317 completed the one year follow-up, 188 completed the 2 year follow-up and 160 participants completed assessments at all three time points. Seventy-five CHR participants completed only the baseline assessment because they made the transition to psychosis within the first year. For the HCs, 115 participants completed all 3

Discussion

The CHR group performed poorer on all tests of social cognition across all time points compared to HCs even though magnitudes of group differences varied depending on the social cognitive domain and/or the assessment time point. Moderate differences between groups were noted in ToM and social perception at baseline and while these differences remained at follow-up assessments, the magnitude of differences decreased over time.

The observed deficit in ToM ability confirms previous evidence that

Contributors

Dr. Piskulic and Ms. Liu undertook the statistical analysis, and Dr. Piskulic wrote the first draft of the manuscript. Dr. Addington was involved in writing of subsequent drafts of the manuscript. All of the authors listed were involved in study design and have contributed to and approved the final manuscript.

Conflict of interest

There are no conflicts of interest for any of the authors with respect to the data in this paper or for the study.

Role of funding source

This study was supported by the National Institute of Mental Health (grant U01 MH081984 to Dr. Addington; grants U01 MH081928; P50 MH080272; Commonwealth of Massachusetts SCDMH82101008006 to Dr. Seidman; grants R01 MH60720, U01 MH082022 and K24 MH76191 to Dr. Cadenhead; grant U01 MH081902 to Dr. Cannon; P50 MH066286 (Prodromal Core) to Dr. Bearden; grant U01 MH082004 to Dr. Perkins; grant U01 MH081988 to Dr. Walker; grant U01 MH082022 to Dr. Woods; and U01 MH081857-05 grant to Dr. Cornblatt.

Acknowledgments

The authors would like to acknowledge Dr. Monica Calkins, Dr. Christian Kohler and Dr. Ruben Gur for their valued assistance with the facial affect tasks.

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