Abnormal Neural Responses to Social Exclusion in Schizophrenia

Social exclusion is an influential concept in politics, mental health and social psychology. Studies on healthy subjects have implicated the medial prefrontal cortex (mPFC), a region involved in emotional and social information processing, in neural responses to social exclusion. Impairments in social interactions are common in schizophrenia and are associated with reduced quality of life. Core symptoms such as delusions usually have a social content. However little is known about the neural underpinnings of social abnormalities. The aim of this study was to investigate the neural substrates of social exclusion in schizophrenia. Patients with schizophrenia and healthy controls underwent fMRI while participating in a popular social exclusion paradigm. This task involves passing a ‘ball’ between the participant and two cartoon representations of other subjects. The extent of social exclusion (ball not being passed to the participant) was parametrically varied throughout the task. Replicating previous findings, increasing social exclusion activated the mPFC in controls. In contrast, patients with schizophrenia failed to modulate mPFC responses with increasing exclusion. Furthermore, the blunted response to exclusion correlated with increased severity of positive symptoms. These data support the hypothesis that the neural response to social exclusion differs in schizophrenia, highlighting the mPFC as a potential substrate of impaired social interactions.

[1]  Rick Richardson,et al.  How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence , 2004 .

[2]  Charles D. Spielberger,et al.  State-Trait Anxiety Inventory for Adults , 2012 .

[3]  K. Williams,et al.  Cyberostracism: effects of being ignored over the Internet. , 2000, Journal of personality and social psychology.

[4]  M. Rosenberg Society and the adolescent self-image , 1966 .

[5]  A. Dickinson,et al.  Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. , 2007, Brain : a journal of neurology.

[6]  Jane F. Banfield,et al.  Medial prefrontal activity predicts memory for self. , 2004, Cerebral cortex.

[7]  M. Leary,et al.  Why does social exclusion hurt? The relationship between social and physical pain. , 2005, Psychological bulletin.

[8]  Matthew F S Rushworth,et al.  The Computation of Social Behavior , 2009, Science.

[9]  S. Kapur Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. , 2003, The American journal of psychiatry.

[10]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

[11]  P. Pattison,et al.  Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. , 2002, Clinical psychology review.

[12]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[13]  M. Roesch,et al.  A new perspective on the role of the orbitofrontal cortex in adaptive behaviour , 2009, Nature Reviews Neuroscience.

[14]  M. Milders,et al.  Frontal operculum temporal difference signals and social motor response learning , 2009, Human brain mapping.

[15]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[16]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[17]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[18]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[19]  T. Heatherton,et al.  Self-esteem modulates medial prefrontal cortical responses to evaluative social feedback. , 2010, Cerebral cortex.

[20]  C. Kohler,et al.  Facial emotion perception in schizophrenia: a meta-analytic review. , 2010, Schizophrenia bulletin.

[21]  J. Decety,et al.  Social brain dysfunctions in schizophrenia: A review of neuroimaging studies , 2006, Psychiatry Research: Neuroimaging.

[22]  M. Angermeyer,et al.  The stigma of mental illness: effects of labelling on public attitudes towards people with mental disorder , 2003, Acta psychiatrica Scandinavica.

[23]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[24]  Serge A. R. B. Rombouts,et al.  Social exclusion and punishment of excluders: Neural correlates and developmental trajectories , 2012, NeuroImage.

[25]  G. Juckel,et al.  Social skills and behavioral problems in schizophrenia: The role of mental state attribution, neurocognition and clinical symptomatology , 2011, Psychiatry Research.

[26]  D. J. Lee Society and the Adolescent Self-Image , 1969 .

[27]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[28]  Iroise Dumontheil,et al.  Developmental influences on the neural bases of responses to social rejection: Implications of social neuroscience for education , 2011, NeuroImage.

[29]  E. Bora,et al.  Theory of mind impairment in schizophrenia: Meta-analysis , 2009, Schizophrenia Research.

[30]  Roz Dixon,et al.  Ostracism , 2007 .

[31]  M. Lieberman,et al.  Functional magnetic resonance imaging responses relate to differences in real-world social experience. , 2007, Emotion.

[32]  S. Woods,et al.  Chlorpromazine equivalent doses for the newer atypical antipsychotics. , 2003, The Journal of clinical psychiatry.

[33]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[34]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[35]  Ben Deen,et al.  Dissociable brain mechanisms for processing social exclusion and rule violation , 2011, NeuroImage.

[36]  S. Lawrie,et al.  Midbrain activation during Pavlovian conditioning and delusional symptoms in schizophrenia. , 2010, Archives of general psychiatry.

[37]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[38]  G. Thornicroft,et al.  Social inclusion, social quality and mental illness , 2003, British Journal of Psychiatry.

[39]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[40]  J. D Steele,et al.  Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis , 2004, NeuroImage.

[41]  Carrie L. Masten,et al.  Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. , 2009, Social cognitive and affective neuroscience.

[42]  J. Henry,et al.  The pain persists: how social exclusion affects individuals with schizophrenia. , 2011, The British journal of clinical psychology.

[43]  David L. Roberts,et al.  The functional significance of social cognition in schizophrenia: a review. , 2006, Schizophrenia bulletin.

[44]  M. Abdel-Hamid,et al.  Mental state attribution, neurocognitive functioning, and psychopathology: What predicts poor social competence in schizophrenia best? , 2007, Schizophrenia Research.