Imaging the “social brain” in schizophrenia: A systematic review of neuroimaging studies of social reward and punishment

https://doi.org/10.1016/j.neubiorev.2020.08.005Get rights and content

Highlights

  • People with schizophrenia spectrum disorders (SSD) experience low social motivation.

  • We review eleven articles studying affective social processing in SSD.

  • Implicated regions are widespread, but can be categorized.

  • We use a previously proposed social interaction network to describe findings.

  • Commonly identified regions include mPFC, ACC, and insula.

Abstract

Decreased social functioning and high levels of loneliness and social isolation are common in schizophrenia spectrum disorders (SSD), contributing to reduced quality of life. One key contributor to social impairment is low social motivation, which may stem from aberrant neural processing of socially rewarding or punishing stimuli. To summarize research on the neurobiology of social motivation in SSD, we performed a systematic literature review of neuroimaging studies involving the presentation of social stimuli intended to elicit feelings of reward and/or punishment. Across 11 studies meeting criteria, people with SSD demonstrated weaker modulation of brain activity in regions within a proposed social interaction network, including prefrontal, cingulate, and striatal regions, as well as the amygdala and insula. Firm conclusions regarding neural differences in SSD in these regions, as well as connections within networks, are limited due to conceptual and methodological inconsistencies across the available studies. We conclude by making recommendations for the study of social reward and punishment processing in SSD in future research.

Section snippets

Methods

We conducted a systematic review of the literature related to the functional neuroimaging of social reward and punishment in SSD. We structured our review according the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA; Moher et al., 2009) guidelines.

Results

Our search returned a total of 761 publications, with 493 remaining after removing duplicates. Three of the 493 articles were found through additional sources (e.g., in the citations of another included article). A total of 461 articles were excluded after reviewing the title/abstract, leaving 31 articles remaining. Of these, 20 articles were excluded after the full text review (see Supplementary Materials for reasons for exclusion). A total of 11 articles were included after reviewing the full

Discussion

In this systematic review of the published literature, we identified 11 studies examining neural activity in the context of social reward and punishment in SSD. These studies spanned a variety of passive and interactive paradigms in over 400 participants across 7 years. We summarized key brain structures implicated in within- and between-group differences in neural activity, highlighting those conceptualized as comprising the “social interaction” network, including mentalizing regions (TPJ,

Conclusions

In this review we summarized the current state of the literature examining the neural correlates of social reward and punishment processing in SSD. We described key findings, focusing on methodological differences across studies. We then summarized the patterns of neural activation within (e.g., reward vs. punishment) and between (SSD vs. control) groups. Finally, we made recommendations for future research focused on achieving balance between ecological validity and experimental control.

We

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References (106)

  • E. Hanssen et al.

    Cooperation and sensitivity to social feedback during group interactions in schizophrenia

    Schizophr. Res.

    (2018)
  • K. Hesse et al.

    Experimental variation of social stress in virtual reality – feasibility and first results in patients with psychotic disorders

    J. Behav. Ther. Exp. Psychiatry

    (2017)
  • K. Izuma et al.

    Processing of social and monetary rewards in the human striatum

    Neuron

    (2008)
  • A.M. Kring et al.

    The motivation and pleasure dimension of negative symptoms: neural substrates and behavioral outputs

    Eur. Neuropsychopharmacol.

    (2014)
  • M. Kubota et al.

    Alexithymia and reduced white matter integrity in schizophrenia: a diffusion tensor imaging study on impaired emotional self-awareness

    Schizophr. Res.

    (2012)
  • A. Kujawa et al.

    Electrocortical reactivity to social feedback in youth: a pilot study of the Island Getaway task

    Dev. Cogn. Neurosci.

    (2014)
  • X. Ma et al.

    Sex-and context-dependent effects of oxytocin on social sharing

    Neuroimage

    (2018)
  • B.J. Miller et al.

    How connected are people with schizophrenia? Cell phone, computer, email, and social media use

    Psychiatry Res.

    (2015)
  • K.T. Mueser et al.

    Prevalence and stability of social skill deficits in schizophrenia

    Schizophr. Res.

    (1991)
  • C. Namiki et al.

    Impaired facial emotion recognition and reduced amygdalar volume in schizophrenia

    Psychiatry Res. Neuroimaging

    (2007)
  • K.N. Ochsner

    The social-emotional processing stream: five core constructs and their translational potential for schizophrenia and beyond

    Biol. Psychiatry

    (2008)
  • S.-H. Park et al.

    Increased personal space of patients with schizophrenia in a virtual social environment

    Psychiatry Res.

    (2009)
  • J.R. Peters et al.

    The rewarding nature of provocation-focused rumination in women with borderline personality disorder: a preliminary fMRI investigation

    Borderline Personal. Disord. Emot. Dysregulation

    (2018)
  • U.J. Pfeiffer et al.

    Why we interact: on the functional role of the striatum in the subjective experience of social interaction

    Neuroimage

    (2014)
  • A.E. Pinkham et al.

    Neurocognitive and social cognitive predictors of interpersonal skill in schizophrenia

    Psychiatry Res.

    (2006)
  • M. Rus-Calafell et al.

    A virtual reality-integrated program for improving social skills in patients with schizophrenia: a pilot study

    J. Behav. Ther. Exp. Psychiatry

    (2014)
  • J.D. Salamone et al.

    The mysterious motivational functions of mesolimbic dopamine

    Neuron

    (2012)
  • C.C. Schultz et al.

    Reduced cortical thickness in first episode schizophrenia

    Schizophr. Res.

    (2010)
  • S.F. Taylor et al.

    Meta-analysis of functional neuroimaging studies of emotion perception and experience in schizophrenia

    Biol. Psychiatry

    (2012)
  • D. Alkire et al.

    Social interaction recruits mentalizing and reward systems in middle childhood

    Hum. Brain Mapp.

    (2018)
  • M. Alvarez-Jiménez et al.

    Preventing the second episode: a systematic review and meta-analysis of psychosocial and pharmacological trials in first-episode psychosis

    Schizophr. Bull.

    (2011)
  • N.C. Andreasen

    Negative symptoms in schizophrenia: definition and reliability

    JAMA Psychiatry

    (1982)
  • A. Anticevic et al.

    Amygdala recruitment in schizophrenia in response to aversive emotional material: a meta-analysis of neuroimaging studies

    Schizophr. Bull.

    (2010)
  • A.T. Beck et al.

    Cognitive approaches to schizophrenia: theory and therapy

    Annu. Rev. Clin. Psychol.

    (2005)
  • A.S. Bellack et al.

    An analysis of social competence in schizophrenia

    Br. J. Psychiatry

    (1990)
  • H. Berkowitz

    Effects of prior experimenter-subject relationships on reinforced reaction time of schizophrenics and normals

    J. Abnorm. Soc. Psychol.

    (1964)
  • F. Bitsch et al.

    Impaired right temporoparietal junction-hippocampus connectivity in schizophrenia and its relevance for generating representations of other minds

    Schizophr. Bull.

    (2019)
  • A.B. Bruehl et al.

    Neuroimaging in social anxiety disorder—a meta-analytic review resulting in a new neurofunctional model

    Neurosci. Biobehav. Rev.

    (2014)
  • L.T. Catalano et al.

    The valuation of social rewards in schizophrenia

    J. Abnorm. Psychol.

    (2018)
  • D.K. Cavanaugh et al.

    The effect of “social censure” and “social approval” on the psychomotor performance of schizophrenics

    J. Abnorm. Soc. Psychol.

    (1960)
  • A. Ciaramidaro et al.

    Do you mean me? Communicative intentions recruit the mirror and the mentalizing system

    Soc. Cogn. Affect. Neurosci.

    (2013)
  • C.C. Clements et al.

    Evaluation of the social motivation hypothesis of autism: a systematic review and meta-analysis

    JAMA Psychiatry

    (2018)
  • J.A. Coan et al.

    Lending a hand: social regulation of the neural response to threat

    Psychol. Sci.

    (2006)
  • P.W. Corrigan et al.

    Social support and recovery in people with serious mental illnesses

    Community Ment. Health J.

    (2004)
  • A.P.G. Donate et al.

    Ostracism via virtual chat room—effects on basic needs, anger and pain

    PLoS One

    (2017)
  • G.M.L. Eglit et al.

    Loneliness in schizophrenia: construct clarification, measurement, and clinical relevance

    PLoS One

    (2018)
  • O. FeldmanHall et al.

    Resolving uncertainty in a social world

    Nat. Hum. Behav.

    (2019)
  • G. Foussias et al.

    Negative symptoms in schizophrenia: avolition and Occam’s razor

    Schizophr. Bull.

    (2008)
  • R. Frömer et al.

    Goal congruency dominates reward value in accounting for behavioral and neural correlates of value-based decision-making

    Nat. Commun.

    (2019)
  • D. Fulford et al.

    Social motivation in schizophrenia: the impact of oxytocin on vigor in the context of social and nonsocial reinforcement

    J. Abnorm. Psychol.

    (2018)
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