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Neural, behavioural and real-life correlates of social context sensitivity and social reward learning during interpersonal interactions in the schizophrenia spectrum

Hanssen, E., van Buuren, M., Van Atteveldt, N. , Lemmers-Jansen, I. L. J. & Fett, A-K. ORCID: 0000-0003-0282-273X (2022). Neural, behavioural and real-life correlates of social context sensitivity and social reward learning during interpersonal interactions in the schizophrenia spectrum. Australian and New Zealand Journal of Psychiatry, 56(1), pp. 59-70. doi: 10.1177/00048674211010327

Abstract

Objective
Recent findings suggest that diminished processing of positive contextual information about others during interactions may contribute to social impairment in the schizophrenia spectrum (SZ). This could be due to general social context processing deficits or specific biases against positive information. We studied the impact of positive and negative social contextual information during social interactions using functional neuroimaging and probed whether these neural mechanisms were associated with reallife social functioning in SZ.

Methods
Patients with SZ (N=23) and controls (N=25) played three multi-round trust games during fMRI scanning, with no, positive and negative information about the counterpart’s trustworthiness, while all counterparts were programmed to behave trustworthy. The main outcome variable was the height of the shared amount in the trust game, i.e. investment, representing an indication of trust. The first investment in the game was considered to be basic trust, since no behavioural feedback was given yet. We performed region-of-interest analyses and examined the association with real-life social functioning using the Experience Sampling Method.

Results
Social contextual information had no effect on patients’ first investments, whereas controls made the lowest investment after negative and the highest investments after positive contextual information was provided. Over trials, patients decreased investments, suggesting reduced social reward learning, whereas controls increased investments in response to behavioural feedback in the negative context. Patients engaged the dorsolateral prefrontal cortex (dlPFC) less than controls during context presentation and showed reduced activity within the caudate during repayments. In patients, lower investments were associated with more time spent alone and social exclusion and lower caudate activation was marginally significantly associated with higher perceived social exclusion.

Conclusion
The failure to adapt trust to positive and negative social contexts suggests that patients have a general insensitivity to prior social information, indicating top-down processing impairments. In addition, patients show reduced sensitivity to social reward, i.e. bottom-up processing deficits. Moreover, lower trust and lower neural activation were related to lower real-life social functioning. Together, these findings indicate that improving trust and social interactions in SZ needs a multi-faceted approach that targets both mechanisms.

Publication Type: Article
Additional Information: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
Publisher Keywords: Functional magnetic resonance imaging, experience sampling method, trust, schizophrenia, social context processing
Subjects: B Philosophy. Psychology. Religion > BF Psychology
H Social Sciences > HM Sociology
R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
Departments: School of Health & Psychological Sciences > Psychology
SWORD Depositor:
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