Neuroimaging of social motivation during winning and losing: Associations with social anhedonia across the psychosis spectrum

Amy M. Jimenez; Peter E. Clayson; Arpi S. Hasratian; Junghee Lee; Eric A. Reavis; Jonathan K. Wynn; Michael F. Green; William P. Horan

doi:10.1016/j.neuropsychologia.2023.108621

Neuroimaging of social motivation during winning and losing: Associations with social anhedonia across the psychosis spectrum

Amy M. Jimenez, Peter E. Clayson, Arpi S. Hasratian, Junghee Lee, Eric A. Reavis, Jonathan K. Wynn, Michael F. Green, William P. Horan

Research output: Contribution to journal › Article › peer-review

Abstract

Background: Individuals with psychosis spectrum disorders (PSD) have difficulty developing social relationships. This difficulty may reflect reduced response to social feedback involving functional alterations in brain regions that support the social motivation system: ventral striatum, orbital frontal cortex, insula, dorsal anterior cingulate cortex, and amygdala. Whether these alterations span PSD is unknown. Methods: 71 individuals with PSD, 27 unaffected siblings, and 37 control participants completed a team-based fMRI task. After each trial, participants received performance feedback paired with the expressive face of a teammate or opponent. A 2 × 2 (win versus loss outcome x teammate versus opponent) repeated measures ANOVA by group was performed on activation in the five key regions of interest during receipt of feedback. Results: Across groups, three social motivation regions, ventral striatum, orbital frontal cortex, and amygdala, showed sensitivity to feedback (significant main effect of outcome), with greater activation during win versus loss trials, regardless of whether the feedback was from a teammate or opponent. In PSD, ventral striatum and orbital frontal cortex activation to win feedback was negatively correlated with social anhedonia scores. Conclusions: Patterns of neural activation during social feedback were similar in PSD, their unaffected siblings, and healthy controls. Across the psychosis spectrum, activity in key social motivation regions during social feedback was associated with individual differences in social anhedonia.

Original language	English
Article number	108621
Journal	Neuropsychologia
Volume	188
DOIs	https://doi.org/10.1016/j.neuropsychologia.2023.108621
State	Published - 9 Sep 2023
Externally published	Yes

Bibliographical note

Funding Information:
This research was supported by NIMH Grant 1R01MH107422 (PI: W. Horan). This manuscript is the result of work supported in part with resources and the use of facilities at the Department of Veterans Affairs Greater Los Angeles Healthcare System, VISN 22 Mental Illness Research, Education and Clinical Center (MIRECC) . The authors would like to thank Ana Ceci Myers, Julio Iglesias, James R. Lopez, Jasmin Humble, and the rest of the laboratory staff for assistance in data collection. We also would like to thank One Mind – Center for Cognitive Neuroscience at UCLA for their generous support to the CCN scanner. For generous support, we also thank the Brain Mapping Medical Research Organization, Brain Mapping Support Foundation, Pierson-Lovelace Foundation , The Ahmanson Foundation , William M. and Linda R. Dietel Philanthropic Fund at the Northern Piedmont Community Foundation , Tamkin Foundation, Jennifer Jones-Simon Foundation, Capital Group Companies Charitable Foundation, Robson Family, and Northstar Fund. fMRI data analysis for this study used computational and storage services associated with the Hoffman2 Shared Cluster provided by UCLA Institute for Digital Research and Education's Research Technology Group. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans Affairs or the United States government. These data were presented at the 2021 Society for Research in Psychopathology Annual Meeting.

Funding Information:
This research was supported by NIMH Grant 1R01MH107422 (PI: W. Horan). This manuscript is the result of work supported in part with resources and the use of facilities at the Department of Veterans Affairs Greater Los Angeles Healthcare System, VISN 22 Mental Illness Research, Education and Clinical Center (MIRECC). The authors would like to thank Ana Ceci Myers, Julio Iglesias, James R. Lopez, Jasmin Humble, and the rest of the laboratory staff for assistance in data collection. We also would like to thank One Mind – Center for Cognitive Neuroscience at UCLA for their generous support to the CCN scanner. For generous support, we also thank the Brain Mapping Medical Research Organization, Brain Mapping Support Foundation, Pierson-LovelaceFoundation, The Ahmanson Foundation, William M. and Linda R. Dietel Philanthropic Fund at the Northern Piedmont Community Foundation, Tamkin Foundation, Jennifer Jones-Simon Foundation, Capital Group Companies Charitable Foundation, Robson Family, and Northstar Fund. fMRI data analysis for this study used computational and storage services associated with the Hoffman2 Shared Cluster provided by UCLA Institute for Digital Research and Education's Research Technology Group. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans Affairs or the United States government. These data were presented at the 2021 Society for Research in Psychopathology Annual Meeting.

Publisher Copyright:
© 2023

Keywords

Functional magnetic resonance imaging (fMRI)
Psychotic disorders
Schizophrenia
Sibling study
Social anhedonia
Social motivation
Social reward
Team task

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10.1016/j.neuropsychologia.2023.108621

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title = "Neuroimaging of social motivation during winning and losing: Associations with social anhedonia across the psychosis spectrum",

abstract = "Background: Individuals with psychosis spectrum disorders (PSD) have difficulty developing social relationships. This difficulty may reflect reduced response to social feedback involving functional alterations in brain regions that support the social motivation system: ventral striatum, orbital frontal cortex, insula, dorsal anterior cingulate cortex, and amygdala. Whether these alterations span PSD is unknown. Methods: 71 individuals with PSD, 27 unaffected siblings, and 37 control participants completed a team-based fMRI task. After each trial, participants received performance feedback paired with the expressive face of a teammate or opponent. A 2 × 2 (win versus loss outcome x teammate versus opponent) repeated measures ANOVA by group was performed on activation in the five key regions of interest during receipt of feedback. Results: Across groups, three social motivation regions, ventral striatum, orbital frontal cortex, and amygdala, showed sensitivity to feedback (significant main effect of outcome), with greater activation during win versus loss trials, regardless of whether the feedback was from a teammate or opponent. In PSD, ventral striatum and orbital frontal cortex activation to win feedback was negatively correlated with social anhedonia scores. Conclusions: Patterns of neural activation during social feedback were similar in PSD, their unaffected siblings, and healthy controls. Across the psychosis spectrum, activity in key social motivation regions during social feedback was associated with individual differences in social anhedonia.",

keywords = "Functional magnetic resonance imaging (fMRI), Psychotic disorders, Schizophrenia, Sibling study, Social anhedonia, Social motivation, Social reward, Team task",

author = "Jimenez, {Amy M.} and Clayson, {Peter E.} and Hasratian, {Arpi S.} and Junghee Lee and Reavis, {Eric A.} and Wynn, {Jonathan K.} and Green, {Michael F.} and Horan, {William P.}",

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AU - Hasratian, Arpi S.

AU - Lee, Junghee

AU - Reavis, Eric A.

AU - Wynn, Jonathan K.

AU - Green, Michael F.

AU - Horan, William P.

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Neuroimaging of social motivation during winning and losing: Associations with social anhedonia across the psychosis spectrum

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