Distinct neural computations scale the violation of expected reward and emotion in social transgressions

Abstract Traditional decision-making models conceptualize humans as adaptive learners utilizing the differences between expected and actual rewards (prediction errors, PEs) to maximize outcomes, but rarely consider the influence of violations of emotional expectations (emotional PEs) and how it diff...

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Main Authors: Ting Xu, Lei Zhang, Feng Zhou, Kun Fu, Xianyang Gan, Zhiyi Chen, Ran Zhang, Chunmei Lan, Lan Wang, Keith M. Kendrick, Dezhong Yao, Benjamin Becker
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-025-07561-7
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author Ting Xu
Lei Zhang
Feng Zhou
Kun Fu
Xianyang Gan
Zhiyi Chen
Ran Zhang
Chunmei Lan
Lan Wang
Keith M. Kendrick
Dezhong Yao
Benjamin Becker
author_facet Ting Xu
Lei Zhang
Feng Zhou
Kun Fu
Xianyang Gan
Zhiyi Chen
Ran Zhang
Chunmei Lan
Lan Wang
Keith M. Kendrick
Dezhong Yao
Benjamin Becker
author_sort Ting Xu
collection DOAJ
description Abstract Traditional decision-making models conceptualize humans as adaptive learners utilizing the differences between expected and actual rewards (prediction errors, PEs) to maximize outcomes, but rarely consider the influence of violations of emotional expectations (emotional PEs) and how it differs from reward PEs. Here, we conducted a fMRI experiment (n = 43) using a modified Ultimatum Game to examine how reward and emotional PEs affect punishment decisions in terms of rejecting unfair offers. Our results revealed that reward relative to emotional PEs exerted a stronger prediction to punishment decisions. On the neural level, the left dorsomedial prefrontal cortex (dmPFC) was strongly activated during reward receipt whereas the emotions engaged the bilateral anterior insula. Reward and emotional PEs were also encoded differently in brain-wide multivariate patterns, with a more sensitive neural signature observed within fronto-insular circuits for reward PE. We further identified a fronto-insular network encompassing the left anterior cingulate cortex, bilateral insula, left dmPFC and inferior frontal gyrus that encoded punishment decisions. In addition, a stronger fronto-insular pattern expression under reward PE predicted more punishment decisions. These findings underscore that reward and emotional violations interact to shape decisions in complex social interactions, while the underlying neurofunctional PEs computations are distinguishable.
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spelling doaj-art-be1d0398c11a46ccb897dcf278195d2f2025-01-26T12:47:58ZengNature PortfolioCommunications Biology2399-36422025-01-018111210.1038/s42003-025-07561-7Distinct neural computations scale the violation of expected reward and emotion in social transgressionsTing Xu0Lei Zhang1Feng Zhou2Kun Fu3Xianyang Gan4Zhiyi Chen5Ran Zhang6Chunmei Lan7Lan Wang8Keith M. Kendrick9Dezhong Yao10Benjamin Becker11Faculty of Psychology, Southwest UniversityCentre for Human Brain Health, School of Psychology, University of BirminghamFaculty of Psychology, Southwest UniversityThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaFaculty of Psychology, Southwest UniversityFaculty of Psychology, Southwest UniversityThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaThe Center of Psychosomatic Medicine, Sichuan Provincial Center for Mental Health, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of ChinaDepartment of Psychology, The University of Hong KongAbstract Traditional decision-making models conceptualize humans as adaptive learners utilizing the differences between expected and actual rewards (prediction errors, PEs) to maximize outcomes, but rarely consider the influence of violations of emotional expectations (emotional PEs) and how it differs from reward PEs. Here, we conducted a fMRI experiment (n = 43) using a modified Ultimatum Game to examine how reward and emotional PEs affect punishment decisions in terms of rejecting unfair offers. Our results revealed that reward relative to emotional PEs exerted a stronger prediction to punishment decisions. On the neural level, the left dorsomedial prefrontal cortex (dmPFC) was strongly activated during reward receipt whereas the emotions engaged the bilateral anterior insula. Reward and emotional PEs were also encoded differently in brain-wide multivariate patterns, with a more sensitive neural signature observed within fronto-insular circuits for reward PE. We further identified a fronto-insular network encompassing the left anterior cingulate cortex, bilateral insula, left dmPFC and inferior frontal gyrus that encoded punishment decisions. In addition, a stronger fronto-insular pattern expression under reward PE predicted more punishment decisions. These findings underscore that reward and emotional violations interact to shape decisions in complex social interactions, while the underlying neurofunctional PEs computations are distinguishable.https://doi.org/10.1038/s42003-025-07561-7
spellingShingle Ting Xu
Lei Zhang
Feng Zhou
Kun Fu
Xianyang Gan
Zhiyi Chen
Ran Zhang
Chunmei Lan
Lan Wang
Keith M. Kendrick
Dezhong Yao
Benjamin Becker
Distinct neural computations scale the violation of expected reward and emotion in social transgressions
Communications Biology
title Distinct neural computations scale the violation of expected reward and emotion in social transgressions
title_full Distinct neural computations scale the violation of expected reward and emotion in social transgressions
title_fullStr Distinct neural computations scale the violation of expected reward and emotion in social transgressions
title_full_unstemmed Distinct neural computations scale the violation of expected reward and emotion in social transgressions
title_short Distinct neural computations scale the violation of expected reward and emotion in social transgressions
title_sort distinct neural computations scale the violation of expected reward and emotion in social transgressions
url https://doi.org/10.1038/s42003-025-07561-7
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