Distinct neural representations for prosocial and self-benefiting effort

Patricia Lockwood, Marco K. Wittmann, Hamed Nili, Mona Matsumoto-Ryan, Ayat Abdurahman, Jo Cutler, Masud Husain, Matthew Apps

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Abstract

Prosocial behaviors—actions that benefit others—are central to individual and societal well-being. Although the mechanisms underlying the financial and moral costs of prosocial behaviors are increasingly understood, this work has often ignored a key influence on behavior: effort. Many prosocial acts are effortful, and people are averse to the costs of exerting them. However, how the brain encodes effort costs when actions benefit others is unknown. During fMRI, participants completed a decision-making task where they chose in each trial whether to “work” and exert force (30%–70% of maximum grip strength) or “rest” (no effort) for rewards (2–10 credits). Crucially, on separate trials, they made these decisions either to benefit another person or themselves. We used a combination of multivariate representational similarity analysis and model-based univariate analysis to reveal how the costs of prosocial and self-benefiting efforts are processed. Strikingly, we identified a unique neural signature of effort in the anterior cingulate gyrus (ACCg) for prosocial acts, both when choosing to help others and when exerting force to benefit them. This pattern was absent for self-benefiting behaviors. Moreover, stronger, specific representations of prosocial effort in the ACCg were linked to higher levels of empathy and higher subsequent exerted force to benefit others. In contrast, the ventral tegmental area and ventral insula represented value preferentially when choosing for oneself and not for prosocial acts. These findings advance our understanding of the neural mechanisms of prosocial behavior, highlighting the critical role that effort has in the brain circuits that guide helping others.
Original languageEnglish
Pages (from-to)4172-4185.e7
Number of pages38
JournalCurrent Biology
Volume32
Issue number19
Early online date26 Aug 2022
DOIs
Publication statusPublished - 10 Oct 2022

Bibliographical note

Funding Information:
This work was supported by a Medical Research Council Fellowship ( MR/P014097/1 and MR/P014097/2 ), a Sir Henry Dale Fellowship funded by the Wellcome Trust and the Royal Society ( 223264/Z/21/Z ), a Christ Church Junior Research Fellowship, a Christ Church Research Centre Grant, and a Jacobs Foundation Research Fellowship to P.L.L.; a Biotechnology and Biological Sciences Research Council David Phillips Fellowship ( BB/R010668/1 ) and a Wellcome Trust Institutional Strategic Support Fund grant awarded to M.A.J.A.; a Wellcome Trust Principal Fellowship to M.H.; and the National Institute for Health Research Biomedical Research Centre , Oxford, United Kingdom. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust ( 203139/Z/16/Z ). We are grateful to Matthew Rushworth, Miriam Klein-Flugge, and Ali Mahmoodi for helpful discussions and to Tanja Muller for input with experimental code. We are also grateful to our colleagues who acted as the other participant during the study.

Funding Information:
This work was supported by a Medical Research Council Fellowship (MR/P014097/1 and MR/P014097/2), a Sir Henry Dale Fellowship funded by the Wellcome Trust and the Royal Society (223264/Z/21/Z), a Christ Church Junior Research Fellowship, a Christ Church Research Centre Grant, and a Jacobs Foundation Research Fellowship to P.L.L.; a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BB/R010668/1) and a Wellcome Trust Institutional Strategic Support Fund grant awarded to M.A.J.A.; a Wellcome Trust Principal Fellowship to M.H.; and the National Institute for Health Research Biomedical Research Centre, Oxford, United Kingdom. The Wellcome Centre for Integrative Neuroimaging is supported by core funding from the Wellcome Trust (203139/Z/16/Z). We are grateful to Matthew Rushworth, Miriam Klein-Flugge, and Ali Mahmoodi for helpful discussions and to Tanja Muller for input with experimental code. We are also grateful to our colleagues who acted as the other participant during the study. Conceptualization, P.L.L. and M.A.J.A.; methodology, P.L.L. M.K.W. H.N. and M.A.J.A.; investigation, P.L.L. M.M.-R. and A.A.; formal analysis, P.L.L. M.K.W. H.N. J.C. and M.A.J.A.; writing – original draft, P.L.L. M.M.-R. and M.A.J.A.; writing – review & editing, P.L.L. M.K.W. H.N. M.M.-R. A.A. J.C. M.H. and M.A.J.A.; funding acquisition, P.L.L. M.A.J.A. and M.H.; supervision, P.L.L. M.A.J.A. and M.H. The authors declare no competing interests. We worked to ensure gender balance in the recruitment of human subjects. We worked to ensure that the study questionnaires were prepared in an inclusive way. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper self-identifies as living with a disability. The author list of this paper includes contributors from the location where the research was conducted who participated in the data collection, design, analysis, and/or interpretation of the work.

Publisher Copyright:
© 2022 The Author(s)

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Keywords

  • social behavior
  • prosocial
  • effort
  • fMRI
  • reward
  • representational similarity analysis
  • computational modeling
  • decision-making
  • anterior cingulate cortex
  • insula

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Neuroscience(all)

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