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The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys.

Authors
  • Basile, Benjamin M1
  • Schafroth, Jamie L1
  • Karaskiewicz, Chloe L1
  • Chang, Steve W C2, 3, 4
  • Murray, Elisabeth A1
  • 1 Section on the Neurobiology of Learning and Memory, Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland, United States of America. , (United States)
  • 2 Department of Psychology, Yale University, New Haven, Connecticut, United States of America. , (United States)
  • 3 Department of Neuroscience, Yale School of Medicine, New Haven, Connecticut, United States of America. , (United States)
  • 4 Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, Connecticut, United States of America. , (United States)
Type
Published Article
Journal
PLoS Biology
Publisher
Public Library of Science
Publication Date
Jun 01, 2020
Volume
18
Issue
6
Identifiers
DOI: 10.1371/journal.pbio.3000677
PMID: 32530910
Source
Medline
Language
English
License
Unknown

Abstract

A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.

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