4.8 Article

Frontal neurons driving competitive behaviour and ecology of social groups

Journal

NATURE
Volume 603, Issue 7902, Pages 661-+

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41586-021-04000-5

Keywords

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Funding

  1. Autism Science Foundation
  2. NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation
  3. NIH [U01NS123130, R01HD059852, R01NS091390]
  4. MGH-ECOR Fund for Medical Discovery Fellowship

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Competitive interactions play a vital role in the ecology of animal species and strongly influence group behavior. Researchers have discovered neurons in the anterior cingulate that adaptively represent the social rank of animals and influence their decision-making. These neurons can track other individuals within a group and accurately predict future success. The application of neuromodulation techniques also reveals that these neurons conditionally influence competitive effort.
Competitive interactions have a vital role in the ecology of most animal species(1-3) and powerfully influence the behaviour of groups(4,5). To succeed, individuals must exert effort based on not only the resources available but also the social rank and behaviour of other group members(2,6,)(7). The single-cellular mechanisms that precisely drive competitive interactions or the behaviour of social groups, however, remain poorly understood. Here we developed a naturalistic group paradigm in which large cohorts of mice competitively foraged for food as we wirelessly tracked neuronal activities across thousands of unique interactions. By following the collective behaviour of the groups, we found neurons in the anterior cingulate that adaptively represented the social rank of the animals in relation to others. Although social rank was closely behaviourally linked to success, these cells disambiguated the relative rank of the mice from their competitive behaviour, and incorporated information about the resources available, the environment, and past success of the mice to influence their decisions. Using multiclass models, we show how these neurons tracked other individuals within the group and accurately predicted upcoming success. Using neuromodulation techniques, we also show how the neurons conditionally influenced competitive effort-increasing the effort of the animals only when they were more dominant to their groupmates and decreasing it when they were subordinate-effects that were not observed in other frontal lobe areas. Together, these findings reveal cingulate neurons that serve to adaptively drive competitive interactions and a putative process that could intermediate the social and economic behaviour of groups.

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