Frontal neurons driving competitive behaviour and ecology of social groups

S. William Li, Omer Zeliger, Leah Strahs, Raymundo Báez-Mendoza, Lance M. Johnson, Aidan McDonald Wojciechowski and Ziv M. Williams ()
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S. William Li: Massachusetts General Hospital, Harvard Medical School
Omer Zeliger: Massachusetts General Hospital, Harvard Medical School
Leah Strahs: Massachusetts General Hospital, Harvard Medical School
Raymundo Báez-Mendoza: Massachusetts General Hospital, Harvard Medical School
Lance M. Johnson: Massachusetts General Hospital, Harvard Medical School
Aidan McDonald Wojciechowski: Massachusetts General Hospital, Harvard Medical School
Ziv M. Williams: Massachusetts General Hospital, Harvard Medical School

Nature, 2022, vol. 603, issue 7902, 661-666

Abstract: Abstract Competitive interactions have a vital role in the ecology of most animal species1–3 and powerfully influence the behaviour of groups4,5. To succeed, individuals must exert effort based on not only the resources available but also the social rank and behaviour of other group members2,6,7. 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.

Date: 2022
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DOI: 10.1038/s41586-021-04000-5

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