Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA.
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, USA.
Nature. 2022 Mar;603(7902):661-666. doi: 10.1038/s41586-021-04000-5. Epub 2022 Mar 16.
Competitive interactions have a vital role in the ecology of most animal species and powerfully influence the behaviour of groups. To succeed, individuals must exert effort based on not only the resources available but also the social rank and behaviour of other group members. 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.
竞争相互作用在大多数动物物种的生态学中起着至关重要的作用,并有力地影响着群体的行为。为了成功,个体必须根据可用资源以及其他群体成员的社会等级和行为来付出努力。然而,精确驱动竞争相互作用或社会群体行为的单细胞机制仍知之甚少。在这里,我们开发了一种自然群体范式,在这个范式中,大量的老鼠竞争觅食,而我们则通过无线方式跟踪数千个独特相互作用中的神经元活动。通过跟踪群体的集体行为,我们发现前扣带皮层中的神经元能够自适应地代表动物相对于其他动物的社会等级。尽管社会等级与行为密切相关,但这些细胞可以从竞争行为中辨别出老鼠的相对等级,并整合有关可用资源、环境和老鼠过去成功的信息,以影响它们的决策。使用多类模型,我们展示了这些神经元如何跟踪群体中的其他个体,并准确预测即将到来的成功。使用神经调节技术,我们还展示了神经元如何有条件地影响竞争努力——仅当动物对其群体同伴更占优势时才会增加它们的努力,而当它们处于劣势时则会减少努力——这种影响在其他额叶区域是观察不到的。总之,这些发现揭示了前扣带皮层中的神经元,它们可以自适应地驱动竞争相互作用,以及一个可能的过程,该过程可以调节群体的社会和经济行为。