Natural variations of adolescent neurogenesis and anxiety predict the hierarchical status of adult inbred mice.

Abstract

Hierarchy provides a survival advantage to social animals in challenging circumstances. In mice, social dominance is associated with trait anxiety which is regulated by adult hippocampal neurogenesis. Here, we test whether adolescent hippocampal neurogenesis may regulate social dominance behavior in adulthood. We observe that adolescent individuals with higher trait anxiety and lower levels of hippocampal neurogenesis prior to the formation of a new group become dominants, suggesting that baseline adolescent neurogenesis predicts hierarchical status. This phenotype persists beyond social hierarchy stabilization. Experimentally reducing neurogenesis prior to the stabilization of social hierarchy in group-housed adolescent males increases the probability of mice to become dominant and increases anxiety. Finally, when innate dominance is assessed in socially isolated and anxiety-matched animals, mice with impaired neurogenesis display a dominant status toward strangers. Together, these results indicate that adolescent neurogenesis predicts and regulates hierarchical and situational dominance behavior along with anxiety-related behavior. These results provide a framework to study the mechanisms underlying social hierarchy and the dysregulation of dominance behavior in psychiatric diseases related to anxiety.