Abstract

Play fighting is a highly rewarding behavior that helps individuals to develop social skills. Early-life stress has been shown to alter play fighting in rats and hamsters as well as to increase aggressive behaviors at adulthood. However, it is not known whether individual differences in stress-induced play fighting are related to differential developmental trajectories towards adult aggression. To address this question, we used a rat model of peripubertal stress (PPS)-induced psychopathology that involves increased aggression at adulthood. We report that, indeed, PPS leads to enhanced play fighting at adolescence. Using a stratification approach, we identify individuals with heightened levels of play fighting as the ones that show abnormal forms of aggression at adulthood. These animals showed as well a rapid habituation of their corticosterone responsiveness to repeated stressor exposure at peripuberty. They also showed a striking increase in mitochondrial function in the amygdala—but not nucleus accumbens—when tested ex vivo. Conversely, low, but not high players, displayed increased expression of the CB1 cannabinoid receptor in the nucleus accumbens shell. Our results highlight adolescence as a potential critical period in which aberrant play fighting is linked to the emergence of adult aggression. They also point at brain energy metabolism during adolescence as a possible target to prevent adult aggression.

Highlights

  • Play fighting, called social or rough-and-tumble play, is a common form of play observed in many species, such as mammals and birds

  • Exposure to peripubertal stress (PPS) leads to enhanced play fighting First, we asked whether exposure to PPS modifies play behavior during adolescence, in an experiment performed at P45 (Fig. 1a)

  • We found an increase in cannabinoid receptor 1 (CB1) gene expression in the nucleus accumbens (NAc) shell of peripubertally stressed rats that show low, but not in those with high play fighting levels

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Summary

Introduction

Called social or rough-and-tumble play, is a common form of play observed in many species, such as mammals and birds It is typically most abundant from weaning until puberty, with a peak at adolescence (32 to 40 days of age in rodents) and gradually declines with the approach of sexual maturity[1]. Corticosterone administration at the exact schedule as our peripubertal stress (PPS) model mimicked alterations in the social domain and led as well to enhanced play fighting[17]. It is not known whether PPS affects play behavior and, in this study, we aimed to investigate the consequences of PPS on play fighting and examined neurobiological correlates

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