Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour

Abstract

Juvenile social play behaviour is regarded as one of the earliest forms of non-mother directed social behaviour in rodents (1). An appealing aspect of juvenile social play behaviour is that it is sexually dimorphic, with males exhibiting higher levels of social play than females, making it an attractive model behaviour to understand both normal juvenile social development and sex differences in social behaviour in a nonreproductive context. It is also becoming clear that, although this sexually dimorphic behaviour is organised by neonatal steroid hormone exposure, the differentiation of social play can be also influenced by the early social environment, such as the amount of maternal care received. Investigations of social play are centered on why and how rats play, brain regions controlling play behaviour, sex differences, and how neurotransmitters and the social environment might influence the organisation of play behaviour. It will be interesting to understand how the social environment impinges on neurotransmitters to influence the steroid-receptor mediated organisation of juvenile social play behaviour. Why do rats play?There are several intriguing concepts with respect to why rats play. Juvenile play behaviour is considered to be rewarding because the opportunity to play can be used as an incentive for maze learning (2, 3) and juvenile rats develop conditioned place preferences for areas associated with play (4). Anticipation of play also elicits 50 kHz ultrasonic vocalisations (5), which are associated with positive affect (6). Indeed, it has been suggested that play is 'joyful' (7) and that some vocalisations during juvenile play might be akin to human laughter (8). Another possible function of play is to establish dominance in the group. After multiple play bouts, juveniles develop dominance hierarchies, which remain relatively stable over the juvenile period (9, 10), although play dominance does not always appear to predict dominance in adulthood (11). Play may also function to better prepare for adult behaviours, such as male sexual and aggressive behaviours (12), because play behaviour predicts adult aggressiveness in males (13). Preventing males from playing has lasting consequences on social (14-16), aggressive (16) and sexual behaviour (16,17). The effect of juvenile isolation on these behaviours appears mainly to be a result of deprivation of play because isolated animals provided with a brief daily period of play do not develop these deficits (16). Therefore, play may serve to prepare for more adaptive social behaviours in adulthood. How do rats play?Juvenile social play behaviour starts to form around 18 days, peaks during the peripubertal period (days 30-40) and wanes after puberty. Play is observed as bites, boxing ⁄ wrestling, pouncing and pinning. Pouncing, the act of jumping on or attacking the nape of a Juvenile social play behaviour is one of the earliest forms of non-mother directed social behaviour in rodents. Juvenile social play behaviour is sexually dimorphic, with males exhibiting ...

The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats

“…There is some precedent for this, in that neuronal survival is influenced by maternal stimulation during early postnatal development (Moore et al, 1992). In adolescence, males tend to exhibit greater levels of play behavior, an effect that is at least partially mediated by perinatal hormonal influences (reviewed in Auger & Oleson, 2009). There is evidence that play behavior during the juvenile and adolescent period affects neural reward circuits, and involves the neocortex (reviewed in Vanderschuren et al, 1997).…”

Convergence of Sex Differences and the Neuroimmune System in Autism Spectrum Disorder

“…In the rodent the BNST is also sexually dimorphic in both cell number and the size of afferent connections to other regions (46), as well as activation threshold to socially salient stimuli such olfaction and novelty (65) The BNST regulates innate fear responses and social play (66). Both the POA and the BNST have distinct reciprocal connections with the amygdala (67).…”

Epigenetic organization of brain sex differences and juvenile social play behavior

“…Specifically, juvenile male rats engage in social play behavior at a higher frequency than do juvenile female rats (Olioff and Stewart 1978). While numerous factors, such as neurotransmitters, and social experience, have been found to alter the development of juvenile social play behavior (Auger and Olesen 2009), sex differences in juvenile play behavior are mainly organized by neonatal testosterone exposure (Beatty et al, 1981; Meaney and Stewart 1981). More specifically, androgen receptors play a critical role in organizing sex difference in juvenile social play behavior (Casto et al, 2003; Meaney and Stewart 1981), with some data suggesting a potential role for estrogen receptors (Olesen et al, 2005).…”