Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels

The early social environment has a profound impact on developmental trajectories. Although an impoverished early environment can undermine the acquisition of appropriate social skills, the specific role played by the different components of an individual's early environment in building social competencies has not been fully elucidated. Here we setup an asynchronous communal nesting paradigm in mice to disentangle the influence of maternal care and early peer interactions on adult social behavior and neural systems reportedly involved in the regulation of social interactions. The asynchronous communal nesting consists of three mothers giving birth three days apart, generating three groups of pups - the Old, the Middle and the Young - all raised in a single nest from birth to weaning. We scored the amount of maternal and peer interactions received by these mice and by a fourth group reared under standard conditions. At adulthood, the four experimental groups have been investigated for social behavior in a social interaction test, i.e. facing an unfamiliar conspecific during five 20-min daily encounters, and for oxytocin receptor and brain derived neurotrophic factor (BDNF) levels. Results show that only individuals exposed to high levels of both maternal and peer interactions demonstrated elaborate adult agonistic competencies, i.e. the ability to promptly display a social status, and high BDNF levels in the hippocampus, frontal cortex and hypothalamus. By contrast, only individuals exposed to high levels of peer interactions showed enhanced adult affiliative behavior and enhanced oxytocin receptor levels in selected nuclei of the amygdala. Overall these findings indicate that early interactions with mother and peers independently shape specific facets of adult social behavior and neural systems involved in social interaction.