Juvenile social play and the development of socio-cognitive skills in male rats: Does everyone benefit?

Social play during early life is important for brain and behavioral development. In rats, rough-and-tumble play (RTP)-their main form of social play-enhances socio-cognitive flexibility and refines the medial prefrontal cortex (mPFC) through dendritic pruning. While restricting RTP impairs these outcomes, it remains unclear whether all individuals benefit equally when play opportunities are abundant. To test this, we reared 54 male rats in large social groups from weaning to adulthood, ensuring rich RTP experiences. Despite these conditions, 20.4% later escalated playful encounters into aggression, indicating reduced social competence. These "incompetent" rats did not differ in play frequency or defensive tactics, suggesting similar juvenile RTP exposure. However, their mPFC layer III pyramidal neurons showed larger dendritic arbors and greater distal spine density, consistent with reduced pruning. These neural and behavioral traits parallel those in play-deprived rats, indicating that some individuals fail to gain RTP's socio-cognitive benefits. This variation mirrors patterns in humans, where not all children benefit equally from play-based interventions, underscoring the need to identify early-life predictors and neural mechanisms underlying individual differences.