Social play is critical for the development of prefrontal inhibitory synapses and cognitive flexibility in rats

Sensory driven activity during early life is critical for setting up the proper connectivity of the sensory cortices. Here we ask if social play behavior, a particular form of social interaction that is highly abundant during post-weaning development, is equally important for setting up connections in the developing prefrontal cortex (PFC). Young rats were deprived from social play with peers for 3 weeks during the period in life when social play behavior normally peaks (P21-42; SPD rats), followed by resocialization until adulthood. We recorded synaptic currents in L5 cells in slices from medial PFC of adult SPD and control rats and observed that inhibitory synaptic currents were reduced in SPD slices, while excitatory synaptic currents were unaffected. This was associated with a decrease in perisomatic inhibitory synapses from parvalbumin-positive GABAergic cells. In parallel experiments, adult SPD rats achieved more reversals in a probabilistic reversal learning task (PRL), which depends on the integrity of the PFC. They appeared to use a different cognitive strategy than controls. One hour of intense play during SPD did not prevent the decrease in inhibitory synaptic inputs and had only a limited effect on behavioral outcomes in the PRL. Our data demonstrate the importance of unrestricted social play for the development of inhibitory synapses in the PFC and cognitive skills in adulthood.