Social separation stress accelerates vocal motor circuit maturation and impairs song learning in zebra finches (Taeniopygia guttata)

Social interactions shape vocal learning, and adverse experiences can impair development of brain regions involved in learning, memory, and cognition. Whether early life social stress shapes motor circuits is less well understood. Here, we used zebra finches (Taeniopygia guttata) to investigate whether social experience modulates vocal learning by regulating expression of perineuronal nets (PNNs), extracellular matrix structures that regulate neural plasticity, in motor circuitry specialized for singing. We show that repeated, short bouts of familial separation during the critical period for vocal learning accelerates PNN formation in the song motor circuit. Moreover, song learning is impaired in birds that were intermittently separated, consistent with PNN-mediated plasticity restriction. Disruption of familial interactions did not drive persistent changes in corticosterone or testosterone, hormones associated with stress and song stabilization, respectively. Our findings demonstrate that intermittent social perturbations can induce structural plasticity in motor circuits, with long-lasting behavioral consequences, thus highlighting the impact of early life social stress on functional organization of vocal motor circuitry. Repeated, short bouts of social separation during the critical period drives premature maturation of perineuronal nets in the vocal motor pathway of zebra finches and impairs vocal imitation, highlighting the impact of early life social stress on the functional organization of vocal motor circuitry.