In group-living animals, chronic juvenile social isolation stress (SIS) can profoundly affect behavior and neuroendocrine regulation. However, its impact on social behavior in avian species, particularly regarding sex-specific neural circuit differences, remains underexplored. This study focused on zebra finches, a species known for its social clustering and cognitive abilities, to elucidate these influences. Results indicated that SIS significantly increased plasma corticosterone levels in females but not in males, suggesting a heightened stress response and susceptibility in females. Additionally, SIS disrupted sociality and flocking behavior in both sexes, with more severe impairments in social recognition observed in females. Mesotocin (MT) levels in the lateral septum of both sexes and in the ventromedial hypothalamus of females were found to mediate the SIS effect, while vasotocin (VT) levels within the social behavior network remained unchanged. Pharmacological interventions confirmed the critical role of MT in reversing SIS-induced impairments in sociality, flocking behavior, and social recognition, particularly in females. These findings highlight unique nucleus- and sex-dependent variations in MT and VT regulation, providing novel insights into the mechanisms governing avian social behavior. This study advances our understanding of the independent evolutionary pathways of neural circuits and neuroendocrine systems that modulate social behaviors across different taxonomic groups.
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