Sexual experience and testosterone during adolescence alter adult neuronal morphology and behavior

Steroid hormones released immediately before and after birth provoke sexual differentiation of neural circuits. Further, steroid hormones secreted during adolescence also exert long lasting effects on the nervous system. Hormones secreted during development may act through two distinct pathways: (1) hormones can directly affect neuron and synapse elimination and (2) endocrine changes in the nervous system may occur secondary to changes in social behaviors. Therefore, a critical period for organization of the nervous system by steroid hormones during adolescence may also be a sensitive period for the effects of social experience. The overall goal of this experiment was to determine whether the opportunity to mate with a sexually receptive female during this adolescent critical period would have enduring effects on behavior and neuronal morphology into adulthood. A second question was to determine the extent to which testosterone mediated the effects of these social interactions on adult outcomes. Compared to sexually inexperienced hamsters and those that experienced sex for the first time in adulthood, hamsters that experienced adolescent sexual experience displayed increased anxiety- and depressive-like behavioral responses. Adolescent sexual experiences decreased the complexity and length of dendrites on prefrontal cortical neurons and increased the expression of the pro-inflammatory cytokine interleukin 1β (IL-1β) in the PFC. In a second experiment, administration of testosterone during the adolescent period largely recapitulated the effects of adolescent sexual experience. These data support the overall hypothesis that a sensitive period extends into adolescence and that salient social stimuli during this time can significantly and persistently alter adult phenotype.