The organizational effects of pubertal testosterone on the maturation of adult social cognition and social proficiency

Maturation of social cognition and a gain in social proficiency are universal aspects of adolescent development that prepare an individual for adulthood. Social cognition involves the perception and interpretation of social cues, followed by the generation of a behavioral response. Social proficiency is acquired through the ability to make behavioral adaptations as one learns from social experience. The pubertal rise in testosterone secretion results in both activation and organization of the neural circuits underlying adult male social behaviors, including sexual behavior, which may contribute to the developmental changes in social cognition and gain in sexual proficiency. To assess the contribution of pubertal testosterone to the maturation of adult social behavior, we utilize the NoT P/T P experimental animal model. In this model, male Syrian hamsters are deprived of testosterone during puberty (defined as NoT P) or for an equivalent amount of time during adulthood (defined as T P) and then given testosterone replacement in adulthood for two weeks before behavior testing. If NoT P and T P males differ in behavior, we infer that the difference is due to organizational effects of pubertal testosterone. If NoT P and T P males show similar behavior, then we infer that the adolescent maturation of that behavior is due to hormone-independent or activational actions. We first tested the hypothesis that the adolescent acquisition of social reward does not depend on organizational effects of pubertal testosterone. We found that both NoT P and T P males show a CPP for vaginal secretions and a receptive female, indicating that the adolescent maturation of social reward is independent of pubertal testosterone. Second, we tested the hypothesis the adolescent gain in sexual proficiency does depend on organizational effects of testosterone. When sexual experience is equated for both NoT P and T P males, NoT P males do not inhibit maladaptive behaviors with sexual experience, whereas T P males do. These data suggest that testosterone during puberty programs the ability to adapt behaviors (via inhibition) in a social context-dependent manner. Third, we tested whether pubertal testosterone organizes the adolescent gain in sexual proficiency through the regulation of the transcription factor DeltaFosB in the infralimbic medial prefrontal cortex (IL). We found that ▵FosB was induced in the IL after sexual experience in T P, but not NoT P, males. Furthermore, over-expression of ▵FosB in the IL of NoT P males prior to sexual behavior testing was sufficient to reverse the deficits in behavioral inhibition found in NoT P males. Taken together, these data provide evidence that social reward develops independently of pubertal testosterone, whereas the ability to inhibit inappropriate behavior is organized by pubertal testosterone through the regulation of ▵FosB in the IL.