Adolescent brain maturation is necessary for adult-typical mesocorticolimbic responses to a rewarding social cue.

The interpretation of social cues must change during adolescence in order to promote appropriate social interactions in adulthood. For example, adult, but not juvenile, male Syrian hamsters find female pheromones contained in vaginal sections (VS) rewarding, and only adult hamsters engage in sexual behavior with a receptive female. We previously demonstrated that the rewarding value of VS is both testosterone- and dopamine-dependent. Additionally, VS induces Fos expression throughout the mesocorticolimbic circuit in adult but not juvenile hamsters. In this study, we determined whether or not treatment of juvenile male hamsters with testosterone is sufficient to promote adult-like neural responses to VS. Juvenile and adult male hamsters were gonadectomized and given empty or testosterone-filled subcutaneous capsules for 1 week. Hamsters were then exposed to either clean or VS-containing mineral oil on their nares, and brains were collected 1 h later for immunohistochemistry to visualize Fos and tyrosine hydroxylase immunoreactive cells. Testosterone treatment failed to promote adult-typical patterns of Fos expression in juvenile hamsters; indeed, in some brain regions, juveniles exposed to VS expressed less Fos compared to age-matched controls while, as expected, adults exposed to VS expressed greater Fos compared to age-matched controls. Age-related changes in tyrosine hydroxylase expression were also observed. These data indicate that testosterone cannot activate the adult-typical pattern of Fos expression in response to female social cues in prepubertal males, and that additional neural maturation during adolescence is required for adult-typical mesocorticolimbic responses to female pheromones.