Puberty: a finishing school for male social behavior

The classical view of steroid-dependent organization of brain and behavior holds that gonadal steroid hormones, acting during an early critical period of development, cause permanent structural changes in neural circuits that determine behavioral responses to hormones in adulthood. This classical view has been modified to incorporate evidence that organizational effects of steroids can occur outside of the established perinatal critical period and that multiple critical periods may exist during development. Experiments in this laboratory indicate that steroid-dependent organization of neural circuits underlying male social behaviors occurs during puberty. This work shows that adult-typical reproductive and flank marking behaviors cannot be activated by gonadal steroids in male Syrian hamsters prior to puberty, suggesting that developmentally timed processes during puberty render the nervous system responsive to activating effects of gonadal steroids in adulthood. Additional experiments demonstrate that the presence or absence of gonadal hormones during puberty is a major factor in the ability of steroids to activate reproductive and flank marking behavior in adult male hamsters and in androgen receptor expression within the neural circuit underlying these behaviors. Thus, gonadal hormones during puberty appear to exert long-lasting changes in neural circuits that are responsible for the programming of activational responses to steroids later in adulthood. A two-stage model for maturation of male social behaviors is proposed: a perinatal critical period for sexual differentiation of neural circuits, followed by the pubertal period, during which gonadal steroids further organize the circuits to enhance behavioral responsiveness to hormones in adulthood. Whether puberty is a critical period for the proposed second wave of steroid-dependent organization of behavioral circuits remains to be determined.