Effects of prepubertal gonadectomy on a male-typical behavior and excitatory synaptic transmission in the amygdala

Mammalian puberty entails the emergence of behaviors such as courtship, coitus, and territorial aggressiveness. In adult rodents, the medial amygdala (MeA) is an important site for gonadal steroid hormone regulation of social behaviors and is sensitive to changes in the level of gonadal steroids. Here we show that prepubertal gonadectomy of male rats reduces the expression of a sexually dimorphic behavior, juvenile rough-and-tumble play, as well as the level of excitatory synaptic transmission assayed in adulthood. Behavioral observations in juveniles showed that gonadectomy reduced the initiation of playful attacks, particularly between postnatal days 31-35. Whole-cell voltage clamp recordings made in slices from adults showed that gonadectomy also reduced the frequency of miniature excitatory postsynaptic currents (mEPSCs) in MeA neurons without affecting paired pulse facilitation, an index of vesicle release probability. As mEPSC frequency can reflect the number of excitatory synapses per neuron, we also compared the dendritic morphology of Lucifer Yellow filled neurons from intact and gonadectomized adults. This showed that gonadectomy significantly reduced the density of dendritic spines without affecting overall dendritic length or branching of MeA neurons, which is consistent with a gonadectomy-induced reduction in the number of excitatory synapses. These findings suggest that peripubertal androgens activate rough-and-tumble play and promote the maintenance and/or development of new excitatory synapses in the MeA.