Sexually Dimorphic Synaptic Organization of the Medial Amygdala

The medial amygdala is important in social behaviors, many of which differ between males and females. The posterodorsal subnucleus of the medial amygdala (MeApd) is particularly sensitive to gonadal steroid hormones and is a likely site for gonadal hormone regulation of sexually dimorphic social behavior. Here we show that the synaptic organization of the MeApd in the rat is sexually dimorphic and lateralized before puberty. With the use of whole-cell voltage-clamp recording and quantitative electron microscopy, we found that, specifically in the left hemisphere, prepubertal males have approximately 80% more excitatory synapses per MeApd neuron than females. In the left but not the right MeApd, miniature EPSC (mEPSC) frequency was significantly greater in males than in females; mEPSC amplitude was not sexually dimorphic. Paired-pulse facilitation of EPSCs, an index of release probability, also was not sexually dimorphic, suggesting that greater mEPSC frequency is caused by a difference in excitatory synapse number. Electron microscopy confirmed that the asymmetric synapse-to-neuron ratio and the total asymmetric synapse number were significantly greater in the left MeApd of males than of females. In contrast to results for excitatory synapses, we found no evidence of sexual dimorphism or laterality in inhibitory synapses. Neither the frequency nor the amplitude of mIPSCs was sexually dimorphic or lateralized. Likewise, the number of symmetric synapses measured with electron microscopy was not sexually dimorphic. These findings show that the excitatory synaptic organization of the left MeApd is sexually differentiated before puberty, which could provide a sexually dimorphic neural substrate for the effects of hormones on adult social behavior.