Social experience is associated with a differential role of aromatase neurons in sexual behavior and territorial aggression in male mice

Abstract

Aromatase (Aro+) neurons located in the Bed Nucleus of the Stria Terminalis (BNST) are crucial for the display of both sexual behavior and territorial aggression in naive male mice. The postero-dorsal part of the Medial Amygdala (MeApd) also contains Aro + neurons that are required for territorial aggression, but these neurons seem dispensable for the display of sexual behavior in naive animals. However, little is known about how Aro + neuron circuitry is influenced by social experience. Using a combination of chemogenetics, activity mapping and retrograde viral tracing, we show that social experience modulates Aro + neurons during sexual behavior and territorial aggression. Chemogenetic inhibition of BNST Aro + neurons in socially experienced male mice revealed that these neurons are required for territorial aggression, but not for sexual behavior. Behavior testing in experienced animals showed a specific increase in activation in the vomeronasal organ (VNO) and the Medial Amygdala (MeA) after sexual behavior but not territorial aggression, assessed by Egr1 expression. We also observed an increase of Egr1 cells in the medial Preoptic Area (mPOA), a brain region implicated in the display of sexual behavior. Combined retrograde viral tracing and Egr1 immunodetection showed that a subset of the activated cells in the MeA are Aro + neurons projecting to the mPOA. These results highlight that social experience induces a differential neural activity in the circuitry controlling sexual behavior and aggression, which include MeA Aro + neurons projecting to the mPOA.