Specialized and experience-dependent neural dynamics in the medial amygdala and bed nucleus of stria terminalis upon social and sexual olfactory and tactile cues

Abstract

The medial amygdala (MeApd) and bed nucleus of the stria terminalis (BNST) are central components of the social behavior network. However, their real-time activity during social and sexual interactions, and their respective contributions to processing olfactory and tactile cues, remain unclear. Here, we used simultaneous dual site fiber photometry to record GCaMP6s signals from the MeApd and BNST in freely behaving male rats during social interaction, copulation, sexual exhaustion, and vaginal occlusion tests. Introduction of a conspecific increased activity in both regions, but the response profiles differed by social context and experience. The MeApd responded robustly to male and female conspecifics, with larger responses to males, whereas BNST activity increased reliably upon female introduction only after sexual experience. During olfactory investigation of a male conspecific, MeApd activity differentiated sniffing of anterior and posterior body regions, while BNST activity showed no comparable spatial selectivity. Neither region showed robust event-aligned responses during sniffing of receptive females. Tactile stimulation during copulation elicited strong calcium responses in both regions. Mounts, intromissions, and ejaculations each triggered significant activity, with ejaculation producing the largest responses. MeApd responses differentiated ejaculation from mounting in sexually naive animals, whereas distinctions in BNST responses emerged primarily after sexual experience. Moreover, responses to intromissions and ejaculations persisted during the final ejaculatory series preceding sexual exhaustion, while responses to mounts were eliminated when vaginal penetration was prevented. Together, these findings identify specialized yet parallel activity dynamics within the MeApd-BNST network. MeApd activity preferentially tracks socially relevant olfactory investigation and the intensity of copulatory sensory feedback, whereas BNST recruitment during sexual behavior is more strongly shaped by sexual experience.