Investigating Experience-Dependent Plasticity in the Accessory Olfactory Bulb

Chemosensory information processing in the mouse accessory olfactory system (AOS) guides the expression of social behavior. After salient chemosensory encounters, the accessory olfactory bulb (AOB) experiences changes in the balance of excitation and inhibition at reciprocal synapses between mitral cells (MCs) and local interneurons. The mechanisms underlying these changes remain controversial. Moreover, it remains unclear whether MC-interneuron plasticity is unique to specific behaviors, such as mating, or whether it is a more general feature of the AOB circuit. Here, we describe a population of AOB internal granule cells (IGCs) that upregulate expression of the immediate early gene Arc following the resident-intruder paradigm in an AOS-dependent manner. Targeted electrophysiological studies revealed that Arc-expressing IGCs in acute AOB slices from resident males displayed stronger excitation than non-expressing neighbors when sensory inputs are stimulated. The increased excitability of Arc-expressing IGCs was not correlated with changes in the strength or number of excitatory synapses with MCs, but was instead associated with increased intrinsic excitability and decreased HCN channel-mediated IH currents. Consistent with increased inhibition by IGCs, MCs responded to sensory input stimulation with decreased depolarization and spiking following resident-intruder encounters. Different populations of IGCs are activated following exposure to males and females, suggesting they are activated in an input-specific fashion. We also describe multiple behavioral paradigms that have been designed to assay social recognition following resident-intruder behavior in conjunction with in vivo manipulation of Arc-expressing IGCs. Together, these results reveal that non-mating behaviors drive AOB inhibitory plasticity, and indicate that increased MC inhibition involves intrinsic excitability changes in Arc-expressing interneurons.