Experience-dependent plasticity in accessory olfactory bulb interneurons following male-male social interaction

Abstract

Conflict of interestThe authors declare no competing financial interests.\n\nAcknowledgementsWe thank Jennifer Torres, Salma Ferdous, and Natasha Browder for technical support. We thank Kimberly Huber and Todd Roberts for critical feedback on the manuscript. This work was funded by the National Institute on Deafness and Other Communication Disorders and the National Institute on Drug Abuse of the National Institutes of Health under award numbers R00DC011780, R01DC015784 (JPM), and T32DA007290 (HLC). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Partial support was also provided by the National Science Foundation (Grant IOS-1451034; JPM, co-PI).\n\nChemosensory 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 targeted electrophysiological studies of AOB inhibitory internal granule cells (IGCs), many of which upregulate the immediate-early gene Arc after male-male social experience. Following the resident-intruder paradigm, 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 is 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. 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.\n\nSignificance StatementThe accessory olfactory bulb (AOB) is a site of experience-dependent plasticity between excitatory mitral cells (MCs) and inhibitory internal granule cells (IGCs), but the physiological mechanisms and behavioral conditions driving this plasticity remain unclear. Here, we report studies of AOB neuronal plasticity following male-male social chemosensory encounters. We show that the plasticity-associated immediate-early gene Arc is selectively expressed in IGCs from resident males following the resident-intruder assay. Following behavior, Arc-expressing IGCs are more strongly excited by sensory input stimulation and MC activation is suppressed. Arc-expressing IGCs do not show increased excitatory synaptic drive, but instead show increased intrinsic excitability. These data indicate that MC-IGC plasticity is induced after male-male social chemosensory encounters, resulting in MC suppression by Arc-expressing IGCs.