Experience-Dependent Plasticity in Accessory Olfactory Bulb Interneurons following Male-Male Social Interaction

• Published in: The Journal of neuroscience 2017-07, Vol.37 (30), p.7240-7252
• Main Authors: Cansler, Hillary L, Maksimova, Marina A, Meeks, Julian P
• Format: Article
• Language: English
• Subjects: Accessory olfactory bulb; Aggression - physiology; Animals; Behavior, Animal - physiology; Chemoreception; Cytoskeletal Proteins - metabolism; Data processing; Depolarization; Excitability; Excitation; Granule cells; Information processing; Inhibition; Interneurons; Interneurons - physiology; Interpersonal Relations; Learning - physiology; Male; Males; Mice, Inbred C57BL; Mitral cells; Nerve Net - physiology; Nerve Tissue Proteins - metabolism; Neuronal Plasticity - physiology; Olfactory bulb; Olfactory Bulb - physiology; Olfactory system; Plastic properties; Plasticity; Smell; Social Behavior; Social factors; Synapses; Synaptic strength; Synaptic Transmission - physiology
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.1031-17.2017

Chemosensory information processing in the mouse accessory olfactory system 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 after male-male social experience. Following the resident-intruder paradigm, -expressing IGCs in acute AOB slices from resident males displayed stronger excitation than nonexpressing neighbors when sensory inputs were stimulated. The increased excitability of -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 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 nonmating behaviors drive AOB inhibitory plasticity and indicate that increased MC inhibition involves intrinsic excitability changes in -expressing interneurons. The 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 is selectively expressed in IGCs from resident males following the resident-intruder assay. After behavior, -expressing IGCs are more strongly excited by sensory input stimulation and MC activation is suppressed. -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 enhanced MC suppression by -expressing IGCs.