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

Abstract

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.

Interneuron functional diversity in the mouse accessory olfactory bulb

“…Future studies of AOB interneurons in vitro or in vivo including these simple intrinsic "fingerprinting" protocols will be able to compare the physiological profiles observed in each cell to those observed in this study. This approach supports the identification of novel physiological types or specific changes to established functionally-defined types that may occur in response to chemosensory experience (Cansler et al, 2017) and/or neuromodulation (Smith et al, 2009;Smith and Araneda, 2010;Leszkowicz et al, 2012). Taken as a whole, these results provide a major improvement in the available physiological data for AOB interneurons, and improve the foundation for studies of AOB circuit function.…”

“…2C, 3) may indicate an intermediate functional phenotype among IGCs. This hypothesis is partially supported by recent studies that showed IGC intrinsic physiology is altered over 2-8 hour time courses by recent chemosensory-driven activity (Cansler et al, 2017;Gao et al, 2017). It is an intriguing possibility that these other, more subtle, differences in IGC physiology may reflect their involvement in recent activation.…”

“…Ultimately, these studies clearly indicate that new tools will be necessary for researchers to selectively monitor and manipulate functional groups of AOB interneurons. Such tools will almost certainly involve the identification of new marker genes, but may also involve the utilization of tools that selectively label interneurons based on recent activation (Cansler et al, 2017;Gao et al, 2017).…”

“…IGCs are the most numerous and are currently the best-studied interneuron subtype in the AOB (Dudley and Moss, 1999;Jia et al, 1999;Araneda and Firestein, 2006;Smith et al, 2009;Taniguchi et al, 2012;Hu et al, 2016). Their known and hypothesized connections to experience-dependent plasticity make them a particularly compelling cell type to study (Brennan et al, 1990;Okutani et al, 1999;Cansler et al, 2017;Gao et al, 2017;Oboti et al, 2017). Despite the relatively strong set of inquiries into IGC function, there are many outstanding questions about IGCs' role in AOB information processing and experience-dependent chemosensory plasticity.…”

Neuronal Intrinsic Physiology Changes During Development of a Learned Behavior

“…It remains possible, however, that the intrinsic properties of participating neurons (passive membrane properties and composition of ion channels) also change during learning. Indeed, changes in ion channels have been observed in a variety of systems and there is a growing appreciation of the possibility of nonsynaptic forms of plasticity contributing to the learning process ( Debanne et al, 2003 ; Mozzachiodi and Byrne, 2010 ; Sehgal et al, 2013 ; Cansler et al, 2017 ). The present experiments explore changes in the intrinsic physiology of neurons in the zebra finch ( Taeniopygia guttata ) as juvenile birds progress through stages of vocal development.…”