Signal Detection and Coding in the Accessory Olfactory System

Abstract

In many mammalian species, the accessory olfactory system plays a central role in guiding behavioral and physiological responses to social and reproductive interactions. Because of its relatively compact structure and its direct access to amygdalar and hypothalamic nuclei, the accessory olfactory pathway provides an ideal system to study sensory control of complex mammalian behavior. During the last several years, many studies employing molecular, behavioral, and physiological approaches have significantly expanded and enhanced our understanding of this system. The purpose of the current review is to integrate older and newer studies to present an updated and comprehensive picture of vomeronasal signaling and coding with an emphasis on early accessory olfactory system processing stages. These include vomeronasal sensory neurons in the vomeronasal organ, and the circuitry of the accessory olfactory bulb. Because the overwhelming majority of studies on accessory olfactory system function employ rodents, this review is largely focused on this phylogenetic order, and on mice in particular. Taken together, the emerging view from both older literature and more recent studies is that the molecular, cellular, and circuit properties of chemosensory signaling along the accessory olfactory pathway are in many ways unique. Yet, it has also become evident that, like the main olfactory system, the accessory olfactory system also has the capacity for adaptive learning, experience, and state-dependent plasticity. In addition to describing what is currently known about accessory olfactory system function and physiology, we highlight what we believe are important gaps in our knowledge, which thus define exciting directions for future investigation.

Synchronous Infra-Slow Oscillations Organize Ensembles of Accessory Olfactory Bulb Projection Neurons into Distinct Microcircuits

“…5C ii ). Within the volume of the AOB, which harbors approximately 7,000 AMCs (Mohrhardt et al, 2018), de facto numbers must be considerably higher. While most microcircuits encompass a '2-dimensional' area of <10 4 μm 2 (data not shown), both pairwise AMC distance within a circuit and its rostro-caudal dimension appear homogeneously distributed across the extent of the AOB (Fig.…”

“…In rodents, the accessory olfactory system controls conspecific chemical communication during social interactions (Dulac and Torello, 2003;Brennan and Zufall, 2006;Tirindelli et al, 2009;Mohrhardt et al, 2018). Sensory neurons in the vomeronasal organ detect behaviorally relevant chemosignals and relay this information to the accessory olfactory bulb (AOB).…”

Paradoxically sparse chemosensory tuning in broadly-integrating external granule cells in the mouse accessory olfactory bulb

“…Stimulation-evoked ∆F/F typically reached a peak within the first 2 seconds of an 8 s VNO stimulus delivery, and displayed slow decay kinetics (decay time 8 -12 s after the peak). Because the decay kinetics of GCaMP6f (Chen et al, 2013) are much faster than previous measurements of spike frequency decay, the slowness of GCaMP6f offset times likely reflects the slow cessation of spiking activity in AOB MCs (Luo et al, 2003;Wagner et al, 2006;Hendrickson et al, 2008;Ben-Shaul et al, 2010;Meeks et al, 2010;Mohrhardt et al, 2018). Of the 266 MCs we studied, 242 (91.0%) responded to at least 1 of the naturalistic stimuli, 199 (74.8%) responded to at least 1 monomolecular sulfated steroid ligand, and 125 (47.0%) were responsive to at least 2 sulfated steroids ( Fig.…”

“…AOB MCs activity is shaped at multiple levels by inhibitory interneurons. The first stage of MC inhibition occurs in the glomerular layer, where AOB JGCs reside and release GABA onto MC dendrites and VSN presynaptic terminals (Mohrhardt et al, 2018). Because there have not been any systematic recordings of AOB interneuron tuning, we first sought to measure tuning in a general population of AOB GABAergic interneurons.…”

Gαi2+ vomeronasal neurons govern the initial outcome of an acute social competition

“…The mechanisms that may mediate social dominance are likely to involve the sensing of pheromones, which in mammals largely depends on the vomeronasal organ (VNO), a chemosensory organ with a crucial role in mediating different innate behaviors [4][5][6] including intermale aggression 7 . Some studies postulate that aggression is needed for the display of dominance behaviors 8,9 .…”