Reliable Sex and Strain Discrimination in the Mouse Vomeronasal Organ and Accessory Olfactory Bulb

Abstract

Animals modulate their courtship and territorial behaviors in response to olfactory cues produced by other animals. In rodents, detecting these cues is the primary role of the accessory olfactory system (AOS). We sought to systematically investigate the natural stimulus coding logic and robustness in neurons of the first two stages of accessory olfactory processing, the vomeronasal organ (VNO) and accessory olfactory bulb (AOB). We show that firing rate responses of just a few well-chosen mouse VNO or AOB neurons can be used to reliably encode both sex and strain of other mice from cues contained in urine. Additionally, we show that this population code can generalize to new concentrations of stimuli and appears to represent stimulus identity in terms of diverging paths in coding space. Together, the results indicate that firing rate code on the temporal order of seconds is sufficient for accurate classification of pheromonal patterns at different concentrations and may be used by AOS neural circuitry to discriminate among naturally occurring urine stimuli.

Experience-Dependent Plasticity Drives Individual Differences in Pheromone-Sensing Neurons

“…This plasticity might therefore be a reflection of cell-survival or receptor-choice mechanisms that ensure balance in the expression of neuronal types and the ability of organisms to detect a wide variety of scents, in essence a long-term form of “decorrelation” (or “gain control” in the abundance of particular cell types) in sensory input. This proposed role is consistent with the decreased animal-to-animal variability of females compared to males (Figure 3F) given that females produce a substantially-larger number and intensity of vomeronasal cues than males (He et al 2008; Nodari et al 2008; Stowers et al 2002; Tolokh et al 2013). Altogether, the mechanism of plasticity remains unknown, and an important topic for future studies.…”

Integrated action of pheromone signals in promoting courtship behavior in male mice

“…The vomeronasal sensory neurons (VSNs) encode information about gender, reproductive status, genetic background and individual differences of animals of the same species, as well as that of heterospecifics (Halem et al, 1999; Holy et al, 2000; Boschat et al, 2002; Wyatt, 2003; Leinders-Zufall et al, 2004; Kimoto et al, 2005; Chamero et al, 2007; Kimoto et al, 2007; He et al, 2008; Haga et al, 2010; Papes et al, 2010; Isogai et al, 2011; Tolokh et al, 2013). The multitude of cues potentially provides snapshots of other animals and surrounding environments to influence reproductive behaviors.…”

<em>Ex Vivo</em> Preparations of the Intact Vomeronasal Organ and Accessory Olfactory Bulb

“…The VNO-AOB ex vivo preparation described in this protocol is a useful alternative to anesthetized in vivo [5][6][7] and acute live slice 17 experiments of AOB function. Unlike acute AOB slice experiments, which also expose circuit elements for electrophysiological and optical recordings, this preparation retains all sensory afferents and intra-AOB connections.…”

“…Several studies have probed AOB neural responses to sources of AOS odors (such as mouse urine) in vivo using anesthetized mice [5][6][7] or freely-exploring animals 8 . The heroic anesthetized in vivo studies involved (a) tracheotomies to ensure deep anesthesia and prevent the aspiration of liquid stimuli [5][6][7] , (b) stimulation of the sympathetic cervical ganglion 6 or direct cannulation of the vomeronasal organ 5,7 to introduce nonvolatile odors and (c) craniotomies with or without frontal lobe ablations to allow electrode advancement into the AOB 6 . Awake/behaving studies [8][9][10] involved surgical implantation of a microdrive.…”