Aversive Learning Increases Release Probability of Olfactory Sensory Neurons

Abstract

Predicting danger from previously associated sensory stimuli is essential for survival.Contributions from altered peripheral sensory inputs are implicated in this process, but the underlying mechanisms remain elusive. Here we use the mammalian olfactory system to investigate such mechanisms. Primary olfactory sensory neurons (OSNs) project their axons directly to the olfactory bulb (OB) glomeruli where their synaptic release is subject to local and cortical influence and neuromodulation. Pairing optogenetic activation of a single glomerulus with foot shock in mice induces freezing to the light stimulation alone during fear retrieval. This is accompanied by enhanced OSN release probability and reduced GABA B receptor expression in the conditioned glomerulus. Furthermore, freezing time is positively correlated with the release probability of OSNs in fear conditioned mice. These results suggest that aversive learning increases peripheral olfactory inputs at the first synapse, which may contribute to the behavioral outcome.

Acquisition of innate odor preference depends on spontaneous and experiential activities during critical period

“…In contrast, spontaneous activities, not odor exposure per se, are required for the convergence of axons (Yu et al, 2004). Past studies have shown that pairing an odor with an aversive unconditioned stimulus can lead to enlarged glomeruli corresponding to the cognate receptor, enhanced transmitter release at the OSN termini, and heightened sensitivity to odor stimulation in the interneuron population (Bhattarai et al, 2020;Dias and Ressler, 2014;Jones et al, 2008;Kass and McGann, 2017). Early exposure of odorants can also lead to increased expression of odorant receptor genes and enlarged olfactory glomeruli (Cadiou et al, 2014;Ibarra-Soria et al, 2017;Todrank et al, 2011).…”

A neural circuit basis for binasal input-enhanced chemosensory avoidance

“…In the mouse, a couple of recent works reported brain state-dependent modulation of retinal ganglion cell output in the superior colliculus (Liang et al, 2020; Schröder et al, 2020). Similarly, associative learning influences OSN synaptic release in the mouse olfactory bulb (Bhattarai et al, 2020). Candidate mechanisms proposed include top-down or local circuit-mediated presynaptic modulation at the axonal terminals (Bhattarai et al, 2020), or retinopedal projections-mediated top-down influence directly at the retina (Liang et al, 2020; Schröder et al, 2020).…”

“…Similarly, associative learning influences OSN synaptic release in the mouse olfactory bulb (Bhattarai et al, 2020). Candidate mechanisms proposed include top-down or local circuit-mediated presynaptic modulation at the axonal terminals (Bhattarai et al, 2020), or retinopedal projections-mediated top-down influence directly at the retina (Liang et al, 2020; Schröder et al, 2020). These hypotheses have the necessary anatomical substrates to support in the mouse.…”