Aversive Learning Increases Release Probability of Olfactory Sensory Neurons

• Published in: Current biology 2020-01, Vol.30 (1), p.31-41.e3
• Main Authors: Bhattarai, Janardhan P., Schreck, Mary, Moberly, Andrew H., Luo, Wenqin, Ma, Minghong
• Format: Article
• Language: English
• Subjects: Animals; Conditioning, Operant; external tufted cells; Fear; fear learning; Female; GABAB receptor; glomeruli; Learning; Male; Mice; olfactory bulb; Olfactory Bulb - physiology; Olfactory Nerve - physiology; olfactory sensory neurons; optogenetics; paired-pulse ratio; release probability
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2019.11.006

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 light stimulation alone during fear retrieval. This is accompanied by an increase in OSN release probability and a reduction in GABAB 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. [Display omitted] •Monoglomerular activation paired with foot shock induces fear learning•Fear learning increases release probability of OSNs•Freezing time is positively correlated with release probability of OSNs•Fear learning causes reduction of presynaptic GABAB receptor expression in OSNs Bhattarai et al. show that pairing foot shock with optogenetic activation of a single glomerulus in the mouse olfactory bulb induces fear learning, which is accompanied by increased release probability of olfactory sensory neurons. This study highlights that the brain regulates peripheral sensory inputs based on predictive values.