Context-dependent inversion of the response in a single sensory neuron type reverses olfactory preference behavior

Abstract

The valence and salience of individual odorants are modulated by an animal’s innate preferences, learned associations, and internal state, as well as by the context of odorant presentation. The mechanisms underlying context-dependent flexibility in odor valence are not fully understood. Here we show that the behavioral response of C. elegans to bacterially-produced medium-chain alcohols switches from attraction to avoidance when presented in the background of a subset of additional attractive chemicals. This context-dependent reversal of odorant preference is driven by cell-autonomous inversion of the response to alcohols in the single AWC olfactory neuron pair. We find that while medium-chain alcohols inhibit the AWC olfactory neurons to drive attraction, these alcohols instead activate AWC to promote avoidance when presented in the background of a second AWC-sensed odorant. We show that these opposing responses are driven via engagement of different odorant-directed signal transduction pathways within AWC. Our results indicate that context-dependent recruitment of alternative intracellular signaling pathways within a single sensory neuron type conveys opposite hedonic valences, thereby providing a robust mechanism for odorant encoding and discrimination at the periphery.

Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality

“…Similar responses have also been observed in the ORNs of aquatic organisms, including lobster ( Bobkov et al, 2012 ), where a subpopulation of lobster ORNs has been shown to rhythmically burst in a fashion essential for determining the edges of a turbulent plume during odor tracking ( Michaelis et al, 2020 ). Recent results in Caenorhabditis elegans show that hedonic changes in olfactory context can change the responses of an ORN ( Khan et al, 2021 ). However, to our knowledge, our results provide the first evidence that ORNs can generate a well-defined set of discrete temporally structured response motifs for different odors.…”

Arrestin-mediated desensitization enables intraneuronal olfactory discrimination in Caenorhabditis elegans

“…The data we present for intraneuronal olfactory discrimination is specific to the particular circumstance in which a saturating concentration of an odorant sensed by one neuron is present along with a lower concentration of a second odorant sensed by the same neuron. While the use of arrestin to desensitize active receptors is presumably relatively generalized across diverse odorants under conditions broadly similar to those we’ve employed, other mechanisms have been recently proposed and likely also play a role ( 23 ).…”

Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality

“…Similar responses have also been observed in the ORNs of aquatic organisms including lobster (Bobkov et al, 2012), where a subpopulation of lobster ORNs has been shown to rhythmically burst in a fashion essential for determining the edges of a turbulent plume during odor tracking (Michaelis et al, 2020). Recent results in C. elegans show that hedonic changes in olfactory context can change the responses of an olfactory receptor neuron(Khan et al, 2021, Preprint ). However, to our knowledge, our results provide the first evidence that ORNs can generate a well-defined set of discrete temporally structured response motifs for different odors.…”