ABSTRACT Lateralization of neuronal functions plays a critical role in regulating behavioral flexibility, but the underlying molecular mechanisms are challenging to establish at a single-neuron level. We previously showed that attraction ofC. elegansto a medium-chain alcohol switches to avoidance in a uniform background of a second attractive odorant. This context-dependent behavioral plasticity is mediated by symmetric inversion of the odor-evoked response sign in the bilateral AWC olfactory neurons. Here we show that this symmetric response plasticity is driven by asymmetric molecular mechanisms in the AWC neuron pair. Mutations in thegcy-12receptor guanylyl cyclase abolish odor response plasticity only in AWCOFF; the opposing odor-evoked response signs in AWCOFFand AWCONingcy-12mutants results in these animals being behaviorally indifferent to this chemical. We find thatgcy-12is expressed, and required, in both AWC neurons to regulate odor response plasticity only in AWCOFF. We further show that disruption of AWC fate lateralization results in loss of asymmetry in the response plasticity ingcy-12mutants. Our results indicate that symmetric neuronal response plasticity can arise from asymmetry in underlying molecular mechanisms, and suggest that lateralization of signaling pathways in defined conditions may enhance neuronal and behavioral flexibility.
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Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type
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 Caenorhabditis 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 these 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 distinct 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.
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- Award ID(s):
- 2042100
- PAR ID:
- 10410864
- Editor(s):
- Desplan, Claude
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 20
- Issue:
- 6
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3001677
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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