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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 sho...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232122/ https://www.ncbi.nlm.nih.gov/pubmed/35696430 http://dx.doi.org/10.1371/journal.pbio.3001677 |
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author | Khan, Munzareen Hartmann, Anna H. O’Donnell, Michael P. Piccione, Madeline Pandey, Anjali Chao, Pin-Hao Dwyer, Noelle D. Bargmann, Cornelia I. Sengupta, Piali |
author_facet | Khan, Munzareen Hartmann, Anna H. O’Donnell, Michael P. Piccione, Madeline Pandey, Anjali Chao, Pin-Hao Dwyer, Noelle D. Bargmann, Cornelia I. Sengupta, Piali |
author_sort | Khan, Munzareen |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-9232122 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-92321222022-06-25 Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type Khan, Munzareen Hartmann, Anna H. O’Donnell, Michael P. Piccione, Madeline Pandey, Anjali Chao, Pin-Hao Dwyer, Noelle D. Bargmann, Cornelia I. Sengupta, Piali PLoS Biol Short Reports 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. Public Library of Science 2022-06-13 /pmc/articles/PMC9232122/ /pubmed/35696430 http://dx.doi.org/10.1371/journal.pbio.3001677 Text en © 2022 Khan et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Short Reports Khan, Munzareen Hartmann, Anna H. O’Donnell, Michael P. Piccione, Madeline Pandey, Anjali Chao, Pin-Hao Dwyer, Noelle D. Bargmann, Cornelia I. Sengupta, Piali Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title | Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title_full | Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title_fullStr | Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title_full_unstemmed | Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title_short | Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
title_sort | context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type |
topic | Short Reports |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232122/ https://www.ncbi.nlm.nih.gov/pubmed/35696430 http://dx.doi.org/10.1371/journal.pbio.3001677 |
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