Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Khan, Munzareen, Hartmann, Anna H., O’Donnell, Michael P., Piccione, Madeline, Pandey, Anjali, Chao, Pin-Hao, Dwyer, Noelle D., Bargmann, Cornelia I., Sengupta, Piali
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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
_version_ 1784735502460518400
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
work_keys_str_mv AT khanmunzareen contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT hartmannannah contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT odonnellmichaelp contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT piccionemadeline contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT pandeyanjali contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT chaopinhao contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT dwyernoelled contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT bargmanncorneliai contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype
AT senguptapiali contextdependentreversalofodorantpreferenceisdrivenbyinversionoftheresponseinasinglesensoryneurontype