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Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila

Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neu...

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Autores principales: Das Chakraborty, Sudeshna, Chang, Hetan, Hansson, Bill S, Sachse, Silke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9142144/
https://www.ncbi.nlm.nih.gov/pubmed/35621267
http://dx.doi.org/10.7554/eLife.74637
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author Das Chakraborty, Sudeshna
Chang, Hetan
Hansson, Bill S
Sachse, Silke
author_facet Das Chakraborty, Sudeshna
Chang, Hetan
Hansson, Bill S
Sachse, Silke
author_sort Das Chakraborty, Sudeshna
collection PubMed
description Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster. We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We show that odors evoke reproducible, stereotypic, and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons.
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spelling pubmed-91421442022-05-28 Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila Das Chakraborty, Sudeshna Chang, Hetan Hansson, Bill S Sachse, Silke eLife Neuroscience Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster. We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We show that odors evoke reproducible, stereotypic, and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons. eLife Sciences Publications, Ltd 2022-05-27 /pmc/articles/PMC9142144/ /pubmed/35621267 http://dx.doi.org/10.7554/eLife.74637 Text en © 2022, Das Chakraborty et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Das Chakraborty, Sudeshna
Chang, Hetan
Hansson, Bill S
Sachse, Silke
Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title_full Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title_fullStr Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title_full_unstemmed Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title_short Higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in Drosophila
title_sort higher-order olfactory neurons in the lateral horn support odor valence and odor identity coding in drosophila
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9142144/
https://www.ncbi.nlm.nih.gov/pubmed/35621267
http://dx.doi.org/10.7554/eLife.74637
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