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Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids

Chemosensory systems are critical for evaluating the caloric value and potential toxicity of food. While animals can discriminate between thousands of odors, much less is known about the discriminative capabilities of taste systems. Fats and sugars represent calorically potent and attractive food so...

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Autores principales: Brown, Elizabeth B, Shah, Kreesha D, Palermo, Justin, Dey, Manali, Dahanukar, Anupama, Keene, Alex C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8169106/
https://www.ncbi.nlm.nih.gov/pubmed/33949306
http://dx.doi.org/10.7554/eLife.67878
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author Brown, Elizabeth B
Shah, Kreesha D
Palermo, Justin
Dey, Manali
Dahanukar, Anupama
Keene, Alex C
author_facet Brown, Elizabeth B
Shah, Kreesha D
Palermo, Justin
Dey, Manali
Dahanukar, Anupama
Keene, Alex C
author_sort Brown, Elizabeth B
collection PubMed
description Chemosensory systems are critical for evaluating the caloric value and potential toxicity of food. While animals can discriminate between thousands of odors, much less is known about the discriminative capabilities of taste systems. Fats and sugars represent calorically potent and attractive food sources that contribute to hedonic feeding. Despite the differences in nutritional value between fats and sugars, the ability of the taste system to discriminate between different rewarding tastants is thought to be limited. In Drosophila, taste neurons expressing the ionotropic receptor 56d (IR56d) are required for reflexive behavioral responses to the medium-chain fatty acid, hexanoic acid. Here, we tested whether flies can discriminate between different classes of fatty acids using an aversive memory assay. Our results indicate that flies are able to discriminate medium-chain fatty acids from both short- and long-chain fatty acids, but not from other medium-chain fatty acids. While IR56d neurons are broadly responsive to short-, medium-, and long-chain fatty acids, genetic deletion of IR56d selectively disrupts response to medium-chain fatty acids. Further, IR56d+ GR64f+ neurons are necessary for proboscis extension response (PER) to medium-chain fatty acids, but both IR56d and GR64f neurons are dispensable for PER to short- and long-chain fatty acids, indicating the involvement of one or more other classes of neurons. Together, these findings reveal that IR56d is selectively required for medium-chain fatty acid taste, and discrimination of fatty acids occurs through differential receptor activation in shared populations of neurons. Our study uncovers a capacity for the taste system to encode tastant identity within a taste category.
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spelling pubmed-81691062021-06-04 Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids Brown, Elizabeth B Shah, Kreesha D Palermo, Justin Dey, Manali Dahanukar, Anupama Keene, Alex C eLife Neuroscience Chemosensory systems are critical for evaluating the caloric value and potential toxicity of food. While animals can discriminate between thousands of odors, much less is known about the discriminative capabilities of taste systems. Fats and sugars represent calorically potent and attractive food sources that contribute to hedonic feeding. Despite the differences in nutritional value between fats and sugars, the ability of the taste system to discriminate between different rewarding tastants is thought to be limited. In Drosophila, taste neurons expressing the ionotropic receptor 56d (IR56d) are required for reflexive behavioral responses to the medium-chain fatty acid, hexanoic acid. Here, we tested whether flies can discriminate between different classes of fatty acids using an aversive memory assay. Our results indicate that flies are able to discriminate medium-chain fatty acids from both short- and long-chain fatty acids, but not from other medium-chain fatty acids. While IR56d neurons are broadly responsive to short-, medium-, and long-chain fatty acids, genetic deletion of IR56d selectively disrupts response to medium-chain fatty acids. Further, IR56d+ GR64f+ neurons are necessary for proboscis extension response (PER) to medium-chain fatty acids, but both IR56d and GR64f neurons are dispensable for PER to short- and long-chain fatty acids, indicating the involvement of one or more other classes of neurons. Together, these findings reveal that IR56d is selectively required for medium-chain fatty acid taste, and discrimination of fatty acids occurs through differential receptor activation in shared populations of neurons. Our study uncovers a capacity for the taste system to encode tastant identity within a taste category. eLife Sciences Publications, Ltd 2021-05-05 /pmc/articles/PMC8169106/ /pubmed/33949306 http://dx.doi.org/10.7554/eLife.67878 Text en © 2021, Brown 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
Brown, Elizabeth B
Shah, Kreesha D
Palermo, Justin
Dey, Manali
Dahanukar, Anupama
Keene, Alex C
Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title_full Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title_fullStr Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title_full_unstemmed Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title_short Ir56d-dependent fatty acid responses in Drosophila uncover taste discrimination between different classes of fatty acids
title_sort ir56d-dependent fatty acid responses in drosophila uncover taste discrimination between different classes of fatty acids
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8169106/
https://www.ncbi.nlm.nih.gov/pubmed/33949306
http://dx.doi.org/10.7554/eLife.67878
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