ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors
Animals must respond to the ingestion of food by generating adaptive behaviors, but the role of gut-brain signaling in behavioral regulation is poorly understood. Here, we identify conserved ion channels in an enteric serotonergic neuron that mediate its responses to food ingestion and decipher how...
Main Authors: | , , , , , , , |
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Format: | Article |
Language: | English |
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Elsevier BV
2020
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Online Access: | https://hdl.handle.net/1721.1/125439 |
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author | Rhoades, Jeffrey L. Nwabudike, Ijeoma Yu, Stephanie K. McLachlan, Ian G. Madan, Gurrein K. Abebe, Eden Powers, Joshua R. Flavell, Steven Willem |
author2 | Picower Institute for Learning and Memory |
author_facet | Picower Institute for Learning and Memory Rhoades, Jeffrey L. Nwabudike, Ijeoma Yu, Stephanie K. McLachlan, Ian G. Madan, Gurrein K. Abebe, Eden Powers, Joshua R. Flavell, Steven Willem |
author_sort | Rhoades, Jeffrey L. |
collection | MIT |
description | Animals must respond to the ingestion of food by generating adaptive behaviors, but the role of gut-brain signaling in behavioral regulation is poorly understood. Here, we identify conserved ion channels in an enteric serotonergic neuron that mediate its responses to food ingestion and decipher how these responses drive changes in foraging behavior. We show that the C. elegans serotonergic neuron NSM acts as an enteric sensory neuron that acutely detects food ingestion. We identify the novel and conserved acid-sensing ion channels (ASICs) DEL-7 and DEL-3 as NSM-enriched channels required for feeding-dependent NSM activity, which in turn drives slow locomotion while animals feed. Point mutations that alter the DEL-7 channel change NSM dynamics and associated behavioral dynamics of the organism. This study provides causal links between food ingestion, molecular and physiological properties of an enteric serotonergic neuron, and adaptive feeding behaviors, yielding a new view of how enteric neurons control behavior. |
first_indexed | 2024-09-23T15:59:31Z |
format | Article |
id | mit-1721.1/125439 |
institution | Massachusetts Institute of Technology |
language | English |
last_indexed | 2024-09-23T15:59:31Z |
publishDate | 2020 |
publisher | Elsevier BV |
record_format | dspace |
spelling | mit-1721.1/1254392022-09-29T17:32:08Z ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors Rhoades, Jeffrey L. Nwabudike, Ijeoma Yu, Stephanie K. McLachlan, Ian G. Madan, Gurrein K. Abebe, Eden Powers, Joshua R. Flavell, Steven Willem Picower Institute for Learning and Memory Animals must respond to the ingestion of food by generating adaptive behaviors, but the role of gut-brain signaling in behavioral regulation is poorly understood. Here, we identify conserved ion channels in an enteric serotonergic neuron that mediate its responses to food ingestion and decipher how these responses drive changes in foraging behavior. We show that the C. elegans serotonergic neuron NSM acts as an enteric sensory neuron that acutely detects food ingestion. We identify the novel and conserved acid-sensing ion channels (ASICs) DEL-7 and DEL-3 as NSM-enriched channels required for feeding-dependent NSM activity, which in turn drives slow locomotion while animals feed. Point mutations that alter the DEL-7 channel change NSM dynamics and associated behavioral dynamics of the organism. This study provides causal links between food ingestion, molecular and physiological properties of an enteric serotonergic neuron, and adaptive feeding behaviors, yielding a new view of how enteric neurons control behavior. University of Minnesota. Caenorhabditis Genetics Center (Grant P40 OD010440) National Institutes of Health (U.S.) (Grant R01NS104892) National Institutes of Health (U.S.) (Grant R01NS076558) National Science Foundation (U.S.) (Grant IOS 1353845) 2020-05-26T12:42:25Z 2020-05-26T12:42:25Z 2019-01 2020-01-21T16:26:01Z Article http://purl.org/eprint/type/JournalArticle 0092-8674 https://hdl.handle.net/1721.1/125439 Rhoades, Jeffrey L. et al. “ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors.” Cell 176 (2019): 85-97.e14 © 2019 The Author(s) en https://dx.doi.org/10.1016/J.CELL.2018.11.023 Cell Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier BV PMC |
spellingShingle | Rhoades, Jeffrey L. Nwabudike, Ijeoma Yu, Stephanie K. McLachlan, Ian G. Madan, Gurrein K. Abebe, Eden Powers, Joshua R. Flavell, Steven Willem ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title | ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title_full | ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title_fullStr | ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title_full_unstemmed | ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title_short | ASICs Mediate Food Responses in an Enteric Serotonergic Neuron that Controls Foraging Behaviors |
title_sort | asics mediate food responses in an enteric serotonergic neuron that controls foraging behaviors |
url | https://hdl.handle.net/1721.1/125439 |
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