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...

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Main Authors: Rhoades, Jeffrey L., Nwabudike, Ijeoma, Yu, Stephanie K., McLachlan, Ian G., Madan, Gurrein K., Abebe, Eden, Powers, Joshua R., Flavell, Steven Willem
Other Authors: Picower Institute for Learning and Memory
Format: Article
Language:English
Published: Elsevier BV 2020
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.
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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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