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A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans
Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis e...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8931235/ https://www.ncbi.nlm.nih.gov/pubmed/35254908 http://dx.doi.org/10.1073/pnas.2115533119 |
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author | Chiang, Yueh-Chen Liao, Chien-Po Pan, Chun-Liang |
author_facet | Chiang, Yueh-Chen Liao, Chien-Po Pan, Chun-Liang |
author_sort | Chiang, Yueh-Chen |
collection | PubMed |
description | Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis elegans induces learned aversion for nutritious bacterial food that displays features of long-term associative memory. Serotonin secreted from the modulatory NSM neuron acts through the SER-4 receptor in the RIB interneuron to drive bacterial avoidance, with NSM and RIB required for the establishment and retrieval for learned aversion, respectively. NSM serotonin synthesis increases early in the induction of systemic mitochondrial stress. Calcium imaging reveals altered RIB responses to bacterial cues in a fraction of stress-primed but not naïve animals. These findings uncover cellular circuits and neuromodulation that enable aversive learning under stress, and lay the foundation for future exploration of behavioral plasticity governed by internal state changes. |
format | Online Article Text |
id | pubmed-8931235 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-89312352022-09-07 A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans Chiang, Yueh-Chen Liao, Chien-Po Pan, Chun-Liang Proc Natl Acad Sci U S A Biological Sciences Physiological stress profoundly alters the internal states of the animals and could drive aversive learning, but signaling and circuit mechanisms underlying such behavioral plasticity remain incompletely understood. Here, we show that mitochondrial disruption in nonneural tissues of Caenorhabditis elegans induces learned aversion for nutritious bacterial food that displays features of long-term associative memory. Serotonin secreted from the modulatory NSM neuron acts through the SER-4 receptor in the RIB interneuron to drive bacterial avoidance, with NSM and RIB required for the establishment and retrieval for learned aversion, respectively. NSM serotonin synthesis increases early in the induction of systemic mitochondrial stress. Calcium imaging reveals altered RIB responses to bacterial cues in a fraction of stress-primed but not naïve animals. These findings uncover cellular circuits and neuromodulation that enable aversive learning under stress, and lay the foundation for future exploration of behavioral plasticity governed by internal state changes. National Academy of Sciences 2022-03-07 2022-03-15 /pmc/articles/PMC8931235/ /pubmed/35254908 http://dx.doi.org/10.1073/pnas.2115533119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Chiang, Yueh-Chen Liao, Chien-Po Pan, Chun-Liang A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title_full | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title_fullStr | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title_full_unstemmed | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title_short | A serotonergic circuit regulates aversive associative learning under mitochondrial stress in C. elegans |
title_sort | serotonergic circuit regulates aversive associative learning under mitochondrial stress in c. elegans |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8931235/ https://www.ncbi.nlm.nih.gov/pubmed/35254908 http://dx.doi.org/10.1073/pnas.2115533119 |
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