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Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans

Sensations, especially nociception, are tightly controlled and regulated by the central and peripheral nervous systems. Osmotic sensation and related physiological and behavioral reactions are essential for animal well-being and survival. In this study, we find that interaction between secondary noc...

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Autores principales: Liu, Hui, Wu, Jing-Jing, Li, Rong, Wang, Ping-Zhou, Huang, Jia-Hao, Xu, Yu, Zhao, Jia-Lu, Wu, Piao-Ping, Li, Si-Jia, Wu, Zheng-Xing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10050701/
https://www.ncbi.nlm.nih.gov/pubmed/37008778
http://dx.doi.org/10.3389/fnmol.2023.1101628
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author Liu, Hui
Wu, Jing-Jing
Li, Rong
Wang, Ping-Zhou
Huang, Jia-Hao
Xu, Yu
Zhao, Jia-Lu
Wu, Piao-Ping
Li, Si-Jia
Wu, Zheng-Xing
author_facet Liu, Hui
Wu, Jing-Jing
Li, Rong
Wang, Ping-Zhou
Huang, Jia-Hao
Xu, Yu
Zhao, Jia-Lu
Wu, Piao-Ping
Li, Si-Jia
Wu, Zheng-Xing
author_sort Liu, Hui
collection PubMed
description Sensations, especially nociception, are tightly controlled and regulated by the central and peripheral nervous systems. Osmotic sensation and related physiological and behavioral reactions are essential for animal well-being and survival. In this study, we find that interaction between secondary nociceptive ADL and primary nociceptive ASH neurons upregulates Caenorhabditis elegans avoidance of the mild and medium hyperosmolality of 0.41 and 0.88 Osm but does not affect avoidance of high osmolality of 1.37 and 2.29 Osm. The interaction between ASH and ADL is actualized through a negative feedback circuit consisting of ASH, ADL, and RIM interneurons. In this circuit, hyperosmolality-sensitive ADL augments the ASH hyperosmotic response and animal hyperosmotic avoidance; RIM inhibits ADL and is excited by ASH; thus, ASH exciting RIM reduces ADL augmenting ASH. The neuronal signal integration modality in the circuit is disexcitation. In addition, ASH promotes hyperosmotic avoidance through ASH/RIC/AIY feedforward circuit. Finally, we find that in addition to ASH and ADL, multiple sensory neurons are involved in hyperosmotic sensation and avoidance behavior.
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spelling pubmed-100507012023-03-30 Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans Liu, Hui Wu, Jing-Jing Li, Rong Wang, Ping-Zhou Huang, Jia-Hao Xu, Yu Zhao, Jia-Lu Wu, Piao-Ping Li, Si-Jia Wu, Zheng-Xing Front Mol Neurosci Molecular Neuroscience Sensations, especially nociception, are tightly controlled and regulated by the central and peripheral nervous systems. Osmotic sensation and related physiological and behavioral reactions are essential for animal well-being and survival. In this study, we find that interaction between secondary nociceptive ADL and primary nociceptive ASH neurons upregulates Caenorhabditis elegans avoidance of the mild and medium hyperosmolality of 0.41 and 0.88 Osm but does not affect avoidance of high osmolality of 1.37 and 2.29 Osm. The interaction between ASH and ADL is actualized through a negative feedback circuit consisting of ASH, ADL, and RIM interneurons. In this circuit, hyperosmolality-sensitive ADL augments the ASH hyperosmotic response and animal hyperosmotic avoidance; RIM inhibits ADL and is excited by ASH; thus, ASH exciting RIM reduces ADL augmenting ASH. The neuronal signal integration modality in the circuit is disexcitation. In addition, ASH promotes hyperosmotic avoidance through ASH/RIC/AIY feedforward circuit. Finally, we find that in addition to ASH and ADL, multiple sensory neurons are involved in hyperosmotic sensation and avoidance behavior. Frontiers Media S.A. 2023-03-15 /pmc/articles/PMC10050701/ /pubmed/37008778 http://dx.doi.org/10.3389/fnmol.2023.1101628 Text en Copyright © 2023 Liu, Wu, Li, Wang, Huang, Xu, Zhao, Wu, Li and Wu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Neuroscience
Liu, Hui
Wu, Jing-Jing
Li, Rong
Wang, Ping-Zhou
Huang, Jia-Hao
Xu, Yu
Zhao, Jia-Lu
Wu, Piao-Ping
Li, Si-Jia
Wu, Zheng-Xing
Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title_full Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title_fullStr Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title_full_unstemmed Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title_short Disexcitation in the ASH/RIM/ADL negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in Caenorhabditis elegans
title_sort disexcitation in the ash/rim/adl negative feedback circuit fine-tunes hyperosmotic sensation and avoidance in caenorhabditis elegans
topic Molecular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10050701/
https://www.ncbi.nlm.nih.gov/pubmed/37008778
http://dx.doi.org/10.3389/fnmol.2023.1101628
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