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Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit

Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles. However, how intersegmentally coordinated patterns of muscular relaxation are regulated by the neural circuits remains poorly understood. Here, we identify Canon, a cl...

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Autores principales: Hiramoto, Atsuki, Jonaitis, Julius, Niki, Sawako, Kohsaka, Hiroshi, Fetter, Richard D., Cardona, Albert, Pulver, Stefan R., Nose, Akinao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8134441/
https://www.ncbi.nlm.nih.gov/pubmed/34011945
http://dx.doi.org/10.1038/s41467-021-23273-y
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author Hiramoto, Atsuki
Jonaitis, Julius
Niki, Sawako
Kohsaka, Hiroshi
Fetter, Richard D.
Cardona, Albert
Pulver, Stefan R.
Nose, Akinao
author_facet Hiramoto, Atsuki
Jonaitis, Julius
Niki, Sawako
Kohsaka, Hiroshi
Fetter, Richard D.
Cardona, Albert
Pulver, Stefan R.
Nose, Akinao
author_sort Hiramoto, Atsuki
collection PubMed
description Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles. However, how intersegmentally coordinated patterns of muscular relaxation are regulated by the neural circuits remains poorly understood. Here, we identify Canon, a class of higher-order premotor interneurons, that regulates muscular relaxation during backward locomotion of Drosophila larvae. Canon neurons are cholinergic interneurons present in each abdominal neuromere and show wave-like activity during fictive backward locomotion. Optogenetic activation of Canon neurons induces relaxation of body wall muscles, whereas inhibition of these neurons disrupts timely muscle relaxation. Canon neurons provide excitatory outputs to inhibitory premotor interneurons. Canon neurons also connect with each other to form an intersegmental circuit and regulate their own wave-like activities. Thus, our results demonstrate how coordinated muscle relaxation can be realized by an intersegmental circuit that regulates its own patterned activity and sequentially terminates motor activities along the anterior-posterior axis.
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spelling pubmed-81344412021-05-24 Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit Hiramoto, Atsuki Jonaitis, Julius Niki, Sawako Kohsaka, Hiroshi Fetter, Richard D. Cardona, Albert Pulver, Stefan R. Nose, Akinao Nat Commun Article Typical patterned movements in animals are achieved through combinations of contraction and delayed relaxation of groups of muscles. However, how intersegmentally coordinated patterns of muscular relaxation are regulated by the neural circuits remains poorly understood. Here, we identify Canon, a class of higher-order premotor interneurons, that regulates muscular relaxation during backward locomotion of Drosophila larvae. Canon neurons are cholinergic interneurons present in each abdominal neuromere and show wave-like activity during fictive backward locomotion. Optogenetic activation of Canon neurons induces relaxation of body wall muscles, whereas inhibition of these neurons disrupts timely muscle relaxation. Canon neurons provide excitatory outputs to inhibitory premotor interneurons. Canon neurons also connect with each other to form an intersegmental circuit and regulate their own wave-like activities. Thus, our results demonstrate how coordinated muscle relaxation can be realized by an intersegmental circuit that regulates its own patterned activity and sequentially terminates motor activities along the anterior-posterior axis. Nature Publishing Group UK 2021-05-19 /pmc/articles/PMC8134441/ /pubmed/34011945 http://dx.doi.org/10.1038/s41467-021-23273-y Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hiramoto, Atsuki
Jonaitis, Julius
Niki, Sawako
Kohsaka, Hiroshi
Fetter, Richard D.
Cardona, Albert
Pulver, Stefan R.
Nose, Akinao
Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title_full Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title_fullStr Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title_full_unstemmed Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title_short Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit
title_sort regulation of coordinated muscular relaxation in drosophila larvae by a pattern-regulating intersegmental circuit
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8134441/
https://www.ncbi.nlm.nih.gov/pubmed/34011945
http://dx.doi.org/10.1038/s41467-021-23273-y
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