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A circuit mechanism for the propagation of waves of muscle contraction in Drosophila

Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae a...

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Autores principales: Fushiki, Akira, Zwart, Maarten F, Kohsaka, Hiroshi, Fetter, Richard D, Cardona, Albert, Nose, Akinao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4829418/
https://www.ncbi.nlm.nih.gov/pubmed/26880545
http://dx.doi.org/10.7554/eLife.13253
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author Fushiki, Akira
Zwart, Maarten F
Kohsaka, Hiroshi
Fetter, Richard D
Cardona, Albert
Nose, Akinao
author_facet Fushiki, Akira
Zwart, Maarten F
Kohsaka, Hiroshi
Fetter, Richard D
Cardona, Albert
Nose, Akinao
author_sort Fushiki, Akira
collection PubMed
description Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion. DOI: http://dx.doi.org/10.7554/eLife.13253.001
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spelling pubmed-48294182016-04-15 A circuit mechanism for the propagation of waves of muscle contraction in Drosophila Fushiki, Akira Zwart, Maarten F Kohsaka, Hiroshi Fetter, Richard D Cardona, Albert Nose, Akinao eLife Neuroscience Animals move by adaptively coordinating the sequential activation of muscles. The circuit mechanisms underlying coordinated locomotion are poorly understood. Here, we report on a novel circuit for the propagation of waves of muscle contraction, using the peristaltic locomotion of Drosophila larvae as a model system. We found an intersegmental chain of synaptically connected neurons, alternating excitatory and inhibitory, necessary for wave propagation and active in phase with the wave. The excitatory neurons (A27h) are premotor and necessary only for forward locomotion, and are modulated by stretch receptors and descending inputs. The inhibitory neurons (GDL) are necessary for both forward and backward locomotion, suggestive of different yet coupled central pattern generators, and its inhibition is necessary for wave propagation. The circuit structure and functional imaging indicated that the commands to contract one segment promote the relaxation of the next segment, revealing a mechanism for wave propagation in peristaltic locomotion. DOI: http://dx.doi.org/10.7554/eLife.13253.001 eLife Sciences Publications, Ltd 2016-02-15 /pmc/articles/PMC4829418/ /pubmed/26880545 http://dx.doi.org/10.7554/eLife.13253 Text en © 2016, Fushiki et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Fushiki, Akira
Zwart, Maarten F
Kohsaka, Hiroshi
Fetter, Richard D
Cardona, Albert
Nose, Akinao
A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title_full A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title_fullStr A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title_full_unstemmed A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title_short A circuit mechanism for the propagation of waves of muscle contraction in Drosophila
title_sort circuit mechanism for the propagation of waves of muscle contraction in drosophila
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4829418/
https://www.ncbi.nlm.nih.gov/pubmed/26880545
http://dx.doi.org/10.7554/eLife.13253
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