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Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae

The ability to adjust the speed of locomotion is essential for survival. In limbed animals, the frequency of locomotion is modulated primarily by changing the duration of the stance phase. The underlying neural mechanisms of this selective modulation remain an open question. Here, we report a neural...

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Autores principales: Liu, Yingtao, Hasegawa, Eri, Nose, Akinao, Zwart, Maarten F, Kohsaka, Hiroshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409504/
https://www.ncbi.nlm.nih.gov/pubmed/37551094
http://dx.doi.org/10.7554/eLife.83328
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author Liu, Yingtao
Hasegawa, Eri
Nose, Akinao
Zwart, Maarten F
Kohsaka, Hiroshi
author_facet Liu, Yingtao
Hasegawa, Eri
Nose, Akinao
Zwart, Maarten F
Kohsaka, Hiroshi
author_sort Liu, Yingtao
collection PubMed
description The ability to adjust the speed of locomotion is essential for survival. In limbed animals, the frequency of locomotion is modulated primarily by changing the duration of the stance phase. The underlying neural mechanisms of this selective modulation remain an open question. Here, we report a neural circuit controlling a similarly selective adjustment of locomotion frequency in Drosophila larvae. Drosophila larvae crawl using peristaltic waves of muscle contractions. We find that larvae adjust the frequency of locomotion mostly by varying the time between consecutive contraction waves, reminiscent of limbed locomotion. A specific set of muscles, the lateral transverse (LT) muscles, co-contract in all segments during this phase, the duration of which sets the duration of the interwave phase. We identify two types of GABAergic interneurons in the LT neural network, premotor neuron A26f and its presynaptic partner A31c, which exhibit segmentally synchronized activity and control locomotor frequency by setting the amplitude and duration of LT muscle contractions. Altogether, our results reveal an inhibitory central circuit that sets the frequency of locomotion by controlling the duration of the period in between peristaltic waves. Further analysis of the descending inputs onto this circuit will help understand the higher control of this selective modulation.
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spelling pubmed-104095042023-08-09 Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae Liu, Yingtao Hasegawa, Eri Nose, Akinao Zwart, Maarten F Kohsaka, Hiroshi eLife Neuroscience The ability to adjust the speed of locomotion is essential for survival. In limbed animals, the frequency of locomotion is modulated primarily by changing the duration of the stance phase. The underlying neural mechanisms of this selective modulation remain an open question. Here, we report a neural circuit controlling a similarly selective adjustment of locomotion frequency in Drosophila larvae. Drosophila larvae crawl using peristaltic waves of muscle contractions. We find that larvae adjust the frequency of locomotion mostly by varying the time between consecutive contraction waves, reminiscent of limbed locomotion. A specific set of muscles, the lateral transverse (LT) muscles, co-contract in all segments during this phase, the duration of which sets the duration of the interwave phase. We identify two types of GABAergic interneurons in the LT neural network, premotor neuron A26f and its presynaptic partner A31c, which exhibit segmentally synchronized activity and control locomotor frequency by setting the amplitude and duration of LT muscle contractions. Altogether, our results reveal an inhibitory central circuit that sets the frequency of locomotion by controlling the duration of the period in between peristaltic waves. Further analysis of the descending inputs onto this circuit will help understand the higher control of this selective modulation. eLife Sciences Publications, Ltd 2023-08-08 /pmc/articles/PMC10409504/ /pubmed/37551094 http://dx.doi.org/10.7554/eLife.83328 Text en © 2023, Liu et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Liu, Yingtao
Hasegawa, Eri
Nose, Akinao
Zwart, Maarten F
Kohsaka, Hiroshi
Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title_full Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title_fullStr Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title_full_unstemmed Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title_short Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae
title_sort synchronous multi-segmental activity between metachronal waves controls locomotion speed in drosophila larvae
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409504/
https://www.ncbi.nlm.nih.gov/pubmed/37551094
http://dx.doi.org/10.7554/eLife.83328
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