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A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling
An animal adapts its motor behavior to navigate the external environment. This adaptation depends on proprioception, which provides feedback on an animal’s body postures. How proprioception mechanisms interact with motor circuits and contribute to locomotor adaptation remains unclear. Here, we descr...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193984/ https://www.ncbi.nlm.nih.gov/pubmed/37155851 http://dx.doi.org/10.1073/pnas.2219341120 |
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author | Ji, Hongfei Fouad, Anthony D. Li, Zihao Ruba, Andrew Fang-Yen, Christopher |
author_facet | Ji, Hongfei Fouad, Anthony D. Li, Zihao Ruba, Andrew Fang-Yen, Christopher |
author_sort | Ji, Hongfei |
collection | PubMed |
description | An animal adapts its motor behavior to navigate the external environment. This adaptation depends on proprioception, which provides feedback on an animal’s body postures. How proprioception mechanisms interact with motor circuits and contribute to locomotor adaptation remains unclear. Here, we describe and characterize proprioception-mediated homeostatic control of undulatory movement in the roundworm Caenorhabditis elegans. We found that the worm responds to optogenetically or mechanically induced decreases in midbody bending amplitude by increasing its anterior amplitude. Conversely, it responds to increased midbody amplitude by decreasing the anterior amplitude. Using genetics, microfluidic and optogenetic perturbation response analyses, and optical neurophysiology, we elucidated the neural circuit underlying this compensatory postural response. The dopaminergic PDE neurons proprioceptively sense midbody bending and signal to AVK interneurons via the D2-like dopamine receptor DOP-3. The FMRFamide-like neuropeptide FLP-1, released by AVK, regulates SMB head motor neurons to modulate anterior bending. We propose that this homeostatic behavioral control optimizes locomotor efficiency. Our findings demonstrate a mechanism in which proprioception works with dopamine and neuropeptide signaling to mediate motor control, a motif that may be conserved in other animals. |
format | Online Article Text |
id | pubmed-10193984 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-101939842023-11-08 A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling Ji, Hongfei Fouad, Anthony D. Li, Zihao Ruba, Andrew Fang-Yen, Christopher Proc Natl Acad Sci U S A Biological Sciences An animal adapts its motor behavior to navigate the external environment. This adaptation depends on proprioception, which provides feedback on an animal’s body postures. How proprioception mechanisms interact with motor circuits and contribute to locomotor adaptation remains unclear. Here, we describe and characterize proprioception-mediated homeostatic control of undulatory movement in the roundworm Caenorhabditis elegans. We found that the worm responds to optogenetically or mechanically induced decreases in midbody bending amplitude by increasing its anterior amplitude. Conversely, it responds to increased midbody amplitude by decreasing the anterior amplitude. Using genetics, microfluidic and optogenetic perturbation response analyses, and optical neurophysiology, we elucidated the neural circuit underlying this compensatory postural response. The dopaminergic PDE neurons proprioceptively sense midbody bending and signal to AVK interneurons via the D2-like dopamine receptor DOP-3. The FMRFamide-like neuropeptide FLP-1, released by AVK, regulates SMB head motor neurons to modulate anterior bending. We propose that this homeostatic behavioral control optimizes locomotor efficiency. Our findings demonstrate a mechanism in which proprioception works with dopamine and neuropeptide signaling to mediate motor control, a motif that may be conserved in other animals. National Academy of Sciences 2023-05-08 2023-05-16 /pmc/articles/PMC10193984/ /pubmed/37155851 http://dx.doi.org/10.1073/pnas.2219341120 Text en Copyright © 2023 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 Ji, Hongfei Fouad, Anthony D. Li, Zihao Ruba, Andrew Fang-Yen, Christopher A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title | A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title_full | A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title_fullStr | A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title_full_unstemmed | A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title_short | A proprioceptive feedback circuit drives Caenorhabditis elegans locomotor adaptation through dopamine signaling |
title_sort | proprioceptive feedback circuit drives caenorhabditis elegans locomotor adaptation through dopamine signaling |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10193984/ https://www.ncbi.nlm.nih.gov/pubmed/37155851 http://dx.doi.org/10.1073/pnas.2219341120 |
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