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Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates
Superfast muscles (SFMs) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFMs share excitation-c...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5699865/ https://www.ncbi.nlm.nih.gov/pubmed/29165242 http://dx.doi.org/10.7554/eLife.29425 |
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author | Mead, Andrew F Osinalde, Nerea Ørtenblad, Niels Nielsen, Joachim Brewer, Jonathan Vellema, Michiel Adam, Iris Scharff, Constance Song, Yafeng Frandsen, Ulrik Blagoev, Blagoy Kratchmarova, Irina Elemans, Coen PH |
author_facet | Mead, Andrew F Osinalde, Nerea Ørtenblad, Niels Nielsen, Joachim Brewer, Jonathan Vellema, Michiel Adam, Iris Scharff, Constance Song, Yafeng Frandsen, Ulrik Blagoev, Blagoy Kratchmarova, Irina Elemans, Coen PH |
author_sort | Mead, Andrew F |
collection | PubMed |
description | Superfast muscles (SFMs) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFMs share excitation-contraction coupling pathway adaptations for speed, and if SFMs arose once, or from independent evolutionary events. Here, we demonstrate that to achieve rapid actomyosin crossbridge kinetics bat and songbird SFM express myosin heavy chain genes that are evolutionarily and ontologically distinct. Furthermore, we show that all known SFMs share multiple functional adaptations that minimize excitation-contraction coupling transduction times. Our results suggest that SFM evolved independently in sound-producing organs in ray-finned fish, birds, and mammals, and that SFM phenotypes operate at a maximum operational speed set by fundamental constraints in synchronous muscle. Consequentially, these constraints set a fundamental limit to the maximum speed of fine motor control. |
format | Online Article Text |
id | pubmed-5699865 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-56998652017-11-24 Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates Mead, Andrew F Osinalde, Nerea Ørtenblad, Niels Nielsen, Joachim Brewer, Jonathan Vellema, Michiel Adam, Iris Scharff, Constance Song, Yafeng Frandsen, Ulrik Blagoev, Blagoy Kratchmarova, Irina Elemans, Coen PH eLife Structural Biology and Molecular Biophysics Superfast muscles (SFMs) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFMs share excitation-contraction coupling pathway adaptations for speed, and if SFMs arose once, or from independent evolutionary events. Here, we demonstrate that to achieve rapid actomyosin crossbridge kinetics bat and songbird SFM express myosin heavy chain genes that are evolutionarily and ontologically distinct. Furthermore, we show that all known SFMs share multiple functional adaptations that minimize excitation-contraction coupling transduction times. Our results suggest that SFM evolved independently in sound-producing organs in ray-finned fish, birds, and mammals, and that SFM phenotypes operate at a maximum operational speed set by fundamental constraints in synchronous muscle. Consequentially, these constraints set a fundamental limit to the maximum speed of fine motor control. eLife Sciences Publications, Ltd 2017-11-22 /pmc/articles/PMC5699865/ /pubmed/29165242 http://dx.doi.org/10.7554/eLife.29425 Text en © 2017, Mead et al http://creativecommons.org/licenses/by/4.0/ 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 | Structural Biology and Molecular Biophysics Mead, Andrew F Osinalde, Nerea Ørtenblad, Niels Nielsen, Joachim Brewer, Jonathan Vellema, Michiel Adam, Iris Scharff, Constance Song, Yafeng Frandsen, Ulrik Blagoev, Blagoy Kratchmarova, Irina Elemans, Coen PH Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title | Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title_full | Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title_fullStr | Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title_full_unstemmed | Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title_short | Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
title_sort | fundamental constraints in synchronous muscle limit superfast motor control in vertebrates |
topic | Structural Biology and Molecular Biophysics |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5699865/ https://www.ncbi.nlm.nih.gov/pubmed/29165242 http://dx.doi.org/10.7554/eLife.29425 |
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