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Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length

We most often consider muscle as a motor generating force in the direction of shortening, but less often consider its roles as a spring or a brake. Here we develop a fully three-dimensional spatially explicit model of muscle to isolate the locations of forces and energies that are difficult to separ...

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Detalles Bibliográficos
Autores principales: Williams, C. David, Regnier, Michael, Daniel, Thomas L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499250/
https://www.ncbi.nlm.nih.gov/pubmed/23166482
http://dx.doi.org/10.1371/journal.pcbi.1002770
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author Williams, C. David
Regnier, Michael
Daniel, Thomas L.
author_facet Williams, C. David
Regnier, Michael
Daniel, Thomas L.
author_sort Williams, C. David
collection PubMed
description We most often consider muscle as a motor generating force in the direction of shortening, but less often consider its roles as a spring or a brake. Here we develop a fully three-dimensional spatially explicit model of muscle to isolate the locations of forces and energies that are difficult to separate experimentally. We show the strain energy in the thick and thin filaments is less than one third the strain energy in attached cross-bridges. This result suggests the cross-bridges act as springs, storing energy within muscle in addition to generating the force which powers muscle. Comparing model estimates of energy consumed to elastic energy stored, we show that the ratio of these two properties changes with sarcomere length. The model predicts storage of a greater fraction of energy at short sarcomere lengths, suggesting a mechanism by which muscle function shifts as force production declines, from motor to spring. Additionally, we investigate the force that muscle produces in the radial or transverse direction, orthogonal to the direction of shortening. We confirm prior experimental estimates that place radial forces on the same order of magnitude as axial forces, although we find that radial forces and axial forces vary differently with changes in sarcomere length.
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spelling pubmed-34992502012-11-19 Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length Williams, C. David Regnier, Michael Daniel, Thomas L. PLoS Comput Biol Research Article We most often consider muscle as a motor generating force in the direction of shortening, but less often consider its roles as a spring or a brake. Here we develop a fully three-dimensional spatially explicit model of muscle to isolate the locations of forces and energies that are difficult to separate experimentally. We show the strain energy in the thick and thin filaments is less than one third the strain energy in attached cross-bridges. This result suggests the cross-bridges act as springs, storing energy within muscle in addition to generating the force which powers muscle. Comparing model estimates of energy consumed to elastic energy stored, we show that the ratio of these two properties changes with sarcomere length. The model predicts storage of a greater fraction of energy at short sarcomere lengths, suggesting a mechanism by which muscle function shifts as force production declines, from motor to spring. Additionally, we investigate the force that muscle produces in the radial or transverse direction, orthogonal to the direction of shortening. We confirm prior experimental estimates that place radial forces on the same order of magnitude as axial forces, although we find that radial forces and axial forces vary differently with changes in sarcomere length. Public Library of Science 2012-11-15 /pmc/articles/PMC3499250/ /pubmed/23166482 http://dx.doi.org/10.1371/journal.pcbi.1002770 Text en © 2012 Williams et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Williams, C. David
Regnier, Michael
Daniel, Thomas L.
Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title_full Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title_fullStr Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title_full_unstemmed Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title_short Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length
title_sort elastic energy storage and radial forces in the myofilament lattice depend on sarcomere length
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499250/
https://www.ncbi.nlm.nih.gov/pubmed/23166482
http://dx.doi.org/10.1371/journal.pcbi.1002770
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