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Abstract

Crossbridge binding, state transitions, and force in active muscle is dependent on the radial spacing between the myosin-containing thick filament and the actin-containing thin filament in the filament lattice. This radial spacing has been previously shown through spatially explicit modeling and experimental efforts to greatly affect quasi-static, isometric, force production in muscle. It has recently been suggested that this radial spacing might also be able to drive differences in mechanical function, or net work, under dynamic oscillations like those which occur in muscles in vivo. However, previous spatially explicit models either had no radial spacing dependence, meaning the radial spacing could not be investigated, or did include radial spacing dependence but could not reproduce in vivo net work during dynamic oscillations and only investigated isometric contractions. Here we show the first spatially explicit model to include radial crossbridge dependence which can produce mechanical function similar to real muscle. Using this spatially explicit model of a half sarcomere, we show that when oscillated at strain amplitudes and frequencies like those in the main flight muscles of the hawkmoth Manduca sexta, mechanical function (net work) does depend on the lattice spacing. In addition, since the trajectory of lattice spacing changes during dynamic oscillation can vary from organism to organism, we can prescribe a trajectory of lattice spacing changes in the spatially explicit half sarcomere model and investigate the extent to which the time course of lattice spacing changes can affect mechanical function. We simulated a half sarcomere undergoing dynamic oscillations and prescribed the Poisson’s ratio of the lattice to be either 0 (constant lattice spacing) or 0.5 (isovolumetric lattice spacing changes). We also simulated net work using lattice spacing data taken from M. sexta which has a variable Poisson’s ratio. Our simulation results indicate that the lattice spacing can change the mechanical function of muscle, and that in some cases a 1 nm difference can switch the net work of the half sarcomere model from positive (motor-like) to negative (brake-like).

Details

1009240
Company / organization
Title
Nanometer scale difference in myofilament lattice structure of muscle alters muscle function in a spatially explicit model
Publication title
Volume
21
Issue
4
First page
e1012862
Number of pages
24
Publication year
2025
Publication date
Apr 2025
Section
Research Article
Publisher
Public Library of Science
Place of publication
San Francisco
Country of publication
United States
Publication subject
ISSN
1553734X
e-ISSN
15537358
Source type
Scholarly Journal
Language of publication
English
Document type
Journal Article
Publication history
 
 
Milestone dates
2024-05-29 (Received); 2025-02-09 (Accepted); 2025-04-07 (Published)
ProQuest document ID
3270580275
Document URL
https://www.proquest.com/scholarly-journals/nanometer-scale-difference-myofilament-lattice/docview/3270580275/se-2?accountid=208611
Copyright
© 2025 Tune and Sponberg. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Last updated
2025-11-11
Database
ProQuest One Academic