Dataset Information

The Energy of Muscle Contraction. I. Tissue Force and Deformation During Fixed-End Contractions.

ABSTRACT: During contraction the energy of muscle tissue increases due to energy from the hydrolysis of ATP. This energy is distributed across the tissue as strain-energy potentials in the contractile elements, strain-energy potential from the 3D deformation of the base-material tissue (containing cellular and extracellular matrix effects), energy related to changes in the muscle's nearly incompressible volume and external work done at the muscle surface. Thus, energy is redistributed through the muscle's tissue as it contracts, with only a component of this energy being used to do mechanical work and develop forces in the muscle's longitudinal direction. Understanding how the strain-energy potentials are redistributed through the muscle tissue will help enlighten why the mechanical performance of whole muscle in its longitudinal direction does not match the performance that would be expected from the contractile elements alone. Here we demonstrate these physical effects using a 3D muscle model based on the finite element method. The tissue deformations within contracting muscle are large, and so the mechanics of contraction were explained using the principles of continuum mechanics for large deformations. We present simulations of a contracting medial gastrocnemius muscle, showing tissue deformations that mirror observations from magnetic resonance imaging. This paper tracks the redistribution of strain-energy potentials through the muscle tissue during fixed-end contractions, and shows how fibre shortening, pennation angle, transverse bulging and anisotropy in the stress and strain of the muscle tissue are all related to the interaction between the material properties of the muscle and the action of the contractile elements.

SUBMITTER: Wakeling JM

PROVIDER: S-EPMC7487973 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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The Energy of Muscle Contraction. I. Tissue Force and Deformation During Fixed-End Contractions.

Wakeling James M JM Ross Stephanie A SA Ryan David S DS Bolsterlee Bart B Konno Ryan R Domínguez Sebastián S Nigam Nilima N

Frontiers in physiology 20200831

During contraction the energy of muscle tissue increases due to energy from the hydrolysis of ATP. This energy is distributed across the tissue as strain-energy potentials in the contractile elements, strain-energy potential from the 3D deformation of the base-material tissue (containing cellular and extracellular matrix effects), energy related to changes in the muscle's nearly incompressible volume and external work done at the muscle surface. Thus, energy is redistributed through the muscle's ...[more]

PMID: 32982762

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Project description:During muscle contraction, chemical energy is converted to mechanical energy when ATP is hydrolysed during cross-bridge cycling. This mechanical energy is then distributed and stored in the tissue as the muscle deforms or is used to perform external work. We previously showed how energy is distributed through contracting muscle during fixed-end contractions; however, it is not clear how the distribution of tissue energy is altered by the kinetic energy of muscle mass during dynamic contractions. In this study we conducted simulations of a 3D continuum muscle model that accounts for tissue mass, as well as force-velocity effects, in which the muscle underwent sinusoidal work-loop contractions coupled with bursts of excitation. We found that increasing muscle size, and therefore mass, increased the kinetic energy per unit volume of the muscle. In addition to greater relative kinetic energy per cycle, relatively more energy was also stored in the aponeurosis, and less was stored in the base material, which represented the intra and extracellular tissue components apart from the myofibrils. These energy changes in larger muscles due to greater mass were associated lower mass-specific mechanical work output per cycle, and this reduction in mass-specific work was greatest for smaller initial pennation angles. When we compared the effects of mass on the model tissue behaviour to that of in situ muscle with added mass during comparable work-loop trials, we found that greater mass led to lower maximum and higher minimum acceleration in the longitudinal (x) direction near the middle of the muscle compared to at the non-fixed end, which indicates that greater mass contributes to tissue non-uniformity in whole muscle. These comparable results for the simulated and in situ muscle also show that this modelling framework behaves in ways that are consistent with experimental muscle. Overall, the results of this study highlight that muscle mass is an important determinant of whole muscle behaviour.

Project description:Changes in muscle shape could play an important role during contraction allowing to circumvent some limits imposed by the fascicle force-velocity (F-V) and power-velocity (P-V) relationships. Indeed, during low-force high-velocity contractions, muscle belly shortening velocity could exceed muscle fascicles shortening velocity, allowing the muscles to operate at higher F-V and P-V potentials (i.e., at a higher fraction of maximal force/power in accordance to the F-V and P-V relationships). By using an ultrafast ultrasound, we investigated the role of muscle shape changes (vastus lateralis) in determining belly gearing (muscle belly velocity/fascicle velocity) and the explosive torque during explosive dynamic contractions (EDC) at angular accelerations ranging from 1000 to 4000°.s-2. By means of ultrasound and dynamometric data, the F-V and P-V relationships both for fascicles and for the muscle belly were assessed. During EDC, fascicle velocity, belly velocity, belly gearing, and knee extensors torque data were analysed from 0 to 150 ms after torque onset; the fascicles and belly F-V and P-V potentials were thus calculated for each EDC. Absolute torque decreased as a function of angular acceleration (from 80 to 71 Nm, for EDC at 1000 and 4000°.s-1, respectively), whereas fascicle velocity and belly velocity increased with angular acceleration (P < 0.001). Belly gearing increased from 1.11 to 1.23 (or EDC at 1000 and 4000°.s-1, respectively) and was positively corelated with the changes in muscle thickness and pennation angle (the changes in latter two equally contributing to belly gearing changes). For the same amount of muscle's mechanical output (force or power), the fascicles operated at higher F-V and P-V potential than the muscle belly (e.g., P-V potential from 0.70 to 0.56 for fascicles and from 0.65 to 0.41 for the muscle belly, respectively). The present results experimentally demonstrate that belly gearing could play an important role during explosive contractions, accommodating the largest part of changes in contraction velocity and allowing the fascicle to operate at higher F-V and P-V potentials.

Dataset Information

The Energy of Muscle Contraction. I. Tissue Force and Deformation During Fixed-End Contractions.

Publications

The Energy of Muscle Contraction. I. Tissue Force and Deformation During Fixed-End Contractions.

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