A Mathematical Model of Muscle Containing Heterogeneous Half-Sarcomeres Exhibits Residual Force Enhancement
| Autor: | Kenneth S. Campbell, P. Chris Hatfield, Stuart G. Campbell |
|---|---|
| Rok vydání: | 2011 |
| Předmět: |
Sarcomeres
Materials science Muscle Fibers Skeletal Biophysics Isometric exercise Residual Models Biological Biophysics Simulations Sarcomere Standard deviation Strain energy 03 medical and health sciences Cellular and Molecular Neuroscience 0302 clinical medicine Isometric Contraction Genetics medicine Animals Computer Simulation Biomechanics Muscle Skeletal lcsh:QH301-705.5 Biology Molecular Biology Ecology Evolution Behavior and Systematics Simulation 030304 developmental biology Stochastic Processes 0303 health sciences Ecology Tension (physics) Computational Biology Skeletal muscle Mechanics Biomechanical Phenomena medicine.anatomical_structure lcsh:Biology (General) Computational Theory and Mathematics Modeling and Simulation Biophysic Al Simulations medicine.symptom 030217 neurology & neurosurgery Muscle Contraction Research Article Muscle contraction |
| Zdroj: | PLoS Computational Biology PLoS Computational Biology, Vol 7, Iss 9, p e1002156 (2011) |
| ISSN: | 1553-7358 |
| DOI: | 10.1371/journal.pcbi.1002156 |
| Popis: | A skeletal muscle fiber that is stimulated to contract and then stretched from L1 to L2 produces more force after the initial transient decays than if it is stimulated at L2. This behavior has been well studied experimentally, and is known as residual force enhancement. The underlying mechanism remains controversial. We hypothesized that residual force enhancement could reflect mechanical interactions between heterogeneous half-sarcomeres. To test this hypothesis, we subjected a computational model of interacting heterogeneous half-sarcomeres to the same activation and stretch protocols that produce residual force enhancement in real preparations. Following a transient period of elevated force associated with active stretching, the model predicted a slowly decaying force enhancement lasting >30 seconds after stretch. Enhancement was on the order of 13% above isometric tension at the post-stretch muscle length, which agrees well with experimental measurements. Force enhancement in the model was proportional to stretch magnitude but did not depend strongly on the velocity of stretch, also in agreement with experiments. Even small variability in the strength of half-sarcomeres (2.1% standard deviation, normally distributed) was sufficient to produce a 5% force enhancement over isometric tension. Analysis of the model suggests that heterogeneity in half-sarcomeres leads to residual force enhancement by storing strain energy introduced during active stretch in distributions of bound cross-bridges. Complex interactions between the heterogeneous half-sarcomeres then dissipate this stored energy at a rate much slower than isolated cross-bridges would cycle. Given the variations in half-sarcomere length that have been observed in real muscle preparations and the stochastic variability inherent in all biological systems, half-sarcomere heterogeneity cannot be excluded as a contributing source of residual force enhancement. Author Summary Textbooks often state that the force produced by a contracting muscle depends on its length. Nearly 60 years ago, it was discovered that this length-tension relationship is violated if the muscle is stretched to a given length while contracting, in which case the muscle produces more force than if it was stretched to the given length prior to contraction. This effect is known as residual force enhancement, and its mechanism remains controversial. Understanding residual force enhancement is important because it potentially affects outcomes of many in vivo and in vitro experiments where contracting muscles or muscle preparations are stretched. In this work, we use a computational model of half-sarcomeres connected in series to show that residual force enhancement is an emergent behavior of the contractile system when the half-sarcomeres are not completely identical. Force enhancement in the model shares several key properties with the phenomenon observed in real muscle, including independence from the rate of stretch and proportionality to stretch magnitude. Enhancement in the model is produced by a previously undescribed mechanism in which complex interactions between the heterogeneous half-sarcomeres dissipate strain-energy from the imposed stretch at very slow rates, creating a long-lasting, enhanced level of force. |
| Databáze: | OpenAIRE |
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