Abstract
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.
Highlights
Stretching a contracting muscle produces a dynamic, non-linear force response
We investigate residual force enhancement using a biophysically-detailed computational model of heterogeneous half-sarcomeres that was originally developed for a different purpose [19]
The slowly dissipating phase of the tension response seen in the heterogeneous case strongly resembles the residual force enhancement observed experimentally
Summary
Stretching a contracting muscle produces a dynamic, non-linear force response. The basic experimental finding was first described by Abbott & Aubert [5]. They found that a dogfish muscle stretched during active contraction produced greater steady-state force than if stretched to the same length prior to activation. (A stretch protocol of this kind is depicted in Figure 1.) This was seen as a departure from the well known steady-state length tension relationship as the muscle could be made to produce different amounts of force at a given length by changing its history of movement. Since Abbott & Aubert’s initial description, force enhancement has been observed in many other species, muscle types, and experimental preparations (reviewed elsewhere [6])
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