How muscle ageing affects rapid goal-directed movement: mechanistic insights from a simple model

As humans and other animals age, passive and active muscle properties change markedly, with reduced peak tension, peak strain rate, activation and deactivation rate, and increased parallel stiffness. It is thought that these alterations modify locomotor performance, but establishing causal links is difficult when many parameters vary at once. We developed a simplified model of an elbow joint with two antagonistic Hill-type muscles, and varied the associated muscle parameters combinatorially over a large range. For a given parameter combination, we found optimal joint movements that minimized cumulative squared error to a target while starting and ending at rest. Emergent behaviour from the optimisations compared well to ballistic point-to-point arm movements in humans. Age-associated reductions of maximum isometric force, maximum strain rate and activation rate all had detrimental effects on performance, independent of other parameters. In contrast, deactivation time and passive parallel stiffness had no effect on performance on their own, but pronounced interactive effects with each other. Increasing stiffness reduced joint movement time at fast deactivation rates, but increased movement time at slow deactivation rates. This occurs because antagonist muscles resist the passive tension at rest, but are stretched eccentrically by the agonist, amplifying their active resistive force. Fast-deactivating muscles can avoid this resistive effect, allowing the passive stiffness to amplify accelerating force and enhance performance. In all cases, coactivation emerged as optimal during and after the braking period, and during the acceleration phase when stiffness increased. As deactivation time increased, so too did coactivation levels– but coactivation was not generally associated with a reduction in performance. Our simulations offer evidence that age-related changes in muscle strength, activation time and maximum contraction velocity can reduce ballistic performance in a goal-directed task, but the effects of increased muscle stiffness and deactivation time depend on their relative values.Author summary: As humans age, our muscles can get weaker, less excitable, stiffer and slower. At the same time, older adults tend to reach more slowly– making balance recovery more difficult. Since older muscles change in multiple ways simultaneously, we don’t know which alterations most affect performance, or whether they interact. We developed a simple model of a human elbow joint, and used optimisation to find muscle activities that optimised speed and accuracy. We then digitally “aged” the muscle by modifying its properties to determine which most strongly alter performance. We found that the muscle activation rate, as well as its peak force and maximum contraction speed, most affect the speed and accuracy of reaching. On their own, muscle stiffness and speed of deactivation (turning “off” the muscle) don’t affect performance. If the muscle turns off quickly, high stiffness helps the arm move faster, analogous to loading and firing a slingshot. However, if the muscle turns off slowly, higher stiffness slows the arm down– as if trying to shoot a slingshot without releasing the elastic bands. Altogether, our results help point to the key muscle changes that slow movement with ageing, allowing future research to better target therapeutic interventions.