From muscle fibres to muscle gears: how dynamic fascicle orientation and shape change impact skeletal muscle function.

Abstract

Skeletal muscle architectural design strongly affects force-generating capacity and excursion range, and its functional importance to animal and human movement is well founded. Traditionally, this 'structure-function relation' has been inferred from architecture measurements with muscles at rest (from anatomical dissections or medical imaging techniques such as ultrasonography or magnetic resonance imaging) and muscle function tested under quasi-steady force conditions (e.g. isometric). A contemporary view recognises that, during active, dynamic contractions, muscles undergo load- and velocity-dependent changes in architecture and three-dimensional shape while remaining near-constant volume. Consequently, whole-muscle length change and velocity can become decoupled from fascicle length change and velocity, such that the whole muscle cannot be treated as a simple linear velocity transmission system but instead as a geared system where the input fascicle length change and velocity differ from the output whole muscle length change and velocity. This phenomenon is described by the concept of 'muscle gearing' and can be quantified as the ratio of the velocities or displacement of the muscle to the fascicle. Gear ratios are not fixed; instead, gear shifts with force and velocity, allowing the whole-muscle output to better match the mechanical demands of the task. Variable gearing is thought to emerge from load-dependent changes in fascicle angle and three-dimensional muscle deformations under volume-preserving and tissue constraints. Variable gearing has important functional implications, as it influences fascicle operating length and shortening velocity for a given task and thereby shifts where fascicles operate along their intrinsic force-length and force-velocity relationships. Through these effects, along with changes in the projection of fascicle force onto the muscle line of action as pennation varies, variable gearing can broaden whole-muscle force and power output across movement conditions. Accordingly, muscle gearing should be considered an integral component of a comprehensive framework for understanding dynamic muscle function in both normal and pathological states. Here, we synthesise evidence from animal and human studies to characterise variation in gearing across muscles, species and contraction conditions, and the factors that may underlie it. We use a previously validated three-dimensional finite-element muscle model to interrogate mechanisms that are difficult to isolate experimentally and, for the first time, demonstrate an effect of muscle activation on gearing. We also consider how ageing, injury and exercise training may alter gearing. Overall, muscle gearing has important functional implications, and our modelling demonstrates that it is an emergent property of the physics of muscle contraction.