From muscle fibres to gears: How fibre rotation and shape change impact 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. This review aims to (i) provide a brief historical overview of how the muscle structure-function relation has been understood from resting muscle structure measurements and modelling and steady-force contractions to observations during dynamic, time-varying active contractions, and (ii) synthesise evidence on muscle gearing, including its measurement, functional consequences, and current understanding of the factors that influence it by reviewing findings from animal and human studies and raising hypotheses to explain the variation in gearing identified across muscle, species, and contraction conditions. Given the challenges in experimentally isolating the contribution of individual factors, we also employ a previously validated three-dimensional finite-element muscle model to interrogate the mechanical phenomena underpinning variable gearing and for the first time report effects from muscle activation. Finally, we briefly discuss the potential role of gearing in the observed changes in muscle function with ageing, injury, and exercise training. Overall, muscle gearing is a distinctive feature of skeletal muscles with important functional implications, and our modelling demonstrates that it is an emergent property of the physics of muscle contraction.