Beyond power limits: the kinetic energy capacity of skeletal muscle

Abstract

Muscle is the universal agent of animal movement, and limits to muscle performance are therefore an integral aspect of animal behaviour, ecology, and evolution. A mechanical perspective on movement makes it amenable to analysis from first principles, and so brings the seeming certitude of simple physical laws to the challenging comparative study of complex biological systems. Early contributions on movement biomechanics considered muscle energy output to be limited by muscle work capacity, Wmax; triggered by seminal work in the late 1960s, it is now held broadly that a complete analysis of muscle energy output is to also consider muscle power capacity, for no unit of work can be delivered in arbitrarily brief time. Here, we adopt a critical stance towards this paradigmatic notion of a power-limit, and argue that the alternative constraint to muscle energy output is instead imposed by a characteristic kinetic energy capacity, Kmax, dictated by the maximum speed with which the actuating muscle can shorten. The two critical energies can now be directly compared, and define the physiological similarity index, {Gamma} = Kmax/Wmax. It is the explanatory power of this comparison that lends weight to a shift in perspective from muscle power to kinetic energy capacity, as is argued through a series of brief illustrative examples. {Gamma} emerges as an important dimensionless number in musculoskeletal dynamics, and sparks novel hypotheses on functional adaptations in musculoskeletal "design" that depart from the parsimonious evolutionary null hypothesis of geometric similarity.