Integrating muscle energetics into biomechanical models to understand variance in the cost of movement

In this Review, we explore the state of the art of biomechanical models for estimating energy consumption during terrestrial locomotion. We consider different mechanical models that provide a solid framework to understand movement energetics from the perspective of force and work requirements. Whilst such models are highly informative, they lack specificity for predicting absolute metabolic rates across a range of species or variations in movement patterns. Muscles consume energy when they activate to generate tension, as well as when they shorten to generate positive work. Phenomenological muscle models incorporating steady-state parameters have been developed and are able to reproduce how muscle fibre energy consumption changes under different contractile conditions; however, such models are difficult to validate when scaled up to whole muscle. This is, in part, owing to limited availability of data that relate muscle dynamics to energetic rates during contraction of large mammalian muscles. Furthermore, factors including the compliance of tendinous tissue, dynamic shape changes and motor unit recruitment can alter the dynamics of muscle contractile tissue and potentially improve muscle efficiency under some locomotion conditions. Despite the many challenges, energetic cost estimates derived from musculoskeletal models that simulate muscle function required to generate movement have been shown to reasonably predict changes in human metabolic rates under different movement conditions. However, accurate predictions of absolute metabolic rate are still elusive. We suggest that conceptual models may be adapted based on our understanding of muscle energetics to better predict the variance in movement energetics both within and between terrestrial species.