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Understanding how muscles use energy is essential for elucidating the role of skeletal muscle in animal locomotion. Yet, experimental measures of in vivo muscle energetics are challenging to obtain, so physiologically-based muscle models are often used to estimate energy use. These predictions of individual muscle energy expenditure are not often compared to indirect whole-body measures of energetic cost. Here, we examined and illustrated the capability of physiologically-based muscle models to predict in vivo measures of energy use, which rely on fundamental relationships between muscle mechanical state and energy consumption. To improve model predictions and ensure a physiological basis for model parameters, we refined our model to include data from isolated muscle experiments and account for inefficiencies in ATP recovery processes. Simulations were performed to capture three different experimental protocols, which involved varying contraction frequency, duty cycle, and muscle fascicle length. Our results demonstrated the ability of the model to capture the dependence of energetic cost on mechanical state across contractile conditions, but tended to under predict the magnitude of energetic cost. Our analysis revealed that the model was most sensitive to the force-velocity parameters and the data informing the energetic parameters when predicting in vivo energetic rates. This work highlights it is the mechanics of skeletal muscle contraction that govern muscle energy use, although the precise physiological parameters for human muscle likely require detailed investigation., (© 2025. Published by The Company of Biologists.)

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., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2025. Published by The Company of Biologists.)

Cerebral palsy results from an upper motor neuron lesion and significantly affects skeletal muscle stiffness. The increased stiffness that occurs is partly a result of changes in the microstructural components of muscle. In particular, alterations in extracellular matrix, sarcomere length, fibre diameter, and fat content have been reported; however, experimental studies have shown wide variability in the degree of alteration. Many studies have reported changes in the extracellular matrix, while others have reported no differences. A consistent finding is increased sarcomere length in cerebral palsy affected muscle. Often many components are altered simultaneously, making it difficult to determine the individual effects on muscle stiffness. In this study, we use a three dimensional modelling approach to isolate individual effects of microstructural alterations typically occurring due to cerebral palsy on whole muscle behaviour; in particular, the effects of extracellular matrix volume fraction, stiffness, and sarcomere length. Causation between the changes to the microstructure and the overall muscle response is difficult to determine experimentally, since components of muscle cannot be manipulated individually; however, utilising a modelling approach allows greater control over each factor. We find that extracellular matrix volume fraction has the largest effect on whole muscle stiffness and mitigates effects from sarcomere length., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Konno, Nigam, Wakeling and Ross.)

Skeletal muscle tissue has a highly complex and heterogeneous structure comprising several physical length scales. In the simplest model of muscle tissue, it can be represented as a one dimensional nonlinear spring in the direction of muscle fibres. However, at the finest level, muscle tissue includes a complex network of collagen fibres, actin and myosin proteins, and other cellular materials. This study shall derive an intermediate physical model which encapsulates the major contributions of the muscle components to the elastic response apart from activation-related along-fibre responses. The micro-mechanical factors in skeletal muscle tissue (eg. connective tissue, fluid, and fibres) can be homogenized into one material aggregate that will capture the behaviour of the combination of material components. In order to do this, the corresponding volume fractions for each type of material need to be determined by comparing the stress-strain relationship for a volume containing each material. This results in a model that accounts for the micro-mechanical features found in muscle and can therefore be used to analyze effects of neuro-muscular diseases such as cerebral palsy or muscular dystrophies. The purpose of this study is to construct a model of muscle tissue that, through choosing the correct material parameters based on experimental data, will accurately capture the mechanical behaviour of whole muscle. This model is then used to look at the impacts of the bulk modulus and material parameters on muscle deformation and strain energy-density distributions., Competing Interests: The authors have declared that no competing interests exist.