Computational modelling of muscle fibre operating ranges in the hindlimb of a small ground bird (Eudromia elegans), with implications for modelling locomotion in extinct species

Author summary The structure and behaviour of individual muscles greatly influence an animal's ability to move and perform tasks. Experimental investigation of how muscles function within a living animal can be difficult, providing insight on limited aspects for few muscles. Computer models of the musculoskeletal system can partly overcome this challenge, and provide valuable insight into features not easily (if at all) measurable in experiments alone. Here a detailed three-dimensional musculoskeletal model of the hindlimb of a small ground bird, a tinamou, is combined with experimental motion and force data for walking and running, and used to explore muscle function during these gaits. Feeding experimental data into the model, a simulation is used to estimate muscle activity, and the pattern of change in their constituent fibres. Fibre length change is an important determinant of muscle function because the amount of force that can be produced varies with the amount and rate of contraction or stretch. For the first time, patterns of fibre length change in every key muscle of the bird hindlimb have been studied, broadening understanding of muscle function across the diversity of modern animals. The results also have bearing on how muscle function is reconstructed for extinct animals (e.g., dinosaurs). The arrangement and physiology of muscle fibres can strongly influence musculoskeletal function and whole-organismal performance. However, experimental investigation of muscle function during in vivo activity is typically limited to relatively few muscles in a given system. Computational models and simulations of the musculoskeletal system can partly overcome these limitations, by exploring the dynamics of muscles, tendons and other tissues in a robust and quantitative fashion. Here, a high-fidelity, 26-degree-of-freedom musculoskeletal model was developed of the hindlimb of a small ground bird, the elegant-crested tinamou (Eudromia elegans, similar to 550 g), including all the major muscles of the limb (36 actuators per leg). The model was integrated with biplanar fluoroscopy (XROMM) and forceplate data for walking and running, where dynamic optimization was used to estimate muscle excitations and fibre length changes throughout both gaits. Following this, a series of static simulations over the total range of physiological limb postures were performed, to circumscribe the bounds of possible variation in fibre length. During gait, fibre lengths for all muscles remained between 0.5 to 1.21 times optimal fibre length, but operated mostly on the ascending limb and plateau of the active force-length curve, a result that parallels previous experimental findings for birds, humans and other species. However, the ranges of fibre length varied considerably among individual muscles, especially when considered across the total possible range of joint excursion. Net length change of muscle-tendon units was mostly less than optimal fibre length, sometimes markedly so, suggesting that approaches that use muscle-tendon length change to estimate optimal fibre length in extinct species are likely underestimating this important parameter for many muscles. The results of this study clarify and broaden understanding of muscle function in extant animals, and can help refine approaches used to study extinct species.

Automated summary

This study combined a detailed musculoskeletal model of a small ground bird's hindlimb with experimental motion and force data to explore muscle function during walking and running. The results provided insights into muscle function across different muscles and can help refine approaches used to study extinct species. Computational models like this one can be useful in understanding musculoskeletal function and whole-organismal performance.