Abstract
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, ~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.
Highlights
The ultimate driver of almost all vertebrate movement is skeletal muscle [1,2]
Almost all tuning factors in the optimal solution exceeded one (Fig 3), indicating that most muscle–tendon unit (MTU) needed both lo and LS to be increased from their original values (Table 2)
Many MTUs only required a level of tuning well within the scope of variation due to either measurement error or genuine intra- or inter-individual variation
Summary
The ultimate driver of almost all vertebrate movement is skeletal muscle [1,2]. Spanning from one bone to another, the contractile force of a muscle–often delivered via in-series tendon– exerts a moment (rotational force) about one or more joints, effecting movement. [3], only in the past half a century has the highly complex behaviour of skeletal muscle and tendon in relation to whole-organism biomechanics become increasingly appreciated. Much of this advancement in understanding has been due to the use of various forms of lumpedparameter models based on the pioneering work of Hill [4], which emphasize the contributions of both active and passive components to force production, and how these are modulated by the degree and rate of muscle shortening or lengthening [1,5,6,7]. Computational models of the musculoskeletal system using Hill-type models of muscle contraction have proven as valuable tools to investigating the complex, highly dimensional and highly nonlinear ways in which muscles help coordinate steady and unsteady movement in various species [14,15,16,17,18], and how these can vary in abnormal conditions such as pathology [19,20,21,22]
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