Abstract
Muscles attach to bones via tendons that stretch and recoil, affecting muscle force generation and metabolic energy consumption. In this study, we investigated the effect of tendon compliance on the metabolic cost of running using a full-body musculoskeletal model with a detailed model of muscle energetics. We performed muscle-driven simulations of running at 2–5 m/s with tendon force–strain curves that produced between 1 and 10% strain when the muscles were developing maximum isometric force. We computed the average metabolic power consumed by each muscle when running at each speed and with each tendon compliance. Average whole-body metabolic power consumption increased as running speed increased, regardless of tendon compliance, and was lowest at each speed when tendon strain reached 2–3% as muscles were developing maximum isometric force. When running at 2 m/s, the soleus muscle consumed less metabolic power at high tendon compliance because the strain of the tendon allowed the muscle fibers to operate nearly isometrically during stance. In contrast, the medial and lateral gastrocnemii consumed less metabolic power at low tendon compliance because less compliant tendons allowed the muscle fibers to operate closer to their optimal lengths during stance. The software and simulations used in this study are freely available at simtk.org and enable examination of muscle energetics with unprecedented detail.
Highlights
The complexity of the human body is a byproduct of millions of years of evolution
Simulations performed by Dorn et al [23] suggest that the plantarflexors are primarily responsible for increasing running speed up to 7.0 m/s, while the hip muscles play a more substantial role above this speed. These findings suggest that the economy of running is greatly affected by the dynamics of the calcaneal tendon, and that the relative importance of this tendon to overall running economy varies with speed
We explored three hypotheses: (i) whole-body metabolic power consumption is a convex function of tendon compliance, reaching its lowest value when tendon strain is approximately 3–4% at Fmax, the range of tendon stretch suggested by Zajac [32]; (ii) for very low and very high tendon compliances, the muscles crossing the ankle experience a greater increase in metabolic power than those crossing the knee or hip; and (iii) metrics based solely on muscle activations or positive fiber mechanical power exhibit trends that are different from the predictions of a detailed muscle energetics model
Summary
The complexity of the human body is a byproduct of millions of years of evolution. Energetic requirements have increased over the course of human evolution as the hominid brain increased in size and capability [1]. We are driven to maximize energy intake and minimize energy use. It is thought that our ancestors developed hunting [2] and scavenging [3] strategies to obtain calories, and may have first adopted bipedalism in an arboreal environment to harvest fruits efficiently [4]. Humans have evolved mechanisms that decrease caloric expenditure during locomotion, adopting a bipedal gait and naturally selecting walking speeds [5, 6] and PLOS ONE | DOI:10.1371/journal.pone.0150378. Humans have evolved mechanisms that decrease caloric expenditure during locomotion, adopting a bipedal gait and naturally selecting walking speeds [5, 6] and PLOS ONE | DOI:10.1371/journal.pone.0150378 March 1, 2016
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