Insights into muscle metabolic energetics: Modelling muscle-tendon mechanics and metabolic rates during walking across speeds

Abstract

Prior studies have produced models to predict metabolic rates based on experimental observations of isolated muscle contraction from various species. Such models can provide reliable predictions of metabolic rates in humans if muscle properties and control are accurately modeled. This study aimed to examine how muscle-tendon model calibration and metabolic energy models influenced estimation of muscle-tendon states and time-series metabolic rates, to evaluate the agreement with empirical data, and to provide predictions of the metabolic rate of muscle groups and gait phases across walking speeds. Three-dimensional musculoskeletal simulations with prescribed kinematics and dynamics were performed. An optimal control formulation was used to compute muscle-tendon states with four levels of individualization, ranging from a scaled generic model and muscle controls based on minimal activations, to calibration of passive muscle forces, personalization of Achilles and quadriceps tendon stiffnesses, to finally informing muscle controls with electromyography. We computed metabolic rates based on existing models. Simulations with calibrated passive forces and personalized tendon stiffness most accurately estimate muscle excitations and fiber lengths. Interestingly, the inclusion of electromyography did not improve our estimates. The whole-body average metabolic cost was better estimated using Bhargava et al. 2004 and Umberger 2010 models. We estimated metabolic rate peaks near early stance, pre-swing, and initial swing at all walking speeds. Plantarflexors accounted for the highest cost among muscle groups at the preferred speed and was similar to the cost of hip adductors and abductors combined. Also, the swing phase accounted for slightly more than one-quarter of the total cost in a gait cycle, and its relative cost decreased with walking speed.