Human Leg Model Predicts Ankle Muscle-Tendon Morphology, State, Roles and Energetics in Walking

Abstract

A common feature in biological neuromuscular systems is the redundancy in joint actuation. Understanding how these redundancies are resolved in typical joint movements has been a long-standing problem in biomechanics, neuroscience and prosthetics. Many empirical studies have uncovered neural, mechanical and energetic aspects of how humans resolve these degrees of freedom to actuate leg joints for common tasks like walking. However, a unifying theoretical framework that explains the many independent empirical observations and predicts individual muscle and tendon contributions to joint actuation is yet to be established. Here we develop a computational framework to address how the ankle joint actuation problem is resolved by the neuromuscular system in walking. Our framework is founded upon the proposal that a consideration of both neural control and leg muscle-tendon morphology is critical to obtain predictive, mechanistic insight into individual muscle and tendon contributions to joint actuation. We examine kinetic, kinematic and electromyographic data from healthy walking subjects to find that human leg muscle-tendon morphology and neural activations enable a metabolically optimal realization of biological ankle mechanics in walking. This optimal realization (a) corresponds to independent empirical observations of operation and performance of the soleus and gastrocnemius muscles, (b) gives rise to an efficient load-sharing amongst ankle muscle-tendon units and (c) causes soleus and gastrocnemius muscle fibers to take on distinct mechanical roles of force generation and power production at the end of stance phase in walking. The framework outlined here suggests that the dynamical interplay between leg structure and neural control may be key to the high walking economy of humans, and has implications as a means to obtain insight into empirically inaccessible features of individual muscle and tendons in biomechanical tasks. Biological neuromuscular systems are generally able to perform a specified movement task in several ways – as they have significantly more degrees of freedom than mechanical constraints. Understanding how humans resolve these redundancies to drive individual muscles and tendons in typical joint movements is of interest in the fields of biomechanics, neuroscience and prosthetics. Many experimental studies have uncovered neural, mechanical and energetic features of individual muscle and tendon function in common tasks like walking and running. However, a unifying theoretical framework that explains the many independent empirical observations is yet to be established. In this work, we show that leg muscle-tendon morphology and neural co-ordination, together, enable efficient ankle movements in walking. This finding provides quantitative insight into the operation and performance of posterior-leg muscles and tendons in walking, and motivates the idea that different muscle-tendon units take on different mechanical roles to best actuate the ankle in gait. Results reported have implications both for better understanding neuromuscular co-ordination in gait, and for the design of lower limb prosthetic and orthotic technologies.