Stabilisation of walking by intrinsic muscle properties revealed in a three-dimensional muscle-driven simulation

Abstract

A fundamental question in movement science is how humans perform stable movements in the presence of disturbances such as contact with objects. It remains unclear how the nervous system, with delayed responses to disturbances, maintains the stability of complex movements. We hypothesised that intrinsic muscle properties (i.e. the force–length–velocity properties of muscle fibres and tendon elasticity) may help stabilise human walking by responding instantaneously to a disturbance and providing forces that help maintain the movement trajectory. To investigate this issue, we generated a 3D muscle-driven simulation of walking and analysed the changes in the simulation's motion when a disturbance was applied to models with and without intrinsic muscle properties. Removing the intrinsic properties reduced the stability; this was true when the disturbing force was applied at a variety of times and in different directions. Thus, intrinsic muscle properties play a unique role in stabilising walking, complementing the delayed response of the central nervous system.

Keywords:

• biomechanics
• simulation
• muscle
• walking
• stability

Acknowledgements

We thank Ayman Habib, Ajay Seth, Jeffrey Reinbolt, Peter Loan, Samuel Hamner, May Liu, Michael Schwartz, Allison Arnold, Darryl Thelen and Melanie Fox for feedback and assistance. We also thank Eran Guendelman for processing motion capture data and scaling the musculoskeletal model used in this study and Yuri Ivanenko for providing the EMG data from Cappellini et al. (2006). This work was funded by the Achievement Rewards for College Scientists Foundation and by the National Institutes of Health through the Roadmap for Medical Research U54 GM072970, NIH R01 NS55380, NIH R01 HD033929 and NIH GM63495.