Unconstrained muscle-tendon workloops indicate resonance tuning as a mechanism for elastic limb behavior during terrestrial locomotion
Edited by Andrew A. Biewener, Harvard University, Bedford, MA, and accepted by the Editorial Board September 3, 2015 (received for review January 26, 2015)
Significance
The fields of terrestrial biomechanics and bio-inspired robotics have identified spring-like limb mechanics as critical to stable and efficient gait. In biological systems, distal muscle groups cycling large amounts of energy in series tendons are a primary source of compliance. To investigate the origins of this behavior, we coupled a biological muscle-tendon to a feedback controlled servomotor simulating the inertial/gravitational environment of terrestrial gait. We drove this bio-robotic system via direct nerve stimulation across a range of frequencies to explore the influence of neural control on muscle-tendon interactions. This study concluded that by matching stimulation frequency to that of the passive biomechanical system, muscle-tendon interactions resulting in spring-like behavior occur naturally and do not require closed-loop neural control.
Abstract
In terrestrial locomotion, there is a missing link between observed spring-like limb mechanics and the physiological systems driving their emergence. Previous modeling and experimental studies of bouncing gait (e.g., walking, running, hopping) identified muscle-tendon interactions that cycle large amounts of energy in series tendon as a source of elastic limb behavior. The neural, biomechanical, and environmental origins of these tuned mechanics, however, have remained elusive. To examine the dynamic interplay between these factors, we developed an experimental platform comprised of a feedback-controlled servo-motor coupled to a biological muscle-tendon. Our novel motor controller mimicked in vivo inertial/gravitational loading experienced by muscles during terrestrial locomotion, and rhythmic patterns of muscle activation were applied via stimulation of intact nerve. This approach was based on classical workloop studies, but avoided predetermined patterns of muscle strain and activation—constraints not imposed during real-world locomotion. Our unconstrained approach to position control allowed observation of emergent muscle-tendon mechanics resulting from dynamic interaction of neural control, active muscle, and system material/inertial properties. This study demonstrated that, despite the complex nonlinear nature of musculotendon systems, cyclic muscle contractions at the passive natural frequency of the underlying biomechanical system yielded maximal forces and fractions of mechanical work recovered from previously stored elastic energy in series-compliant tissues. By matching movement frequency to the natural frequency of the passive biomechanical system (i.e., resonance tuning), muscle-tendon interactions resulting in spring-like behavior emerged naturally, without closed-loop neural control. This conceptual framework may explain the basis for elastic limb behavior during terrestrial locomotion.
Acknowledgments
We thank Siddharth Vadakkeevedu for assistance with experiments. Funding for this research was supplied by the College of Engineering, North Carolina State University, and Grant 2011152 from the United States-Israel Binational Science Foundation (to G.S.S.).
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Published online: October 12, 2015
Published in issue: October 27, 2015
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Acknowledgments
We thank Siddharth Vadakkeevedu for assistance with experiments. Funding for this research was supplied by the College of Engineering, North Carolina State University, and Grant 2011152 from the United States-Israel Binational Science Foundation (to G.S.S.).
Notes
This article is a PNAS Direct Submission. A.A.B. is a guest editor invited by the Editorial Board.
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The authors declare no conflict of interest.
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Unconstrained muscle-tendon workloops indicate resonance tuning as a mechanism for elastic limb behavior during terrestrial locomotion, Proc. Natl. Acad. Sci. U.S.A.
112 (43) E5891-E5898,
https://doi.org/10.1073/pnas.1500702112
(2015).
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