Abstract
Motor control comprises not only descending input from the nervous system and proprioceptive feedback, but also muscle viscoelastic properties, body dynamics, and interactions with the environment. Proprioceptive sense organs and spinal reflexes regulate muscle stiffness dynamically during perturbations. In addition to these slower acting reflexes, the nonlinear, viscoelastic behavior of muscles also provides instantaneous dynamic tuning of stiffness during load perturbations. Despite recognition of the contribution of these muscle properties to motor control, a theoretical framework that accounts for them has remained largely undeveloped. We recently proposed a novel molecular mechanism, the “winding filament” hypothesis, which accounts for the viscoelastic properties of active muscle. This hypothesis proposes that the giant, elastic titin protein is first engaged mechanically during Ca2+ activation in skeletal muscle, and the cross-bridges then wind titin on the thin filaments, storing elastic potential energy during force development. Mechanical engagement of the titin spring upon Ca2+ activation provides a mechanism by which nearly invariant contractile and viscoelastic properties can be produced regardless of the initial sarcomere length at which the muscles are activated. Winding of titin on the thin filaments with force development changes a muscle’s equilibrium position and stiffness as a function of muscle recruitment. These changes, in turn, produce forces that move the limbs to their final position regardless of unexpected perturbations. By adjusting their stiffness instantaneously to changes in load, muscles themselves control interactions between body and environment, and manage interactions between antagonistic muscles, which interact via their loads. By providing a biological mechanism for muscle intrinsic properties, the winding filament hypothesis provides inspiration for the design of a new generation of actuators and prostheses that, like muscles, will exhibit self-stabilization based on variable, nonlinear compliance.
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Acknowledgments
We thank Michael Richardson, Michael Riley, and Kevin Shockley for inviting us to participate in the symposium and for editing this book. T. Richard Nichols and Cinnamon Pace provided helpful comments on the manuscript. Our research was supported by grants IOS-0732949, IIS-0827688, and IOS-1025806 from the National Science Foundation, and by TRIF Growing Biotechnology grants from Northern Arizona University.
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Nishikawa, K.C., Monroy, J.A., Powers, K.L., Gilmore, L.A., Uyeno, T.A., Lindstedt, S.L. (2013). A Molecular Basis for Intrinsic Muscle Properties: Implications for Motor Control. In: Richardson, M., Riley, M., Shockley, K. (eds) Progress in Motor Control. Advances in Experimental Medicine and Biology, vol 782. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5465-6_6
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