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Stochastic optimal open-loop control as a theory of force and impedance planning via muscle co-contraction

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  • Bastien Berret
  • Frédéric Jean

Abstract

Understanding the underpinnings of biological motor control is an important issue in movement neuroscience. Optimal control theory is a leading framework to rationalize this problem in computational terms. Previously, optimal control models have been devised either in deterministic or in stochastic settings to account for different aspects of motor control (e.g. average behavior versus trial-to-trial variability). While these approaches have yielded valuable insights about motor control, they typically fail in explaining muscle co-contraction. Co-contraction of a group of muscles associated to a motor function (e.g. agonist and antagonist muscles spanning a joint) contributes to modulate the mechanical impedance of the neuromusculoskeletal system (e.g. joint viscoelasticity) and is thought to be mainly under the influence of descending signals from the brain. Here we present a theory suggesting that one primary goal of motor planning may be to issue feedforward (open-loop) motor commands that optimally specify both force and impedance, according to noisy neuromusculoskeletal dynamics and to optimality criteria based on effort and variance. We show that the proposed framework naturally accounts for several previous experimental findings regarding the regulation of force and impedance via muscle co-contraction in the upper-limb. Stochastic optimal (closed-loop) control, preprogramming feedback gains but requiring on-line state estimation processes through long-latency sensory feedback loops, may then complement this nominal feedforward motor command to fully determine the limb’s mechanical impedance. The proposed stochastic optimal open-loop control theory may provide new insights about the general articulation of feedforward/feedback control mechanisms and justify the occurrence of muscle co-contraction in the neural control of movement.Author summary: This study presents a novel computational theory to explain the planning of force and impedance (e.g. viscoelasticity) in the neural control of movement. It assumes that one main goal of motor planning is to elaborate feedforward motor commands that determine both the force and the impedance required for the task at hand. These feedforward motor commands (i.e. that are defined prior to movement execution) are designed to minimize effort and variance costs considering the uncertainty arising from sensorimotor or environmental noise. A major outcome of this mathematical framework is the explanation of muscle co-contraction (i.e. the concurrent contraction of a group of muscles involved in a motor function). Muscle co-contraction has been shown to occur in many situations but previous modeling works struggled to account for it. Although effortful, co-contraction contributes to increase the robustness of motor behavior (e.g. small variance) upstream of sophisticated optimal closed-loop control processes that require state estimation from delayed sensory feedback to function. This work may have implications regarding our understanding of the neural control of movement in computational terms. It also provides a theoretical ground to explain how to optimally plan force and impedance within a general and versatile framework.

Suggested Citation

  • Bastien Berret & Frédéric Jean, 2020. "Stochastic optimal open-loop control as a theory of force and impedance planning via muscle co-contraction," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-28, February.
  • Handle: RePEc:plo:pcbi00:1007414
    DOI: 10.1371/journal.pcbi.1007414
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    References listed on IDEAS

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    1. Paul T E Cusack, 2020. "The Human Brain," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(3), pages 24261-24266, October.
    2. Christopher M. Harris & Daniel M. Wolpert, 1998. "Signal-dependent noise determines motor planning," Nature, Nature, vol. 394(6695), pages 780-784, August.
    3. Sang-Hoon Yeo & David W Franklin & Daniel M Wolpert, 2016. "When Optimal Feedback Control Is Not Enough: Feedforward Strategies Are Required for Optimal Control with Active Sensing," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-22, December.
    4. Etienne Burdet & Rieko Osu & David W. Franklin & Theodore E. Milner & Mitsuo Kawato, 2001. "The central nervous system stabilizes unstable dynamics by learning optimal impedance," Nature, Nature, vol. 414(6862), pages 446-449, November.
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    1. Bastien Berret & Adrien Conessa & Nicolas Schweighofer & Etienne Burdet, 2021. "Stochastic optimal feedforward-feedback control determines timing and variability of arm movements with or without vision," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-24, June.

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