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Plos Computational Biology

Publication date: 2022-06-01
Volume: 18
Publisher: Public Library of Science (PLoS)

Author:

Wouwe, Tom Van
Ting, Lena H ; De Groote, Friedl

Keywords:

Science & Technology, Life Sciences & Biomedicine, Biochemical Research Methods, Mathematical & Computational Biology, Biochemistry & Molecular Biology, OPTIMAL FEEDBACK-CONTROL, SIGNAL-DEPENDENT NOISE, SHORT-RANGE STIFFNESS, END-POINT STIFFNESS, SENSORY INTEGRATION, TIBIALIS ANTERIOR, UNSTABLE DYNAMICS, IMPEDANCE CONTROL, MOTOR CONTROL, MUSCLE, Computer Simulation, Humans, Models, Biological, Movement, Muscle Contraction, Muscles, Postural Balance, 01 Mathematical Sciences, 06 Biological Sciences, 08 Information and Computing Sciences, Bioinformatics

Abstract:

Optimal control simulations have shown that both musculoskeletal dynamics and physiological noise are important determinants of movement. However, due to the limited efficiency of available computational tools, deterministic simulations of movement focus on accurately modelling the musculoskeletal system while neglecting physiological noise, and stochastic simulations account for noise while simplifying the dynamics. We took advantage of recent approaches where stochastic optimal control problems are approximated using deterministic optimal control problems, which can be solved efficiently using direct collocation. We were thus able to extend predictions of stochastic optimal control as a theory of motor coordination to include muscle coordination and movement patterns emerging from non-linear musculoskeletal dynamics. In stochastic optimal control simulations of human standing balance, we demonstrated that the inclusion of muscle dynamics can predict muscle co-contraction as minimal effort strategy that complements sensorimotor feedback control in the presence of sensory noise. In simulations of reaching, we demonstrated that nonlinear multi-segment musculoskeletal dynamics enables complex perturbed and unperturbed reach trajectories under a variety of task conditions to be predicted. In both behaviors, we demonstrated how interactions between task constraint, sensory noise, and the intrinsic properties of muscle influence optimal muscle coordination patterns, including muscle co-contraction, and the resulting movement trajectories. Our approach enables a true minimum effort solution to be identified as task constraints, such as movement accuracy, can be explicitly imposed, rather than being approximated using penalty terms in the cost function. Our approximate stochastic optimal control framework predicts complex features, not captured by previous simulation approaches, providing a generalizable and valuable tool to study how musculoskeletal dynamics and physiological noise may alter neural control of movement in both healthy and pathological movements.