Concurrent adaptation of force and impedance in the redundant muscle system

This article examines the validity of a model to explain how humans learn to perform movements in environments with novel dynamics, including unstable dynamics typical of tool use. In this model, a simple rule specifies how the activation of each muscle is adapted from one movement to the next. Simulations of multijoint arm movements with a neuromuscular plant that incorporates neural delays, reflexes, and signal-dependent noise, demonstrate that the controller is able to compensate for changing internal or environment dynamics and noise properties. The computational model adapts by learning both the appropriate forces and required limb impedance to compensate precisely for forces and instabilities in arbitrary directions with patterns similar to those observed in motor learning experiments. It learns to regulate reciprocal activation and co-activation in a redundant muscle system during repeated movements without requiring any explicit transformation from hand to muscle space. Independent error-driven change in the activation of each muscle results in a coordinated control of the redundant muscle system and in a behavior that reduces instability, systematic error, and energy.

[1]  Weiping Li,et al.  Applied Nonlinear Control , 1991 .

[2]  R. R. Carter,et al.  Stiffness regulation by reflex action in the normal human hand. , 1990, Journal of neurophysiology.

[3]  Etienne Burdet,et al.  Quantization of human motions and learning of accurate movements , 1998, Biological Cybernetics.

[4]  A. Kacelnik,et al.  Shaping of Hooks in New Caledonian Crows , 2002, Science.

[5]  David E Vaillancourt,et al.  Effects of aging on the regularity of physiological tremor. , 2005, Journal of neurophysiology.

[6]  Rieko Osu,et al.  Endpoint Stiffness of the Arm Is Directionally Tuned to Instability in the Environment , 2007, The Journal of Neuroscience.

[7]  Karl M. Newell,et al.  Aging, Complexity, and Motor Performance , 2006 .

[8]  Rieko Osu,et al.  CNS Learns Stable, Accurate, and Efficient Movements Using a Simple Algorithm , 2008, The Journal of Neuroscience.

[9]  H. Gomi,et al.  Task-Dependent Viscoelasticity of Human Multijoint Arm and Its Spatial Characteristics for Interaction with Environments , 1998, The Journal of Neuroscience.

[10]  Michael I. Jordan,et al.  Smoothness maximization along a predefined path accurately predicts the speed profiles of complex arm movements. , 1998, Journal of neurophysiology.

[11]  K. An,et al.  Shoulder muscle moment arms during horizontal flexion and elevation. , 1997, Journal of shoulder and elbow surgery.

[12]  R A Scheidt,et al.  Persistence of motor adaptation during constrained, multi-joint, arm movements. , 2000, Journal of neurophysiology.

[13]  M. Kawato,et al.  Impedance control balances stability with metabolically costly muscle activation. , 2004, Journal of neurophysiology.

[14]  Evert-Jan Nijhof,et al.  Simulation of Multijoint Arm Movements , 2000 .

[15]  Keng Peng Tee,et al.  A model of force and impedance in human arm movements , 2004, Biological Cybernetics.

[16]  Rieko Osu,et al.  The central nervous system stabilizes unstable dynamics by learning optimal impedance , 2001, Nature.

[17]  Zeungnam Bien,et al.  Iterative learning control: analysis, design, integration and applications , 1998 .

[18]  Masazumi Katayama,et al.  Virtual trajectory and stiffness ellipse during multijoint arm movement predicted by neural inverse models , 1993, Biological Cybernetics.

[19]  M. Taussig The Nervous System , 1991 .

[20]  Rieko Osu,et al.  Different mechanisms involved in adaptation to stable and unstable dynamics. , 2003, Journal of neurophysiology.

[21]  Michael I. Jordan,et al.  Optimal feedback control as a theory of motor coordination , 2002, Nature Neuroscience.

[22]  Reza Shadmehr,et al.  Quantifying Generalization from Trial-by-Trial Behavior of Adaptive Systems that Learn with Basis Functions: Theory and Experiments in Human Motor Control , 2003, The Journal of Neuroscience.

[23]  Sybert H. Stroeve,et al.  Impedance characteristics of a neuromusculoskeletal model of the human arm II. Movement control , 1999, Biological Cybernetics.

[24]  David J. Ostry,et al.  Compensation for loads during arm movements using equilibrium-point control , 2000, Experimental Brain Research.

[25]  M. Arbib,et al.  Role of the cerebellum in reaching movements in humans. II. A neural model of the intermediate cerebellum , 1998, The European journal of neuroscience.

[26]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[27]  Raul Benitez,et al.  Motor adaptation as a greedy optimization of error and effort. , 2007, Journal of neurophysiology.

[28]  W. Rymer,et al.  Muscle stiffness during transient and continuous movements of cat muscle: perturbation characteristics and physiological relevance , 1994, IEEE Transactions on Biomedical Engineering.

[29]  M. Kawato,et al.  A hierarchical neural-network model for control and learning of voluntary movement , 2004, Biological Cybernetics.

[30]  K. Newell,et al.  Noise, information transmission, and force variability. , 1999, Journal of experimental psychology. Human perception and performance.

[31]  Maura Casadio,et al.  Force field compensation can be learned without proprioceptive error , 2009 .

[32]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Denise C. Park,et al.  Handbook of the Psychology of Aging , 1979 .

[34]  Jian-Xin Xu,et al.  Iterative Learning Control , 1998 .

[35]  Reza Shadmehr,et al.  Motor Adaptation as a Process of Reoptimization , 2008, The Journal of Neuroscience.

[36]  M. Kawato,et al.  Functional significance of stiffness in adaptation of multijoint arm movements to stable and unstable dynamics , 2003, Experimental Brain Research.

[37]  Sybert H. Stroeve,et al.  Impedance characteristics of a neuromusculoskeletal model of the human arm I. Posture control , 1999, Biological Cybernetics.

[38]  I. Hunter,et al.  Dynamics of human ankle stiffness: variation with mean ankle torque. , 1982, Journal of biomechanics.

[39]  S. Delp,et al.  Variation of muscle moment arms with elbow and forearm position. , 1995, Journal of biomechanics.

[40]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[41]  Etienne Burdet,et al.  Experimental evaluation of nonlinear adaptive controllers , 1998 .

[42]  M. Kawato,et al.  Visual Feedback Is Not Necessary for the Learning of Novel Dynamics , 2007, PloS one.

[43]  R. Meir,et al.  Explaining patterns of neural activity in the primary motor cortex using spinal cord and limb biomechanics models. , 2007, Journal of neurophysiology.

[44]  Peter J. Beek,et al.  Can co-activation reduce kinematic variability? A simulation study , 2005, Biological Cybernetics.

[45]  Kurt A. Thoroughman,et al.  Rapid Reshaping of Human Motor Generalization , 2005, The Journal of Neuroscience.

[46]  Iven M. Y. Mareels,et al.  Stability and motor adaptation in human arm movements , 2005, Biological Cybernetics.

[47]  Emmanuel Guigon,et al.  Computational Motor Control : Redundancy and Invariance , 2007 .

[48]  Reza Shadmehr,et al.  Learning of action through adaptive combination of motor primitives , 2000, Nature.

[49]  M. Kawato,et al.  Optimal impedance control for task achievement in the presence of signal-dependent noise. , 2004, Journal of neurophysiology.

[50]  Peter M. H. Rack,et al.  Limitations of Somatosensory Feedback in Control of Posture and Movement , 2011 .

[51]  F B de Waal,et al.  Cultural primatology comes of age , 1999, Nature.

[52]  David W Franklin,et al.  Impedance control and internal model use during the initial stage of adaptation to novel dynamics in humans , 2005, The Journal of physiology.

[53]  M. Kawato,et al.  Adaptation to Stable and Unstable Dynamics Achieved By Combined Impedance Control and Inverse Dynamics Model , 2003 .