Control of reaching movements by muscle synergy combinations

Controlling the movement of the arm to achieve a goal, such as reaching for an object, is challenging because it requires coordinating many muscles acting on many joints. The central nervous system (CNS) might simplify the control of reaching by directly mapping initial states and goals into muscle activations through the combination of muscle synergies, coordinated recruitment of groups of muscles with specific activation profiles. Here we review recent results from the analysis of reaching muscle patterns supporting such a control strategy. Muscle patterns for point-to-point movements can be reconstructed by the combination of a small number of time-varying muscle synergies, modulated in amplitude and timing according to movement directions and speeds. Moreover, the modulation and superposition of the synergies identified from point-to-point movements captures the muscle patterns underlying multi-phasic movements, such as reaching through a via-point or to a target whose location changes after movement initiation. Thus, the sequencing of time-varying muscle synergies might implement an intermittent controller which would allow the construction of complex movements from simple building blocks.

[1]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  E. Bizzi,et al.  The construction of movement by the spinal cord , 1999, Nature Neuroscience.

[3]  J. F. Soechting,et al.  Spatial/temporal characteristics of a motor pattern for reaching. , 1994, Journal of neurophysiology.

[4]  Francesco Lacquaniti,et al.  Modulation of phasic and tonic muscle synergies with reaching direction and speed. , 2008, Journal of neurophysiology.

[5]  Emilio Bizzi,et al.  Combinations of muscle synergies in the construction of a natural motor behavior , 2003, Nature Neuroscience.

[6]  Ashvin Shah,et al.  A computational model of muscle recruitment for wrist movements. , 2002, Journal of neurophysiology.

[7]  Francisco J. Valero Cuevas,et al.  Challenges and New Approaches to Proving the Existence of Muscle Synergies of Neural Origin , 2012, PLoS Comput. Biol..

[8]  J. F. Soechting,et al.  Invariant characteristics of a pointing movement in man , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Lena H Ting,et al.  Muscle synergy organization is robust across a variety of postural perturbations. , 2006, Journal of neurophysiology.

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

[11]  Francesco Lacquaniti,et al.  Patterned control of human locomotion , 2012, The Journal of physiology.

[12]  M. Tresch,et al.  The case for and against muscle synergies , 2022 .

[13]  P. Morasso Spatial control of arm movements , 2004, Experimental Brain Research.

[14]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

[15]  F. Lacquaniti,et al.  Coordination of Locomotion with Voluntary Movements in Humans , 2005, The Journal of Neuroscience.

[16]  Andrea d'Avella,et al.  Modularity for Sensorimotor Control: Evidence and a New Prediction , 2010, Journal of motor behavior.

[17]  S. Giszter,et al.  Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors , 2004, The Journal of Neuroscience.

[18]  T. Flash,et al.  Arm Trajectory Modifications During Reaching Towards Visual Targets , 1991, Journal of Cognitive Neuroscience.

[19]  Emanuel Todorov,et al.  Cosine Tuning Minimizes Motor Errors , 2002, Neural Computation.

[20]  F. Lacquaniti,et al.  Some factors pertinent to the organization and control of arm movements , 1982, Brain Research.

[21]  E. Bizzi,et al.  Article history: , 2005 .

[22]  Emilio Bizzi,et al.  Coordination and localization in spinal motor systems , 2002, Brain Research Reviews.

[23]  John M. Hollerbach,et al.  Dynamic interactions between limb segments during planar arm movement , 1982, Biological Cybernetics.

[24]  Simon A. Overduin,et al.  Microstimulation Activates a Handful of Muscle Synergies , 2012, Neuron.

[25]  Emilio Bizzi,et al.  Shared and specific muscle synergies in natural motor behaviors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Francesco Lacquaniti,et al.  Superposition and modulation of muscle synergies for reaching in response to a change in target location. , 2011, Journal of neurophysiology.

[28]  M. Posner,et al.  Processing of visual feedback in rapid movements. , 1968, Journal of experimental psychology.

[29]  M. Flanders Temporal patterns of muscle activation for arm movements in three- dimensional space , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Peter J. Gawthrop,et al.  Intermittent control: a computational theory of human control , 2011, Biological Cybernetics.

[31]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[32]  G. Gottlieb,et al.  Directional control of planar human arm movement. , 1997, Journal of neurophysiology.

[33]  C. Atkeson,et al.  Kinematic features of unrestrained vertical arm movements , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  L. Ting,et al.  Muscle synergies characterizing human postural responses. , 2007, Journal of neurophysiology.

[35]  Vladimir M. Zatsiorsky,et al.  Muscle synergies during shifts of the center of pressure by standing persons , 2003, Experimental Brain Research.

[36]  Andrea d'Avella,et al.  Modularity in the motor system: decomposition of muscle patterns as combinations of time-varying synergies , 2001, NIPS.

[37]  Robert Sessions Woodworth,et al.  THE ACCURACY OF VOLUNTARY MOVEMENT , 1899 .

[38]  Henrik Gollee,et al.  Human control of an inverted pendulum: Is continuous control necessary? Is intermittent control effective? Is intermittent control physiological? , 2011, The Journal of physiology.

[39]  S. Giszter,et al.  A Neural Basis for Motor Primitives in the Spinal Cord , 2010, The Journal of Neuroscience.

[40]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

[41]  M. Flanders,et al.  Basic features of phasic activation for reaching in vertical planes , 1996, Experimental Brain Research.

[42]  Lars Omlor,et al.  Anechoic Blind Source Separation Using Wigner Marginals , 2011, J. Mach. Learn. Res..

[43]  E. Bizzi,et al.  Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors , 2005, The Journal of Neuroscience.

[44]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

[45]  Lena H Ting,et al.  A limited set of muscle synergies for force control during a postural task. , 2005, Journal of neurophysiology.

[46]  J. F. Soechting,et al.  Path constraints on point-to-point arm movements in three-dimensional space , 1986, Neuroscience.

[47]  Neville Hogan,et al.  Serial processing in human movement production , 1998, Neural Networks.

[48]  E. Bizzi,et al.  Book Review: Modular Organization of Spinal Motor Systems , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[49]  Simon Giszter,et al.  Primitives, premotor drives, and pattern generation: a combined computational and neuroethological perspective. , 2007, Progress in brain research.

[50]  Lena H Ting,et al.  Neuromechanics of muscle synergies for posture and movement , 2007, Current Opinion in Neurobiology.

[51]  Simon A. Overduin,et al.  Modulation of Muscle Synergy Recruitment in Primate Grasping , 2008, The Journal of Neuroscience.