Superposition and modulation of muscle synergies for reaching in response to a change in target location.

We have recently shown that the muscle patterns for reaching are well described by the combination of a few time-varying muscle synergies supporting the notion of a modular architecture for arm control. Here we investigated whether the muscle patterns for reaching movements involving online corrections are also generated by the combination of the same set of time-varying muscle synergies used for point-to-point movements. We recorded endpoint kinematics and EMGs from up to 16 arm muscles of 5 subjects reaching from a central location to 8 peripheral targets in the frontal plane, from each peripheral target to 1 of the 2 adjacent targets, and from the central location initially to 1 peripheral target and, after a delay of either 50, 150, or 250 ms from the go signal, to 1 of the 2 adjacent targets. Time-varying muscle synergies were extracted from the averaged, phasic, normalized EMGs of point-to-point movements and fit to the patterns of target change movements using an iterative optimization algorithm. In all subjects, three time-varying muscle synergies explained a large fraction of the data variation of point-to-point movements. The superposition and modulation of the same three synergies reconstructed the muscle patterns for target change movements better than the superposition and modulation of the corresponding point-to-point muscle patterns, appropriately aligned. While at the kinematic level the corrective trajectory for reaching during a change in target location can be obtained by the delayed superposition of the trajectory from the initial to the final target, at the muscle level the underlying phasic muscle patterns are captured by the amplitude and timing modulation of the same time-varying muscle synergies recruited for point-to-point movements. These results suggest that a common modular architecture is used for the control of unperturbed arm movement and for its visually guided online corrections.

[1]  B. Day,et al.  Voluntary modification of automatic arm movements evoked by motion of a visual target , 1999, Experimental Brain Research.

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

[3]  Emanuel Todorov,et al.  Structured variability of muscle activations supports the minimal intervention principle of motor control. , 2009, Journal of neurophysiology.

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

[5]  C. C. A. M. Gielen,et al.  Motor programmes for goal-directed movements are continuously adjusted according to changes in target location , 2004, Experimental Brain Research.

[6]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[7]  A B Ajiboye,et al.  Muscle synergies as a predictive framework for the EMG patterns of new hand postures , 2009, Journal of neural engineering.

[8]  E. Megaw Possible modification to a rapid on-going programmed manual response. , 1974, Brain research.

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

[10]  M. Flanders,et al.  Timing of muscle activation in a hand movement sequence. , 2006, Cerebral cortex.

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

[12]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[13]  Stacie A. Chvatal,et al.  Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. , 2011, Journal of neurophysiology.

[14]  M. Desmurget,et al.  An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia , 2000, Nature Neuroscience.

[15]  M. Lemay,et al.  Modularity of motor output evoked by intraspinal microstimulation in cats. , 2004, Journal of neurophysiology.

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

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

[18]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

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

[20]  J. Kalaska,et al.  Sequential activation of muscle synergies during locomotion in the intact cat as revealed by cluster analysis and direct decomposition. , 2006, Journal of neurophysiology.

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

[22]  J. F. Soechting,et al.  Modification of trajectory of a pointing movement in response to a change in target location. , 1983, Journal of neurophysiology.

[23]  R. Caminiti,et al.  Cortical mechanisms for online control of hand movement trajectory: the role of the posterior parietal cortex. , 2009, Cerebral cortex.

[24]  Christian Ethier,et al.  Linear Summation of Cat Motor Cortex Outputs , 2006, The Journal of Neuroscience.

[25]  P. Morasso,et al.  Trajectory formation and handwriting: A computational model , 1982, Biological Cybernetics.

[26]  Lena H Ting,et al.  Subject-specific muscle synergies in human balance control are consistent across different biomechanical contexts. , 2010, Journal of neurophysiology.

[27]  T. Milner,et al.  A model for the generation of movements requiring endpoint precision , 1992, Neuroscience.

[28]  W. Rymer,et al.  Endpoint force fluctuations reveal flexible rather than synergistic patterns of muscle cooperation. , 2008, Journal of neurophysiology.

[29]  J. Vercher,et al.  Target and hand position information in the online control of goal-directed arm movements , 2003, Experimental Brain Research.

[30]  E. R. Crossman,et al.  Feedback Control of Hand-Movement and Fitts' Law , 1983, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[31]  J. T. Massey,et al.  Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. , 1981, Journal of neurophysiology.

[32]  Lilian Fautrelle,et al.  Muscular synergies during motor corrections: Investigation of the latencies of muscle activities , 2010, Behavioural Brain Research.

[33]  W J Kargo,et al.  Rapid Correction of Aimed Movements by Summation of Force-Field Primitives , 2000, The Journal of Neuroscience.

[34]  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.

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

[36]  Dario Farina,et al.  Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane. , 2010, Journal of neurophysiology.

[37]  C. Gielen,et al.  Modification of muscle activation patterns during fast goal-directed arm movements. , 1984, Journal of motor behavior.

[38]  R A Abrams,et al.  Optimality in human motor performance: ideal control of rapid aimed movements. , 1988, Psychological review.

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

[40]  C. Bard,et al.  Control of Rapid Arm Movements When Target Position Is Altered During Saccadic Suppression. , 1995, Journal of motor behavior.

[41]  Martha Flanders,et al.  Muscular and postural synergies of the human hand. , 2004, Journal of neurophysiology.

[42]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 2004, Experimental Brain Research.

[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]  J F Kalaska,et al.  Integration of predictive feedforward and sensory feedback signals for online control of visually guided movement. , 2009, Journal of neurophysiology.

[45]  F. P. Kendall,et al.  Muscles: Testing and Function, with Posture and Pain , 1993 .

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

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

[48]  Konrad Paul Kording,et al.  Relevance of error: what drives motor adaptation? , 2009, Journal of neurophysiology.

[49]  J. Saunders,et al.  Humans use continuous visual feedback from the hand to control fast reaching movements , 2003, Experimental Brain Research.

[50]  Emanuel Todorov,et al.  Evidence for the Flexible Sensorimotor Strategies Predicted by Optimal Feedback Control , 2007, The Journal of Neuroscience.

[51]  T. Milner,et al.  The effect of accuracy constraints on three-dimensional movement kinematics , 1990, Neuroscience.

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

[53]  Scott T. Grafton,et al.  Updating target location at the end of an orienting saccade affects the characteristics of simple point-to-point movements. , 2005, Journal of experimental psychology. Human perception and performance.

[54]  L. Miller,et al.  Primary motor cortical neurons encode functional muscle synergies , 2002, Experimental Brain Research.

[55]  J. Houk,et al.  Deciding when and how to correct a movement: discrete submovements as a decision making process , 2007, Experimental Brain Research.

[56]  Joseph Classen,et al.  Modular Organization of Finger Movements by the Human Central Nervous System , 2006, Neuron.

[57]  L. Carlton Processing visual feedback information for movement control. , 1981, Journal of experimental psychology. Human perception and performance.

[58]  K. E. Novak,et al.  The use of overlapping submovements in the control of rapid hand movements , 2002, Experimental Brain Research.

[59]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[60]  F. A. Mussa-lvaldi,et al.  Convergent force fields organized in the frog's spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

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

[63]  Emilio Bizzi,et al.  Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. , 2009, Journal of neurophysiology.

[64]  Francesco Lacquaniti,et al.  Modular Control of Limb Movements during Human Locomotion , 2007, The Journal of Neuroscience.

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

[66]  Simone Ferrari-Toniolo,et al.  Online Control of Hand Trajectory and Evolution of Motor Intention in the Parietofrontal System , 2011, The Journal of Neuroscience.

[67]  R N Lemon,et al.  A novel algorithm to remove electrical cross‐talk between surface EMG recordings and its application to the measurement of short‐term synchronisation in humans , 2002, The Journal of physiology.

[68]  R. Miall,et al.  Intermittency in human manual tracking tasks. , 1993, Journal of motor behavior.

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

[70]  Daeyeol Lee,et al.  Manual interception of moving targets II. On-line control of overlapping submovements , 1997, Experimental Brain Research.

[71]  C. Prablanc,et al.  Automatic control during hand reaching at undetected two-dimensional target displacements. , 1992, Journal of neurophysiology.

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

[73]  N. Hogan,et al.  Quantization of continuous arm movements in humans with brain injury. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[75]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

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

[77]  E. Bizzi,et al.  Modules in the brain stem and spinal cord underlying motor behaviors. , 2011, Journal of neurophysiology.

[78]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[79]  Tamar Flash,et al.  Mechanisms underlying the generation of averaged modified trajectories , 1995, Biological Cybernetics.

[80]  C. Prablanc,et al.  Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement , 1986, Nature.