Toward a new theory of motor synergies.

Driven by recent empirical studies, we offer a new understanding of the degrees of freedom problem, and propose a refined concept of synergy as a neural organization that ensures a one-to-many mapping of variables providing for both stability of important performance variables and flexibility of motor patterns to deal with possible perturbations and/or secondary tasks. Empirical evidence is reviewed, including a discussion of the operationalization of stability/flexibility through the method of the uncontrolled manifold. We show how this concept establishes links between the various accounts for how movement is organized in redundant effector systems.

[1]  D. Sternad,et al.  Decomposition of variability in the execution of goal-oriented tasks: three components of skill improvement. , 2004, Journal of experimental psychology. Human perception and performance.

[2]  G. L. Gottlieb,et al.  Reconstruction of shifting elbow joint compliant characteristics during fast and slow movements , 1991, Neuroscience.

[3]  William J. Kargo,et al.  Conserved temporal dynamics and vector superposition of primitives in frog wiping reflexes during spontaneous extensor deletions , 2000, Neurocomputing.

[4]  M. Latash,et al.  Prehension Synergies , 2004, Exercise and sport sciences reviews.

[5]  F. Huddle Coordination , 1966, Open Knowledge Institutions.

[6]  S. Gandevia,et al.  Limited independent flexion of the thumb and fingers in human subjects. , 1994, The Journal of physiology.

[7]  G. Schöner Timing, Clocks, and Dynamical Systems , 2002, Brain and Cognition.

[8]  K. Newell Motor skill acquisition. , 1991, Annual review of psychology.

[9]  Tomoki Fukai,et al.  Sequence generation in arbitrary temporal patterns from theta-nested gamma oscillations: a model of the basal ganglia-thalamo-cortical loops , 1999, Neural Networks.

[10]  G. Schöner,et al.  Effects of varying task constraints on solutions to joint coordination in a sit-to-stand task , 2001, Experimental Brain Research.

[11]  Ferdinando A. Mussa-Ivaldi,et al.  Vector summation of end-point impedance in kinematically redundant manipulators , 1993, Proceedings of 1993 IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS '93).

[12]  M L Latash,et al.  On the problem of adequate language in motor control. , 1998, Motor control.

[13]  Håkan Johansson,et al.  Static and dynamic input-output relations of the feline medial gastrocnemius motoneuron-muscle system subjected to recurrent inhibition: a model study , 2003, Biological Cybernetics.

[14]  Neville Hogan,et al.  Integrable Solutions of Kinematic Redundancy via Impedance Control , 1991, Int. J. Robotics Res..

[15]  Loukia D. Loukopoulos,et al.  Planning reaches by evaluating stored postures. , 1995, Psychological review.

[16]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

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

[18]  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.

[19]  Riccardo Mazzocchio,et al.  Pharmacologically induced enhancement of recurrent inhibition in humans: effects on motoneurone discharge patterns. , 2003, The Journal of physiology.

[20]  John P Scholz,et al.  Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. , 2003, Brain : a journal of neurology.

[21]  T D Sanger,et al.  Human Arm Movements Described by a Low-Dimensional Superposition of Principal Components , 2000, The Journal of Neuroscience.

[22]  G. Schöner Recent Developments and Problems in Human Movement Science and Their Conceptual Implications , 1995 .

[23]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[24]  Mark L Latash,et al.  The organization of quick corrections within a two-joint synergy in conditions of unexpected blocking and release of a fast movement , 2000, Clinical Neurophysiology.

[25]  J. Massion,et al.  Axial synergies during human upper trunk bending , 1998, Experimental Brain Research.

[26]  M. Latash,et al.  Finger coordination in persons with Down syndrome: atypical patterns of coordination and the effects of practice , 2002, Experimental Brain Research.

[27]  Richard S. Sutton,et al.  Neural networks for control , 1990 .

[28]  J. Kelso,et al.  Functionally specific articulatory cooperation following jaw perturbations during speech: evidence for coordinative structures. , 1984, Journal of experimental psychology. Human perception and performance.

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

[30]  M. Latash,et al.  Structure of motor variability in marginally redundant multifinger force production tasks , 2001, Experimental Brain Research.

[31]  L. Nashner,et al.  Relation of automatic postural responses and reaction-time voluntary movements of human leg muscles , 2004, Experimental Brain Research.

[32]  W. Kargo,et al.  Early Skill Learning Is Expressed through Selection and Tuning of Cortically Represented Muscle Synergies , 2003, The Journal of Neuroscience.

[33]  G. Gottlieb,et al.  Coordinating movement at two joints: a principle of linear covariance. , 1996, Journal of neurophysiology.

[34]  N. A. Bernstein Dexterity and Its Development , 1996 .

[35]  J. M. Macpherson,et al.  Postural responses in the cat to unexpected rotations of the supporting surface: evidence for a centrally generated synergic organization , 2004, Experimental Brain Research.

[36]  J. Kelso,et al.  Learning as change of coordination dynamics: theory and experiment. , 1992, Journal of motor behavior.

[37]  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.

[38]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[39]  M. Kawato,et al.  Formation and control of optimal trajectory in human multijoint arm movement , 1989, Biological Cybernetics.

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

[41]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during sinusoid tracing. , 1993, Journal of neurophysiology.

[42]  D. Domkin,et al.  Structure of joint variability in bimanual pointing tasks , 2002, Experimental Brain Research.

[43]  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.

[44]  Paola Cesari,et al.  Body-goal Variability Mapping in an Aiming Task , 2006, Biological Cybernetics.

[45]  A. G. Feldman,et al.  Interjoint coordination dynamics during reaching in stroke , 2003, Experimental Brain Research.

[46]  J. Scholz,et al.  Learning a throwing task is associated with differential changes in the use of motor abundance , 2005, Experimental Brain Research.

[47]  J A Kelso,et al.  Dynamic pattern generation in behavioral and neural systems. , 1988, Science.

[48]  Z. Hasan,et al.  Activity of wrist muscles elicited during imposed or voluntary movements about the elbow joint. , 1991, Journal of motor behavior.

[49]  Gregor Schöner,et al.  Goal-equivalent joint coordination in pointing: affect of vision and arm dominance. , 2002, Motor control.

[50]  Karl M Newell,et al.  Task goals and change in dynamical degrees of freedom with motor learning. , 2003, Journal of experimental psychology. Human perception and performance.

[51]  Mark L. Latash,et al.  Kinematic description of variability of fast movements: analytical and experimental approaches , 1993, Biological Cybernetics.

[52]  H. Wilson Simplified dynamics of human and mammalian neocortical neurons. , 1999, Journal of theoretical biology.

[53]  C J Snijders,et al.  The hand of the musician: the kinematics of the bidigital finger system with anatomical restrictions. , 1993, Journal of biomechanics.

[54]  J. Massion,et al.  Kinematic synergies and equilibrium control during trunk movement under loaded and unloaded conditions , 1999, Experimental Brain Research.

[55]  E. J. Vrijenhoek,et al.  Arm position constraints during pointing and reaching in 3-D space. , 1997, Journal of neurophysiology.

[56]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[57]  A. Rossi,et al.  Distribution of recurrent inhibition in the human upper limb. , 1993, Acta physiologica Scandinavica.

[58]  Mark L. Latash,et al.  Joint angle variability in 3D bimanual pointing: uncontrolled manifold analysis , 2005, Experimental Brain Research.

[59]  Mitsuo Kawato,et al.  Computational schemes and neural network models for formulation and control of multijoint arm trajectory , 1990 .

[60]  W. Rymer,et al.  Target-dependent differences between free and constrained arm movements in chronic hemiparesis , 2004, Experimental Brain Research.

[61]  M. Latash,et al.  The relation between posture and movement: A study of a simple synergy in a two-joint task , 1995 .

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

[63]  Dagmar Sternad,et al.  A randomization method for the calculation of covariation in multiple nonlinear relations: illustrated with the example of goal-directed movements , 2003, Biological Cybernetics.

[64]  Shinji Kakei,et al.  Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons. , 2004, Progress in brain research.

[65]  M. Latash,et al.  Muscle modes and synergies during voluntary body sway , 2007, Experimental Brain Research.

[66]  M. Latash,et al.  Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis , 2005, Experimental Brain Research.

[67]  M. Latash,et al.  Muscle modes during shifts of the center of pressure by standing persons: effect of instability and additional support , 2004, Experimental Brain Research.

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

[69]  M Desmurget,et al.  Postural and synergic control for three-dimensional movements of reaching and grasping. , 1995, Journal of neurophysiology.

[70]  Richard A. Schmidt,et al.  Motor Learning and Performance , 1991 .

[71]  Mark L. Latash,et al.  The role of kinematic redundancy in adaptation of reaching , 2006, Experimental Brain Research.

[72]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[73]  Jack M. Winters,et al.  Multiple Muscle Systems , 1990, Springer New York.

[74]  L. A. Merkle,et al.  Using factor analysis to identify neuromuscular synergies during treadmill walking , 1998, Journal of Neuroscience Methods.

[75]  Gregor Schöner,et al.  Coordination underlying the control of whole body momentum during sit-to-stand. , 2002, Gait & posture.

[76]  W. T. Thach,et al.  Dynamic coordination of body parts during prism adaptation. , 2002, Journal of neurophysiology.

[77]  H. Ozeki,et al.  Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[78]  J. Lund,et al.  Anatomical substrates for functional columns in macaque monkey primary visual cortex. , 2003, Cerebral cortex.

[79]  M. Latash,et al.  Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without Down syndrome , 2003, Experimental Brain Research.

[80]  Mark L. Latash,et al.  The basis of a simple synergy: reconstruction of joint equilibrium trajectories during unrestrained arm movements , 1999 .

[81]  J. Kelso,et al.  Coordination dynamics of learning and transfer: collective and component levels. , 1997, Journal of experimental psychology. Human perception and performance.

[82]  Amy J Bastian,et al.  Role of the cerebellum in the control and adaptation of gait in health and disease. , 2004, Progress in brain research.

[83]  Simon R. Gutman,et al.  Basic functions of variability of simple pre-planned movements , 2004, Biological Cybernetics.

[84]  Gregor Schöner,et al.  From Interlimb Coordination to Trajectory Formation: Common Dynamical Principles , 1994 .

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

[86]  Eduardo Sontag Further facts about input to state stabilization , 1990 .

[87]  E. Thelen,et al.  Adaptive Dynamics of the Leg Movement Patterns of Human Infants: I. The Effects of Posture on Spontaneous Kicking. , 1994, Journal of motor behavior.

[88]  Vladimir M. Zatsiorsky,et al.  A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model , 2005, Biological Cybernetics.

[89]  J. F. Soechting,et al.  Force synergies for multifingered grasping , 2000, Experimental Brain Research.

[90]  T. Ebner,et al.  Cerebellar Purkinje Cell Simple Spike Discharge Encodes Movement Velocity in Primates during Visuomotor Arm Tracking , 1999, The Journal of Neuroscience.

[91]  N. Schoppa,et al.  Dendritic processing within olfactory bulb circuits , 2003, Trends in Neurosciences.

[92]  Z. Hasan,et al.  Optimized movement trajectories and joint stiffness in unperturbed, inertially loaded movements , 1986, Biological Cybernetics.

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

[94]  C. Sherrington Flexion‐reflex of the limb, crossed extension‐reflex, and reflex stepping and standing , 1910, The Journal of physiology.

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

[96]  Z Hasan,et al.  The Human Motor Control System's Response to Mechanical Perturbation: Should It, Can It and Does It Ensure Stability? , 2005, Journal of motor behavior.

[97]  C D Mah,et al.  Quantitative analysis of human movement synergies: constructive pattern analysis for gait. , 1994, Journal of motor behavior.

[98]  R N Lemon,et al.  The importance of the cortico-motoneuronal system for control of grasp. , 1998, Novartis Foundation symposium.

[99]  Gregor Schöner,et al.  Identifying the control structure of multijoint coordination during pistol shooting , 2000, Experimental Brain Research.

[100]  D J Ostry,et al.  Are complex control signals required for human arm movement? , 1998, Journal of neurophysiology.

[101]  Vladimir M. Zatsiorsky,et al.  Finger interaction during accurate multi-finger force production tasks in young and elderly persons , 2004, Experimental Brain Research.

[102]  Vladimir M. Zatsiorsky,et al.  Anticipatory covariation of finger forces during self-paced and reaction time force production , 2005, Neuroscience Letters.

[103]  A. G. Feldman,et al.  The origin and use of positional frames of reference in motor control , 1995, Behavioral and Brain Sciences.

[104]  Halla B. Olafsdottir,et al.  The emergence and disappearance of multi-digit synergies during force-production tasks , 2005, Experimental Brain Research.

[105]  J. Bloedel Functional heterogeneity with structural homogeneity: How does the cerebellum operate? , 1992 .

[106]  M. Hayhoe,et al.  The coordination of eye, head, and hand movements in a natural task , 2001, Experimental Brain Research.

[107]  K. Kudo,et al.  Compensatory Coordination of Release Parameters in a Throwing Task , 2000, Journal of motor behavior.

[108]  M. Latash,et al.  Learning multi-finger synergies: an uncontrolled manifold analysis , 2004, Experimental Brain Research.

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

[110]  Daniel Bullock,et al.  Development in a biologically inspired spinal neural network for movement control , 1998, Neural Networks.

[111]  Gregor Schöner,et al.  Effect of accuracy constraint on joint coordination during pointing movements , 2003, Experimental Brain Research.

[112]  Mitsuo Kawato,et al.  Feedback-error-learning neural network for trajectory control of a robotic manipulator , 1988, Neural Networks.

[113]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999 .

[114]  T. Ohtsuki Inhibition of individual fingers during grip strength exertion. , 1981, Ergonomics.

[115]  M. Latash,et al.  Changes in finger coordination and responses to single pulse TMS of motor cortex during practice of a multifinger force production task , 2003, Experimental Brain Research.

[116]  O. I. Fukson,et al.  Adaptability of innate motor patterns and motor control mechanisms , 1986, Behavioral and Brain Sciences.

[117]  A. G. Feldman Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .

[118]  Zong-Ming Li,et al.  Functional degrees of freedom. , 2006, Motor control.

[119]  Gregor Schöner,et al.  The uncontrolled manifold concept: identifying control variables for a functional task , 1999, Experimental Brain Research.

[120]  宇野 洋二,et al.  Formation and control of optimal trajectory in human multijoint arm movement : minimum torque-change model , 1988 .

[121]  J. Winters,et al.  Optimized Strategies for Scaling Goal-Directed Dynamic Limb Movements , 1990 .

[122]  R. Christina,et al.  Psychology of motor behavior and sport , 1978 .

[123]  Ning Lan,et al.  Analysis of an optimal control model of multi-joint arm movements , 1997, Biological Cybernetics.

[124]  J. Foley The co-ordination and regulation of movements , 1968 .

[125]  A. G. Feldman,et al.  Recent Tests of the Equilibrium-Point Hypothesis (λ Model) , 1998 .

[126]  Zoubin Ghahramani,et al.  Perspectives and problems in motor learning , 2001, Trends in Cognitive Sciences.

[127]  Hans Hultborn,et al.  Key mechanisms for setting the input-output gain across the motoneuron pool. , 2004, Progress in brain research.

[128]  B. Vereijken,et al.  Free(z)ing Degrees of Freedom in Skill Acquisition , 1992 .

[129]  R. Emmerik,et al.  The effects of practice on limb kinematics in a throwing task. , 1989, Journal of motor behavior.

[130]  Mark L. Latash,et al.  Feed-forward control of a redundant motor system , 2006, Biological Cybernetics.

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

[132]  E. Bizzi,et al.  Linear combinations of primitives in vertebrate motor control. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[133]  S. Grossberg,et al.  A Self-Organizing Neural Model of Motor Equivalent Reaching and Tool Use by a Multijoint Arm , 1993, Journal of Cognitive Neuroscience.

[134]  M. Latash,et al.  Motor variability within a multi-effector system: experimental and analytical studies of multi-finger production of quick force pulses , 2005, Experimental Brain Research.

[135]  J. Abbs,et al.  Control of complex motor gestures: orofacial muscle responses to load perturbations of lip during speech. , 1984, Journal of neurophysiology.

[136]  R. Shadmehr Generalization as a behavioral window to the neural mechanisms of learning internal models. , 2004, Human movement science.

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

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

[139]  Andrea d'Avella,et al.  Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. , 2006, Journal of neurophysiology.

[140]  Jae Kun Shim,et al.  Is there a timing synergy during multi-finger production of quick force pulses? , 2004, Experimental brain research.

[141]  Jae Kun Shim,et al.  The human central nervous system needs time to organize task-specific covariation of finger forces , 2003, Neuroscience Letters.

[142]  M. Latash,et al.  Enslaving effects in multi-finger force production , 2000, Experimental Brain Research.

[143]  G. Somjen,et al.  Excitability and inhibitability of motoneurons of different sizes. , 1965, Journal of neurophysiology.

[144]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[145]  M. Hoy,et al.  Intralimb coordination of the paw-shake response: a novel mixed synergy. , 1985, Journal of neurophysiology.

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

[147]  Agnès Roby-Brami,et al.  Use of the trunk for reaching targets placed within and beyond the reach in adult hemiparesis , 2002, Experimental Brain Research.

[148]  Gregor Schöner,et al.  Differential joint coordination in the tasks of standing up and sitting down. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[149]  Gregor Schöner,et al.  Understanding finger coordination through analysis of the structure of force variability , 2002, Biological Cybernetics.

[150]  Gregor Schöner,et al.  A mode hypothesis for finger interaction during multi-finger force-production tasks , 2003, Biological Cybernetics.

[151]  M. Latash,et al.  Finger coordination during discrete and oscillatory force production tasks , 2002, Experimental Brain Research.

[152]  M. Latash,et al.  Force sharing among fingers as a model of the redundancy problem , 1998, Experimental Brain Research.