From intention to action: motor cortex and the control of reaching movements.

The motor cortex was experimentally identified more than a century ago using surface electrical stimulation and lesions. Those first studies initiated a debate about the role of the motor cortex in the control of voluntary movement that continues to this day. The main issue concerns the degree to which the descending motor command emanating from the motor cortex specifies the spatiotemporal form of a movement or its causal forces, torques and muscle activity. The neurophysiological evidence supports both perspectives. This chapter surveys some of that evidence, with particular focus on the latter, more 'traditional', role of motor cortex.

[1]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[2]  E. Evarts Activity of pyramidal tract neurons during postural fixation. , 1969, Journal of neurophysiology.

[3]  D R Humphrey,et al.  Predicting Measures of Motor Performance from Multiple Cortical Spike Trains , 1970, Science.

[4]  T. Szabo,et al.  Club endings of primary afferent fibres identified by anterograde horseradish peroxidase labelling. An em study , 1978, Neuroscience Letters.

[5]  W. T. Thach Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. , 1978, Journal of neurophysiology.

[6]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[7]  E. Fetz,et al.  Functional classes of primate corticomotoneuronal cells and their relation to active force. , 1980, Journal of neurophysiology.

[8]  J. Yokota,et al.  Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey , 1981, Neuroscience Letters.

[9]  J. Hollerbach Computers, brains and the control of movement , 1982, Trends in Neurosciences.

[10]  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.

[11]  C. Chandler,et al.  Computers, brains and the control of movement , 1982, Trends in Neurosciences.

[12]  J. Massion,et al.  Neural coding of motor performance , 1983 .

[13]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[14]  S. Hagiwara,et al.  The calcium channel , 1983, Trends in Neurosciences.

[15]  R. Lemon,et al.  Corticospinal neurons with a special role in precision grip , 1983, Brain Research.

[16]  E. Evarts,et al.  Motor Cortex control of finely graded forces. , 1983, Journal of neurophysiology.

[17]  Gerald M. Edelman,et al.  Dynamic aspects of neocortical function , 1984 .

[18]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Fetz,et al.  Patterns of facilitation and suppression of antagonist forelimb muscles from motor cortex sites in the awake monkey. , 1985, Journal of neurophysiology.

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

[21]  A. G. Feldman Once more on the equilibrium-point hypothesis (lambda model) for motor control. , 1986, Journal of motor behavior.

[22]  F. Mussa-Ivaldi,et al.  Do neurons in the motor cortex encode movement direction? An alternative hypothesis , 1988, Neuroscience Letters.

[23]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  S. Grillner,et al.  Visuomotor coordination in reaching and locomotion. , 1989, Science.

[27]  J. F. Soechting,et al.  Sensorimotor representations for pointing to targets in three-dimensional space. , 1989, Journal of neurophysiology.

[28]  J. Flanagan,et al.  The Origin of Electromyograms - Explanations Based on the Equilibrium Point Hypothesis , 1990 .

[29]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  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.

[31]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  E. Fetz,et al.  Neural mechanisms underlying corticospinal and rubrospinal control of limb movements. , 1991, Progress in brain research.

[33]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[34]  J F Soechting,et al.  Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. , 1992, Annual review of neuroscience.

[35]  A. Georgopoulos,et al.  The motor cortex and the coding of force. , 1992, Science.

[36]  J. F. Soechting,et al.  Early stages in a sensorimotor transformation , 1992, Behavioral and Brain Sciences.

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

[38]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[39]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[40]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[41]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[42]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[43]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[44]  R. Lemon,et al.  The influence of single monkey cortico‐motoneuronal cells at different levels of activity in target muscles. , 1994, The Journal of physiology.

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

[46]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[47]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[48]  R. Lemon,et al.  Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey. , 1996, Journal of neurophysiology.

[49]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

[50]  A. G. Feldman,et al.  Central modifications of reflex parameters may underlie the fastest arm movements. , 1997, Journal of neurophysiology.

[51]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

[52]  J. Ashe Force and the motor cortex , 1997, Behavioural Brain Research.

[53]  J. Ashe Erratum to “Force and the motor cortex” [Behavioural Brain Research 86 (1997) 1–15] 1 PII of original article: S0166-4328(96)00145-3 1 , 1997, Behavioural Brain Research.

[54]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. , 1997, Journal of neurophysiology.

[55]  Daniel M. Wolpert,et al.  Signal-dependent noise determines motor planning , 1998, Nature.

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

[57]  P. Cheney,et al.  Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. , 1998, Journal of neurophysiology.

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

[59]  B. Weber,et al.  Context-dependent force coding in motor and premotor cortical areas , 1999, Experimental Brain Research.

[60]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

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

[62]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during spiral tracing. , 1999, Journal of neurophysiology.

[63]  F. Lacquaniti,et al.  Parieto-frontal coding of reaching: an integrated framework , 1999, Experimental Brain Research.

[64]  Reza Shadmehr,et al.  Computational nature of human adaptive control during learning of reaching movements in force fields , 1999, Biological Cybernetics.

[65]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[66]  S Grossberg,et al.  Kinematic coordinates in which motor cortical cells encode movement direction. , 2000, Journal of neurophysiology.

[67]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[68]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

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

[70]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[71]  P. Cheney,et al.  Correlations between corticomotoneuronal (CM) cell postspike effects and cell-target muscle covariation. , 2000, Journal of neurophysiology.

[72]  E. Todorov Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[73]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

[74]  S Grossberg,et al.  A model of movement coordinates in the motor cortex: posture-dependent changes in the gain and direction of single cell tuning curves. , 2001, Cerebral cortex.

[75]  A. G. Feldman,et al.  The timing of control signals underlying fast point-to-point arm movements , 2001, Experimental Brain Research.

[76]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[77]  S. Scott,et al.  Neural activity in primary motor cortex related to mechanical loads applied to the shoulder and elbow during a postural task. , 2001, Journal of neurophysiology.

[78]  Mitsuo Kawato,et al.  MOSAIC Model for Sensorimotor Learning and Control , 2001, Neural Computation.

[79]  Dawn M. Taylor,et al.  Direct Cortical Control of 3D Neuroprosthetic Devices , 2002, Science.

[80]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

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

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

[83]  Stephen H. Scott,et al.  Overlap of internal models in motor cortex for mechanical loads during reaching , 2002, Nature.

[84]  S. Meagher Instant neural control of a movement signal , 2002 .

[85]  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.

[86]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[87]  David J. Ostry,et al.  A critical evaluation of the force control hypothesis in motor control , 2003, Experimental Brain Research.

[88]  Paul Cisek,et al.  Kinematics and kinetics of multijoint reaching in nonhuman primates. , 2003, Journal of neurophysiology.

[89]  C. Gross,et al.  Twitches Versus Movements: A Story of Motor Cortex , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[90]  R. Shadmehr,et al.  A Gain-Field Encoding of Limb Position and Velocity in the Internal Model of Arm Dynamics , 2003, PLoS biology.

[91]  M. M. Morrow,et al.  Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. , 2003, Journal of neurophysiology.

[92]  D. Hoffman,et al.  Sensorimotor transformations in cortical motor areas , 2003, Neuroscience Research.

[93]  J. Kalaska,et al.  Systematic changes in motor cortex cell activity with arm posture during directional isometric force generation. , 2003, Journal of neurophysiology.

[94]  M. Eisen,et al.  Why PLoS Became a Publisher , 2003, PLoS biology.

[95]  Nicholas Hatsopoulos,et al.  Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. , 2004, Journal of neurophysiology.

[96]  A. P. Georgopoulos,et al.  Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex , 1983, Experimental Brain Research.

[97]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[98]  J. Kalaska,et al.  Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics , 2004, Experimental Brain Research.

[99]  P. Cheney,et al.  Properties of primary motor cortex output to forelimb muscles in rhesus macaques. , 2004, Journal of neurophysiology.

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

[101]  S. Scott Optimal feedback control and the neural basis of volitional motor control , 2004, Nature Reviews Neuroscience.

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

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

[104]  A. Georgopoulos,et al.  On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force , 2004, Experimental Brain Research.

[105]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[106]  L. Paninski,et al.  Spatiotemporal tuning of motor cortical neurons for hand position and velocity. , 2004, Journal of neurophysiology.

[107]  L. Paninski,et al.  Superlinear Population Encoding of Dynamic Hand Trajectory in Primary Motor Cortex , 2004, The Journal of Neuroscience.

[108]  David M. Santucci,et al.  Frontal and parietal cortical ensembles predict single‐trial muscle activity during reaching movements in primates , 2005, The European journal of neuroscience.

[109]  Jyl Boline,et al.  On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional dynamic isometric force , 1996, Experimental Brain Research.

[110]  Reza Shadmehr,et al.  Internal models of limb dynamics and the encoding of limb state , 2005, Journal of neural engineering.

[111]  J. Kalaska,et al.  Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. , 2005, Journal of neurophysiology.

[112]  J. A. Pruszynski,et al.  Primate upper limb muscles exhibit activity patterns that differ from their anatomical action during a postural task. , 2006, Journal of neurophysiology.

[113]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[114]  Anatol G. Feldman,et al.  Threshold control of arm posture and movement adaptation to load , 2006, Experimental Brain Research.

[115]  Wei Wu,et al.  Evidence against a single coordinate system representation in the motor cortex , 2006, Experimental Brain Research.

[116]  Benjamin R. Townsend,et al.  Linear encoding of muscle activity in primary motor cortex and cerebellum. , 2006, Journal of neurophysiology.

[117]  John F Kalaska,et al.  Parietal area 5 activity does not reflect the differential time-course of motor output kinetics during arm-reaching and isometric-force tasks. , 2006, Journal of neurophysiology.

[118]  Yasuharu Koike,et al.  Prediction of arm trajectory from a small number of neuron activities in the primary motor cortex , 2006, Neuroscience Research.

[119]  Eilon Vaadia,et al.  Learning from learning: what can visuomotor adaptations tell us about the neuronal representation of movement? , 2009, Advances in experimental medicine and biology.

[120]  Lee E Miller,et al.  Control of muscle synergies by cortical ensembles. , 2009, Advances in experimental medicine and biology.

[121]  Nicholas G Hatsopoulos,et al.  The problem of parametric neural coding in the motor system. , 2009, Advances in experimental medicine and biology.

[122]  H. Kimelberg,et al.  TWIK-1 and TREK-1 Are Potassium Channels Contributing Significantly to Astrocyte Passive Conductance in Rat Hippocampal Slices , 2009, The Journal of Neuroscience.

[123]  Jack M. Winters,et al.  Multiple Muscle Systems: Biomechanics and Movement Organization , 2011 .