Mapping of direction and muscle representation in the human primary motor cortex controlling thumb movements

Larger body parts are somatotopically represented in the primary motor cortex (M1), while smaller body parts, such as the fingers, have partially overlapping representations. The principles that govern the overlapping organization of M1 remain unclear. We used transcranial magnetic stimulation (TMS) to examine the cortical encoding of thumb movements in M1 of healthy humans. We performed M1 mapping of the probability of inducing a thumb movement in a particular direction and used low intensity TMS to disturb a voluntary thumb movement in the same direction during a reaction time task. With both techniques we found spatially segregated representations of the direction of TMS‐induced thumb movements, thumb flexion and extension being best separated. Furthermore, the cortical regions corresponding to activation of a thumb muscle differ, depending on whether the muscle functions as agonist or as antagonist for flexion or extension. In addition, we found in the reaction time experiment that the direction of a movement is processed in M1 before the muscles participating in it are activated. It thus appears that one of the organizing principles for the human corticospinal motor system is based on a spatially segregated representation of movement directions and that the representation of individual somatic structures, such as the hand muscles, overlap.

[1]  Lumy Sawaki,et al.  Effects of Somatosensory Stimulation on Use-Dependent Plasticity in Chronic Stroke , 2006, Stroke.

[2]  M. Hallett,et al.  Excitability of the ipsilateral motor cortex during phasic voluntary hand movement , 2002, Experimental Brain Research.

[3]  L. Cohen,et al.  Enhancing the quality of studies using transcranial magnetic and electrical stimulation with a new computer-controlled system , 2000, Journal of Neuroscience Methods.

[4]  P. Hodges,et al.  A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. , 1996, Electroencephalography and clinical neurophysiology.

[5]  Ichiro Kanazawa,et al.  Shortening of simple reaction time by peripheral electrical and submotor-threshold magnetic cortical stimulation , 1997, Experimental Brain Research.

[6]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[7]  Jens Frahm,et al.  Functional somatotopy of finger representations in human primary motor cortex , 2003, Human brain mapping.

[8]  Rupert Lanzenberger,et al.  Finger Somatotopy in Human Motor Cortex , 2001, NeuroImage.

[9]  K Kaneko,et al.  The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. , 1996, Electroencephalography and clinical neurophysiology.

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

[11]  M Hallett,et al.  Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. , 2000, Brain : a journal of neurology.

[12]  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.

[13]  J. Donoghue,et al.  Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles , 2004, Experimental Brain Research.

[14]  L. Cohen,et al.  Role of voluntary drive in encoding an elementary motor memory. , 2005, Journal of neurophysiology.

[15]  M. Hallett,et al.  Simple reaction time to focal transcranial magnetic stimulation. Comparison with reaction time to acoustic, visual and somatosensory stimuli. , 1992, Brain : a journal of neurology.

[16]  U. Ziemann,et al.  Intracortical inhibition and facilitation in the conventional paired TMS paradigm. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[17]  D. Humphrey Representation of movements and muscles within the primate precentral motor cortex: historical and current perspectives. , 1986, Federation proceedings.

[18]  B L Day,et al.  Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Evidence for the storage of motor programs in the brain. , 1989, Brain : a journal of neurology.

[19]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[20]  A. Schwartz,et al.  On the relationship between joint angular velocity and motor cortical discharge during reaching. , 2001, Journal of neurophysiology.

[21]  Ulf Ziemann,et al.  Delay in simple reaction time after focal transcranial magnetic stimulation of the human brain occurs at the final motor output stage , 1997, Brain Research.

[22]  S. Scott,et al.  Changes in motor cortex activity during reaching movements with similar hand paths but different arm postures. , 1995, Journal of neurophysiology.

[23]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[24]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

[25]  J. Valls-Solé,et al.  Reaction time and acoustic startle in normal human subjects , 1995, Neuroscience Letters.

[26]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[27]  M. Hallett,et al.  Rapid plasticity of human cortical movement representation induced by practice. , 1998, Journal of neurophysiology.

[28]  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.

[29]  P. Thompson,et al.  Interruption of motor programmes by electrical or magnetic brain stimulation in man. , 1989, Progress in brain research.

[30]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[31]  Alexa Riehle,et al.  Spike synchronization and firing rate in a population of motor cortical neurons in relation to movement direction and reaction time , 2003, Biological Cybernetics.

[32]  A. Conforto,et al.  Impact of coil position and electrophysiological monitoring on determination of motor thresholds to transcranial magnetic stimulation , 2004, Clinical Neurophysiology.

[33]  Iole Indovina,et al.  On Somatotopic Representation Centers for Finger Movements in Human Primary Motor Cortex and Supplementary Motor Area , 2001, NeuroImage.

[34]  K D Singh,et al.  Topographic mapping of trans-cranial magnetic stimulation data on surface rendered MR images of the brain. , 1997, Electroencephalography and clinical neurophysiology.

[35]  Leonid Kopylev,et al.  Age‐dependent changes in the ability to encode a novel elementary motor memory , 2003, Annals of neurology.

[36]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[37]  M. Hallett,et al.  Effects of focal transcranial magnetic stimulation on simple reaction time to acoustic, visual and somatosensory stimuli. , 1992, Brain : a journal of neurology.

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

[39]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[40]  John W. Scott,et al.  Selected Writings of John Hughlings Jackson , 1959 .

[41]  S. Wise,et al.  Mechanisms of use-dependent plasticity in the human motor cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Rothwell,et al.  Intracortical inhibition and facilitation in different representations of the human motor cortex. , 1998, Journal of neurophysiology.

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

[44]  L. Sawaki,et al.  Specific and non-specific effects of transcranial magnetic stimulation on simple and go/no-go reaction time , 1999, Experimental Brain Research.

[45]  S. Small,et al.  Somatotopy in human primary motor and somatosensory hand representations revisited. , 2001, Cerebral cortex.