Kinematic specificity of cortical reorganization associated with motor training

Motor training consisting of repetition of directionally specific voluntary thumb movements elicits a short-term memory trace that encodes the kinematic details of the practiced motions in the primary motor cortex. Here, we studied activation patterns associated with this form of training using functional magnetic resonance imaging under careful monitoring of motor training kinematics and electromyography. We identified task-specific reductions in activation in contralateral motor cortex, a region that controls executive motor output, as well as somatosensory cortex and inferior parietal lobule, regions in charge of monitoring motor training kinematics. Our findings are consistent with the hypothesis that a short training period consisting of repetition of finger motions leads to cortical reorganization characterized by a smaller and more efficient network that is specific for the trained movement direction.

[1]  Richard S. J. Frackowiak,et al.  Neural correlates of motor recovery after stroke: a longitudinal fMRI study. , 2003, Brain : a journal of neurology.

[2]  S. Hochstein,et al.  Attentional Demands Following Perceptual Skill Training , 2001, Psychological science.

[3]  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.

[4]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[5]  C. Michel,et al.  PET study of human voluntary saccadic eye movements in darkness: effect of task repetition on the activation pattern , 1998, The European journal of neuroscience.

[6]  T Poggio,et al.  Fast perceptual learning in visual hyperacuity. , 1991, Science.

[7]  F. Chollet,et al.  Within-Session and Between-Session Reproducibility of Cerebral Sensorimotor Activation: A Test–Retest Effect Evidenced with Functional Magnetic Resonance Imaging , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[9]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[11]  R. Cox,et al.  Test-retest precision of functional MR in sensory and motor task activation. , 1996, AJNR. American journal of neuroradiology.

[12]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Gary F. Egan,et al.  The Functional Neuroanatomy and Long-Term Reproducibility of Brain Activation Associated with a Simple Finger Tapping Task in Older Healthy Volunteers: A Serial PET Study , 2000, NeuroImage.

[14]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[15]  L. Cohen,et al.  Enhancement of use-dependent plasticity by d-amphetamine , 2002, Neurology.

[16]  Manfred Fahle,et al.  Perceptual learning: gain without pain? , 2002, Nature Neuroscience.

[17]  L. Cohen,et al.  Modulation of use‐dependent plasticity by d‐amphetamine , 2002, Supplements to Clinical neurophysiology.

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

[19]  R J Seitz,et al.  Representations of Graphomotor Trajectories in the Human Parietal Cortex: Evidence for Controlled Processing and Automatic Performance , 1997, The European journal of neuroscience.

[20]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Heidi Johansen-Berg,et al.  Attention to movement modulates activity in sensori-motor areas, including primary motor cortex , 2001, Experimental Brain Research.

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

[23]  J. Pekar,et al.  Whole-brain functional mapping with isotropic MR imaging. , 1996, Radiology.

[24]  Tracy L. Faber,et al.  Role of posterior parietal cortex in the recalibration of visually guided reaching , 1996, Nature.

[25]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[26]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.

[27]  J. Gabrieli Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[28]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[29]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  M. Farlow,et al.  Cerebrospinal fluid homovanillic acid levels in rapid‐onset dystonia‐parkinsonism , 1998, Annals of neurology.

[31]  L. Cohen,et al.  Cholinergic influences on use-dependent plasticity. , 2002, Journal of neurophysiology.

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

[33]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[34]  J. Tracy,et al.  A comparison of 'Early' and 'Late' stage brain activation during brief practice of a simple motor task. , 2001, Brain research. Cognitive brain research.

[35]  Anthony R. McIntosh,et al.  Task-Independent Effect of Time on rCBF , 1998, NeuroImage.