The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex.

Behavioral and neurophysiological studies suggest that skill learning can be mediated by discrete, experience-driven changes within specific neural representations subserving the performance of the trained task. We have shown that a few minutes of daily practice on a sequential finger opposition task induced large, incremental performance gains over a few weeks of training. These gains did not generalize to the contralateral hand nor to a matched sequence of identical component movements, suggesting that a lateralized representation of the learned sequence of movements evolved through practice. This interpretation was supported by functional MRI data showing that a more extensive representation of the trained sequence emerged in primary motor cortex after 3 weeks of training. The imaging data, however, also indicated important changes occurring in primary motor cortex during the initial scanning sessions, which we proposed may reflect the setting up of a task-specific motor processing routine. Here we provide behavioral and functional MRI data on experience-dependent changes induced by a limited amount of repetitions within the first imaging session. We show that this limited training experience can be sufficient to trigger performance gains that require time to become evident. We propose that skilled motor performance is acquired in several stages: "fast" learning, an initial, within-session improvement phase, followed by a period of consolidation of several hours duration, and then "slow" learning, consisting of delayed, incremental gains in performance emerging after continued practice. This time course may reflect basic mechanisms of neuronal plasticity in the adult brain that subserve the acquisition and retention of many different skills.

[1]  H. Eysenck A THREE-FACTOR THEORY OF REMINISCENCE. , 1965, British journal of psychology.

[2]  L. Squire Mechanisms of memory. , 1986, Lancet.

[3]  J. Pettigrew,et al.  Selective modification of single neuron properties in the visual cortex of kittens , 1974 .

[4]  A. Fiorentini,et al.  Learning in grating waveform discrimination: Specificity for orientation and spatial frequency , 1981, Vision Research.

[5]  E. Kandel,et al.  Molecular biology of learning: modulation of transmitter release. , 1982, Science.

[6]  R. Sekuler,et al.  Direction-specific improvement in motion discrimination , 1987, Vision Research.

[7]  J. Adams Historical review and appraisal of research on the learning, retention, and transfer of human motor skills. , 1987 .

[8]  L. Weiskrantz Problems of learning and memory: one or multiple memory systems? , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  M. Merzenich,et al.  Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. , 1990, Journal of neurophysiology.

[10]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[11]  S. Juliano,et al.  Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[12]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[13]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[15]  R. Seitz,et al.  Learning of Sequential Finger Movements in Man: A Combined Kinematic and Positron Emission Tomography (PET) Study , 1992, The European journal of neuroscience.

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

[17]  A. Keller,et al.  Synaptic proliferation in the motor cortex of adult cats after long-term thalamic stimulation. , 1992, Journal of neurophysiology.

[18]  Á. Pascual-Leone,et al.  Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. , 1993, Brain : a journal of neurology.

[19]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  M. Merzenich,et al.  Cortical plasticity and memory , 1993, Current Opinion in Neurobiology.

[21]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[22]  H. Asanuma,et al.  Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. , 1993, Journal of neurophysiology.

[23]  P. Roland,et al.  Fields in human motor areas involved in preparation for reaching, actual reaching, and visuomotor learning: a positron emission tomography study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  U Polat,et al.  Spatial interactions in human vision: from near to far via experience-dependent cascades of connections. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

[26]  Scott T. Grafton,et al.  Functional imaging of procedural motor learning: Relating cerebral blood flow with individual subject performance , 1994, Human brain mapping.

[27]  J F Soechting,et al.  The learning of novel finger movement sequences. , 1994, Journal of neurophysiology.

[28]  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.

[29]  M. Fahle Human Pattern Recognition: Parallel Processing and Perceptual Learning , 1994, Perception.

[30]  A. Karni,et al.  Dependence on REM sleep of overnight improvement of a perceptual skill. , 1994, Science.

[31]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

[32]  G. Orban,et al.  Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. , 1995, The Journal of physiology.

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

[34]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[35]  A. Karni,et al.  Applications of magnetic resonance imaging to the study of human brain function , 1995, Current Opinion in Neurobiology.

[36]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Xiaoqin Wang,et al.  Remodelling of hand representation in adult cortex determined by timing of tactile stimulation , 1995, Nature.

[38]  O. Hikosaka,et al.  Learning of sequential movements in the monkey: process of learning and retention of memory. , 1995, Journal of neurophysiology.

[39]  MH Schieber Muscular production of individuated finger movements: the roles of extrinsic finger muscles , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  W. T. Thach,et al.  Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. , 1996, Brain : a journal of neurology.

[42]  A. Karni The acquisition of perceptual and motor skills: a memory system in the adult human cortex. , 1996, Brain research. Cognitive brain research.

[43]  Y. Dudai Consolidation: Fragility on the Road to the Engram , 1996, Neuron.

[44]  Gurindar S. Sohi,et al.  Memory systems , 1996, CSUR.

[45]  E Bizzi,et al.  Motor learning by field approximation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Wise,et al.  The Acquisition of Motor Behavior in Vertebrates , 1996 .

[47]  E. Bizzi,et al.  Consolidation in human motor memory , 1996, Nature.

[48]  O. Hikosaka,et al.  Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. , 1996, Journal of neurophysiology.

[49]  S. Kitazawa,et al.  Prism Adaptation of Reaching Movements: Specificity for the Velocity of Reaching , 1997, The Journal of Neuroscience.

[50]  K. Sathian,et al.  Tactile learning is task specific but transfers between fingers , 1997, Perception & psychophysics.

[51]  A. Karni,et al.  Learning perceptual skills: behavioral probes into adult cortical plasticity , 1997, Current Opinion in Neurobiology.

[52]  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.

[53]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

[54]  R L Buckner,et al.  Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.