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

  1. Avi Karni*,
  2. Gundela Meyer,
  3. Christine Rey-Hipolito,
  4. Peter Jezzard,
  5. Michelle M. Adams,
  6. Robert Turner§, and
  7. Leslie G. Ungerleider
  1. Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, 49 Convent Drive, Bethesda MD 20892

Abstract

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.

Footnotes

  • * To whom reprint requests should be addressed at present address: Department of Neurobiology, Brain Research, The Weizmann Institute of Science, Rehovot 76100, Israel; also at Department of Neurology, Sheba Medical Center, Tel-Hashomer, Israel. e-mail: bnkarni{at}weizmann.weizmann.ac.il.

  • Present address: Department of Anatomy, University of La Laguna, Tenerife 38320, Spain.

  • Present address: Department of Neurobiology, Mount Sinai Medical Center, New York, NY 10029.

  • § Present address: Wellcome Department of Cognitive Neurology, Institute of Neurology, London WC1N 3BG, United Kingdom.

  • This paper was presented at a colloquium entitled “Neuroimaging of Human Brain Function,” organized by Michael Posner and Marcus E. Raichle, held May 29–31, 1997, sponsored by the National Academy of Sciences at the Arnold and Mabel Beckman Center in Irvine, CA.

  • ABBREVIATIONS:
    fMRI,
    functional magnetic resonance imaging;
    M1,
    primary motor cortex
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