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Stages of motor skill learning

Abstract

Successful learning of a motor skill requires repetitive training. Once the skill is mastered, it can be remembered for a long period of time. The durable memory makes motor skill learning an interesting paradigm for the study of learning and memory mechanisms. To gain better understanding, one scientific approach is to dissect the process into stages and to study these as well as their interactions. This article covers the growing evidence that motor skill learning advances through stages, in which different storage mechanisms predominate. The acquisition phase is characterized by fast (within session) and slow learning (between sessions). For a short period following the initial training sessions, the skill is labile to interference by other skills and by protein synthesis inhibition, indicating that consolidation processes occur during rest periods between training sessions. During training as well as rest periods, activation in different brain regions changes dynamically. Evidence for stages in motor skill learning is provided by experiments using behavioral, electrophysiological, functional imaging, and cellular/molecular methods.

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References

  1. Thompson R. F. (1986) The neurobiology of learning and memory. Science 233, 941–947.

    PubMed  Article  CAS  Google Scholar 

  2. Ito M. (1993) Neurophysiology of the nodulofloccular system. Rev. Neurol. (Paris) 149, 692–697.

    CAS  Google Scholar 

  3. Laubach M., Wessberg J., and Nicolelis M. A. (2000) Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405, 567–571.

    PubMed  Article  CAS  Google Scholar 

  4. Nissen M. J., Knopman D. S., and Schacter D. L. (1987) Neurochemical dissociation of memory systems. Neurology 37, 789–794.

    PubMed  CAS  Google Scholar 

  5. Brashers-Krug T., Shadmehr R., and Bizzi E. (1996) Consolidation in human motor memory. Nature 382, 252–255.

    PubMed  Article  CAS  Google Scholar 

  6. Sanes J. N. (2003) Neocortical mechanisms in motor learning. Curr. Opin. Neurobiol. 13, 225–231.

    PubMed  Article  CAS  Google Scholar 

  7. Asanuma H. and Pavlides C. (1997) Neurobiological basis of motor learning in mammals. Neuroreport 8, i-vi.

    PubMed  CAS  Google Scholar 

  8. Lee T. D. and Genovese E. D. (1989) Distribution of practice in motor skill acquisition: different effects for discrete and continuous tasks. Res. Q. Exerc. Sport. 60, 59–65.

    PubMed  CAS  Google Scholar 

  9. Lee T. D. and Genovese E. D. (1989) Some reminiscences on distribution of practice effects. Res. Q. Exerc. Sport. 60, 297–299.

    PubMed  CAS  Google Scholar 

  10. Adams J. A. (1961) The second facet of forgetting: a review of the warm-up decrement. Psycholog. Bull. 58, 257–273.

    Article  CAS  Google Scholar 

  11. Luft A. R., Buitrago M. M., Kaelin-Lang A., Dichgans J., and Schulz J. B. (2004) Protein synthesis inhibition blocks consolidation of an acrobatic motor skill. Learn. Mem. 11, 379–382.

    PubMed  Article  Google Scholar 

  12. Walker M. P., Brakefield T., Hobson J. A., and Stickgold R. (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616–620.

    PubMed  Article  CAS  Google Scholar 

  13. Jeannerod M. (1995) Mental imagery in the motor context. Neuropsychologia 33, 1419–1432.

    PubMed  Article  CAS  Google Scholar 

  14. Mulder T., Zijlstra S., Zijlstra W., and Hochstenbach J. (2004) The role of motor imagery in learning a totally novel movement. Exp. Brain Res. 154, 211–217.

    PubMed  Article  Google Scholar 

  15. Karni A., Meyer G., Rey-Hipolito C., et al. (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc. Natl. Acad. Sci. USA 95, 861–868.

    PubMed  Article  CAS  Google Scholar 

  16. Buitrago M. M., Schulz J. B., Dichgans J., and Luft A. R. (2004) Short and long-term motor skill learning in an accelerated rotarod training paradigm. Neurobiol. Learn. Mem. 81, 211–216.

    PubMed  Article  Google Scholar 

  17. Buitrago M. M., Ringer T., Schulz J. B., Dichgans J., and Luft A. R. (2004) Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat. Behav. Brain Res. 155, 249–256.

    PubMed  Article  Google Scholar 

  18. Flanagan J. R., Vetter P., Johansson R. S., and Wolpert D. M. (2003) Prediction precedes control in motor learning. Curr. Biol. 13, 146–150.

    PubMed  Article  CAS  Google Scholar 

  19. Hikosaka O., Nakahara H., Rand M. K., et al. (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci. 22, 464–471.

    PubMed  Article  CAS  Google Scholar 

  20. Pascual-Leone A., Grafman J., and Hallett M. (1994) Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263, 1287–1289.

    PubMed  Article  CAS  Google Scholar 

  21. Rizzolatti G. and Craighero L. (2004) The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192.

    PubMed  Article  CAS  Google Scholar 

  22. Sakai K., Hikosaka O., and Nakamura K. (2004) Emergence of rhythm during motor learning. Trends Cogn. Sci. 8, 547–553.

    PubMed  Article  Google Scholar 

  23. Eversheim U. and Bock O. (2001) Evidence for processing stages in skill acquisition: a dualtask study. Learn. Mem. 8, 183–189.

    PubMed  Article  CAS  Google Scholar 

  24. Shadmehr R. and Brashers-Krug T. (1997) Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409–419.

    PubMed  CAS  Google Scholar 

  25. Halsband U. and Freund H. J. (1993) Motor learning. Curr. Opin. Neurobiol. 3, 940–949.

    PubMed  Article  CAS  Google Scholar 

  26. Floyer-Lea A. and Matthews P. M. (2005) Distinguishable brain activation networks for short- and long-term motor skill learning. J. Neurophysiol., 94, 512–518.

    PubMed  Article  CAS  Google Scholar 

  27. Karni A., Meyer G., Jezzard P., Adams M. M., Turner R., and Ungerleider L. G. (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155–158.

    PubMed  Article  CAS  Google Scholar 

  28. Honda M., Deiber M. P., Ibanez V., Pascual-Leone A., Zhuang P., and Hallett M. (1998) Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study. Brain 121 (Pt 11), 2159–2173.

    PubMed  Article  Google Scholar 

  29. Hund-Georgiadis M. and von Cramon D. Y. (1999) Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals. Exp. Brain Res. 125, 417–425.

    PubMed  Article  CAS  Google Scholar 

  30. Costa R. M., Cohen D., and Nicolelis M. A. (2004) Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr. Biol. 14, 1124–1134.

    PubMed  Article  CAS  Google Scholar 

  31. Nudo R. J., Milliken G. W., Jenkins W. M., and Merzenich M. M. (1996) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16, 785–807.

    PubMed  CAS  Google Scholar 

  32. Kleim J. A., Barbay S., and Nudo R. J. (1998) Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 80, 3321–3325.

    PubMed  CAS  Google Scholar 

  33. Kleim J. A., Bruneau R., Calder K., et al. (2003) Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron 40, 167–176.

    PubMed  Article  CAS  Google Scholar 

  34. Kleim J. A., Hogg T. M., VandenBerg P. M., Cooper N. R., Bruneau R., and Remple M. (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24, 628–633.

    PubMed  Article  CAS  Google Scholar 

  35. Sakai K., Hikosaka O., Miyauchi S., Sasaki Y., Fujimaki N., and Putz B. (1999) Presupplementary motor area activation during sequence learning reflects visuo-motor association. J. Neurosci. 19, RC1.

    Google Scholar 

  36. Nakamura K., Sakai K., and Hikosaka O. (1998) Neuronal activity in medial frontal cortex during learning of sequential procedures. J. Neurophysiol. 80, 2671–2687.

    PubMed  CAS  Google Scholar 

  37. Sakai K., Hikosaka O., Miyauchi S., Takino R., Sasaki Y., and Putz B. (1998) Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. J. Neurosci. 18, 1827–1840.

    PubMed  CAS  Google Scholar 

  38. Kennerley S. W., Sakai K., and Rushworth M. F. (2004) Organization of action sequences and the role of the pre-SMA. J. Neurophysiol. 91, 978–993.

    PubMed  Article  Google Scholar 

  39. Jenkins I. H., Brooks D. J., Nixon P. D., Frackowiak R. S., and Passingham R. E. (1994) Motor sequence learning: a study with positron emission tomography. J. Neurosci. 14, 3775–3790.

    PubMed  CAS  Google Scholar 

  40. Muller R. A., Kleinhans N., Pierce K., Kemmotsu N., and Courchesne E. (2002) Functional MRI of motor sequence acquisition: effects of learning stage and performance. Brain Res. Cogn. Brain Res. 14, 277–293.

    PubMed  Article  Google Scholar 

  41. Grafton S. T., Hazeltine E., and Ivry R. B. (2002) Motor sequence learning with the nondominant left hand. A PET functional imaging study. Exp. Brain Res. 146, 369–378.

    PubMed  Article  Google Scholar 

  42. Toni I., Krams M., Turner R., and Passingham R. E. (1998) The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8, 50–61.

    PubMed  Article  CAS  Google Scholar 

  43. Binkofski F., Amunts K., Stephan K. M., et al. (2000) Broca’s region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Hum. Brain Mapp. 11, 273–285.

    PubMed  Article  CAS  Google Scholar 

  44. Hikosaka O., Nakamura K., Sakai K., and Nakahara H. (2002) Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222.

    PubMed  Article  CAS  Google Scholar 

  45. Tracy J. I., Faro S. S., Mohammed F., Pinus A., Christensen H., and Burkland D. (2001) A comparison of ‘Early’ and ‘Late’ stage brain activation during brief practice of a simple motor task. Brain Res. Cogn. Brain Res. 10, 303–316.

    PubMed  Article  CAS  Google Scholar 

  46. Miyachi S., Hikosaka O., and Lu X. (2002) Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp. Brain Res. 146, 122–126.

    PubMed  Article  Google Scholar 

  47. Doyon J., Song A. W., Karni A., Lalonde F., Adams M. M., and Ungerleider L. G. (2002) Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc. Natl. Acad. Sci. USA 99, 1017–1022.

    PubMed  Article  CAS  Google Scholar 

  48. Deiber M. P., Wise S. P., Honda M., Catalan M. J., Grafman J., and Hallett M. (1997) Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J. Neurophysiol. 78, 977–991.

    PubMed  CAS  Google Scholar 

  49. Shadmehr R. and Holcomb H. H. (1997) Neural correlates of motor memory consolidation. Science 277, 821–825.

    PubMed  Article  CAS  Google Scholar 

  50. Schlaug G., Sanes J. N., Thangaraj V., et al. (1996) Cerebral activation covaries with movement rate. Neuroreport 22, 879–883.

    Article  Google Scholar 

  51. van Mier H., Tempel L. W., Perlmutter J. S., Raichle M. E., and Petersen S. E. (1998) Changes in brain activity during motor learning measured with PET: effects of hand of performance and practice. J. Neurophysiol. 80, 2177–2199.

    PubMed  Google Scholar 

  52. Luft A. R., Buitrago M. M., Ringer T., Dichgans J., and Schulz J. B. (2004) Motor skill learning depends on protein synthesis in motor cortex after training. J. Neurosci. 24, 6515–6520.

    PubMed  Article  CAS  Google Scholar 

  53. Debiec J., LeDoux J. E., and Nader K. (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36, 527–538.

    PubMed  Article  CAS  Google Scholar 

  54. Milekic M. H. and Alberini C. M. (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36, 521–525.

    PubMed  Article  CAS  Google Scholar 

  55. Seeds N. W., Williams B. L., and Bickford P. C. (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270, 1992–1994.

    PubMed  Article  CAS  Google Scholar 

  56. Kleim J. A., Lussnig E., Schwarz E. R., Comery T. A., and Greenough W. T. (1996) Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16, 4529–4535.

    PubMed  CAS  Google Scholar 

  57. Kleim J. A., Vij K., Ballard D. H., and Greenough W. T. (1997) Learning-dependent synaptic modifications in the cerebellar cortex of the adult rat persist for at least four weeks. J. Neurosci. 17, 717–721.

    PubMed  CAS  Google Scholar 

  58. Seitz R. J., Canavan A. G., Yaguez L., et al. (1994) Successive roles of the cerebellum and premotor cortices in trajectorial learning. Neuroreport 20, 2541–2544.

    Article  Google Scholar 

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Correspondence to Andreas R. Luft.

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Luft, A.R., Buitrago, M.M. Stages of motor skill learning. Mol Neurobiol 32, 205–216 (2005). https://doi.org/10.1385/MN:32:3:205

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  • DOI: https://doi.org/10.1385/MN:32:3:205

Index Entries

  • Motor learning
  • plasticity
  • memory
  • electrophysiology
  • gene
  • functional imaging
  • protein synthesis