Stages of motor skill learning

Molecular Neurobiology

Volumn 32, Issue 3, 2005, Pages 205-216

  Luft, Andreas R ^a   Buitrago, Manuel M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Electrophysiology; Functional imaging; Gene; Memory; Motor learning; Plasticity; Protein synthesis

Indexed keywords

BEHAVIOR; BRAIN; ELECTROPHYSIOLOGY; GENE FUNCTION; HUMAN; LEARNING; MOTOR PERFORMANCE; PROTEIN SYNTHESIS; REVIEW; WORKING MEMORY;

EID: 28644452229     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1385/MN:32:3:205     Document Type: Review

References (58)

1. Thompson R. F. (1986) The neurobiology of learning and memory. Science 233, 941-947.
2. Ito M. (1993) Neurophysiology of the nodulofloccular system. Rev. Neurol. (Paris) 149, 692-697.
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.
4. Nissen M. J., Knopman D. S., and Schacter D. L. (1987) Neurochemical dissociation of memory systems. Neurology 37, 789-794.
5. Brashers-Krug T., Shadmehr R., and Bizzi E. (1996) Consolidation in human motor memory. Nature 382, 252-255.
6. Sanes J. N. (2003) Neocortical mechanisms in motor learning. Curr. Opin. Neurobiol. 13, 225-231.
7. Asanuma H. and Pavlides C. (1997) Neurobiological basis of motor learning in mammals. Neuroreport 8, i-vi.
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.
9. Lee T. D. and Genovese E. D. (1989) Some reminiscences on distribution of practice effects. Res. Q. Exerc. Sport. 60, 297-299.
10. Adams J. A. (1961) The second facet of forgetting: a review of the warm-up decrement. Psycholog. Bull. 58, 257-273.
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.
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.
13. Jeannerod M. (1995) Mental imagery in the motor context. Neuropsychologia 33, 1419-1432.
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.
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.
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.
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.
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.
19. Hikosaka O., Nakahara H., Rand M. K., et al. (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci. 22, 464-471.
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.
21. Rizzolatti G. and Craighero L. (2004) The mirror-neuron system. Annu. Rev. Neurosci. 27, 169-192.
22. Sakai K., Hikosaka O., and Nakamura K. (2004) Emergence of rhythm during motor learning. Trends Cogn. Sci. 8, 547-553.
23. Eversheim U. and Bock O. (2001) Evidence for processing stages in skill acquisition: a dual-task study. Learn. Mem. 8, 183-189.
24. Shadmehr R. and Brashers-Krug T. (1997) Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409-419.
25. Halsband U. and Freund H. J. (1993) Motor learning. Curr. Opin. Neurobiol. 3, 940-949.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
44. Hikosaka O., Nakamura K., Sakai K., and Nakahara H. (2002) Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217-222.
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.
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.
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.
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.
49. Shadmehr R. and Holcomb H. H. (1997) Neural correlates of motor memory consolidation. Science 277, 821-825.
50. Schlaug G., Sanes J. N., Thangaraj V., et al. (1996) Cerebral activation covaries with movement rate. Neuroreport 22, 879-883.
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.
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.
53. Debiec J., LeDoux J. E., and Nader K. (2002) Cellular and systems reconsolidation in the hippocampus. Neuron 36, 527-538.
54. Milekic M. H. and Alberini C. M. (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36, 521-525.
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.
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.
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.
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.