Skill representation in the primary motor cortex after long-term practice

Journal of Neurophysiology

Volumn 97, Issue 2, 2007, Pages 1819-1832

  Matsuzaka, Yoshiya ^b,c   Picard, Nathalie ^a,b   Strick, Peter L ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; KINEMATICS; MACACA; MONKEY; MOTOR CORTEX; MOVEMENT (PHYSIOLOGY); NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SKILL; TASK PERFORMANCE; TRAINING;

ANIMALS; ATTENTION; BIOMECHANICS; ELECTROMYOGRAPHY; EYE MOVEMENTS; LEARNING; MACACA MULATTA; MEMORY; MOTOR CORTEX; MOTOR SKILLS; PHOTIC STIMULATION; PRACTICE (PSYCHOLOGY); PSYCHOMOTOR PERFORMANCE; SERIAL LEARNING;

EID: 33846916162     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00784.2006     Document Type: Article

References (57)

1. Asanuma H. Neuronal mechanisms of motor learning in mammals. Neuroreport 2: 217-224, 1991.
2. Ashe J, Georgopoulos AP. Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex 6: 590-600, 1994.
3. Ashe J, Taira M, Smyrnis N, Pellizzer G, Georgakopoulos T, Lurito JT, Georgopoulos AP. Motor cortical activity preceding a memorized movement trajectory with an orthogonal bend. Exp Brain Res 95: 118-130, 1993.
4. Ben-Shaul Y, Drori R, Asher I, Stark E, Nadasdy Z, Abeles M. Neuronal activity in motor cortical areas reflects the sequential context of movement. J Neurophysiol 91: 1748-1762, 2004.
5. Campbell AW. Histological Studies on the Localization of Cerebral Function. Cambridge, UK: Cambridge Univ. Press, 1905.
6. Carpenter AF, Georgopoulos AP, Pellizzer G. Motor cortical encoding of serial order in a context-recall task. Science 283: 1752-1757, 1999.
7. Cunnington R, Windischberger C, Deecke L, Moser E. The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 15: 373-385, 2002.
8. Debaere F, Wenderoth N, Sunaert S, Van Hecke P, Swinnen SP. Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback. Neuroimage 19: 764-776, 2003.
9. Fu Q-G, Flament D, Coltz JD, Ebner TJ. Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol 73: 836-854, 1995.
10. Fu Q-G, Suarez JI, Ebner TJ. Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex. J Neurophysiol 70: 2097-2116, 1993.
11. Fulton JF. Definition of the "motor" and "premotor" areas. Brain 58: 311-316, 1935.
12. Gandolfo F, Li C, Benda BJ, Schioppa CP, Bizzi E. Cortical correlates of learning in monkeys adapting to a new dynamical environment. Proc Natl Acad Sci USA 97: 2259-2263, 2000.
13. Georgopoulos AP, Kalsaka JF, Massey JT. Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. J Neurophysiol 46: 725-743, 1981.
14. Halsband U, Matsuzaka Y, Tanji J. Neuronal activity in the primate supplementary, pre-supplementary and premotor cortex during externally and internally instructed sequential movements. Neurosci Res 20: 149-155, 1994.
15. Hatsopoulos NG, Paninski L, Donoghue JP. Sequential movement representations based on correlated neuronal activity. Exp Brain Res 149: 478-486, 2003.
16. Hund-Georgiadis M, von Cramon DY. Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals. Exp Brain Res 125: 417-425, 1999.
17. Iriki A, Pavlides C, Keller A, Asanuma H. Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. J Neurophysiol 65: 1435-1441, 1991.
18. Jacobsen CF. Influence of motor and premotor lesions upon retention of acquired skilled movements in monkey and chimpanzees. Assoc Res Nerv Ment Dis 13: 225-247, 1934.
19. Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ. Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. Brain 118: 913-933, 1995.
20. Jenkins IH, Jahanshahi M, Jueptner M, Passingham RE, Brooks DJ. Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. Brain 123: 1216-1228, 2000.
21. Kakei S, Hoffman DS, Strick PL. Muscle and movement representations in the primary motor cortex. Science 285: 2136-2139, 1999.
22. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377: 155-158, 1995.
23. Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95: 861-868, 1998.
24. Kleim JA, Barbay S, Nudo RJ. Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80: 3321-3325, 1998.
25. Kleim JA, Bruneau R, Calder K, Pocock D, VandenBerg PM, MacDonald E, Monfils MH, Sutherland RJ, Nader K. Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron 40: 167-176, 2003.
26. Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24: 628-633, 2004.
27. Kwan HC, MacKay WA, Murphy JT, Wong YC. Spatial organization of precentral cortex in awake primates. II. Motor outputs. J Neurophysiol 41: 1120-1131, 1978.
28. Li CSR, Padoa-Schioppa C, Bizzi E. Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30: 593-607, 2001.
29. Lu X, Ashe J. Anticipatory activity in primary motor cortex codes memorized movement sequences. Neuron 45: 967-973, 2005.
30. Lu X, Matsuzawa M, Hikosaka O. A neural correlate of oculomotor sequences in supplementary eye field. Neuron 34: 317-325, 2002.
31. Matsuzaka Y, Picard N, Strick PL. Sequence learning in monkeys. Soc Neurosci Abstr 24: 174, 1998.
32. Matsuzaka Y, Picard N, Strick PL. Activity of M1 neurons associated with over-practiced sequential movements. Soc Neurosci Abstr 26: 1483, 2000.
33. Monfils M-H, Teskey GC. Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation. Neuroscience 125: 329-336, 2004.
34. Moran DW, Schwartz AB. Motor cortical representation of speed and direction during reaching. J Neurophysiol 82: 2676-2692, 1999.
35. Mushiake H, Inase M, Tanji J. Selective coding of motor sequence in the supplementary motor area of the monkey cerebral cortex. Exp Brain Res 82: 208-210, 1990.
36. Mushiake H, Inase M, Tanji J. Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. J Neurophysiol 66: 705-718, 1991.
37. Nakamura K, Sakai K, Hikosaka O. Neuronal activity in medial frontal cortex during learning of sequential procedures. J Neurophysiol 80: 2671-2687, 1998.
38. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16: 785-807, 1996.
39. Nudo RJ, Plautz EJ, Milliken GW. Adaptive plasticity in primate motor cortex as a consequence of behavioral experience and neuronal injury. Semin Neurosci 9: 13-23, 1997.
40. Park MC, Belhaj-Saïf A, Gordon M, Cheney PD. Consistent features in the forelimb representation of primary motor cortex in rhesus macaques. J Neurosci 21: 2784-2792, 2001.
41. Pascual-Leone A, Dang N, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74: 1037-1045, 1995.
42. Pascual-Leone A, Grafman J, Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263: 1287-1289, 1994.
43. Paz R, Boraud T, Natan C, Bergman H, Vaadia E. Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6: 882-890, 2003.
44. Picard N, Strick PL. Activation of the supplementary motor area (SMA) during performance of visually-guided movements. Cereb Cortex 13: 977-986, 2003.
45. Plautz EJ, Milliken GW, Nudo RJ. Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74: 27-55, 2000.
46. Prablanc C, Martin O. Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67: 455-469, 1992.
47. Qi HX, Stepniewska I, Kaas JH. Reorganization of primary motor cortex in adult macaque monkeys with long-standing amputations. J Neurophysiol 84: 2133-2147, 2000.
48. Remple MS, Bruneau RM, VandenBerg PM, Goertzen C, Kleim JA. Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav Brain Res 123: 133-141, 2001.
49. Rioult-Pedotti M-S, Friedman D, Donoghue JP. Learning-induced LTP in neocortex. Science 290: 533-536, 2000.
50. Rioult-Pedotti M-S, Friedman D, Hess G, Donoghue JP. Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1: 230-234, 1998.
51. Sanes JN, Donoghue JP. Plasticity and primary motor cortex. Annu Rev Neurosci 23: 393-415, 2000.
52. Sergio LE, Hamel-Pâquet C, Kalaska JF. Motor cortex neuronal correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. J Neurophysiol 94: 2353-2378, 2005.
53. Snedecor GW, Cochran WG. Statistical Methods. Ames, IA: The Iowa State Univ. Press, 1980.
54. Stefan K, Wycislo M, Gentner R, Schramm A, Naumann M, Reiners K, Classen J. Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex 16: 376-385, 2006.
55. Tanji J, Shima K. Role of supplementary motor area cells in planning several movements ahead. Nature 371: 413-416, 1994.
56. Tyčè F, Boyadjian A, Devanne H. Motor cortex plasticity induced by extensive training revealed by transcranial magnetic stimulation in human. Eur J Neurosci 21: 259-266, 2005.
57. Ziemann U, Iliaćæ TV, Pauli C, Meintzschel F, Ruge D. Learning modifies subsequent induction on long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24: 1666-1672, 2004.