Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task

Journal of Neurophysiology

Volumn 89, Issue 2, 2003, Pages 1039-1056

  Lee, Daeyeol ^a   Quessy, Stephan ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ELECTROENCEPHALOGRAM; HAND MOVEMENT; LEARNING; MALE; MONKEY; MOTOR ACTIVITY; MOTOR CORTEX; NERVE CELL; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; REACTION TIME; TASK PERFORMANCE; VISUOMOTOR COORDINATION;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); ELECTROPHYSIOLOGY; MACACA MULATTA; MALE; MODELS, NEUROLOGICAL; MOTOR CORTEX; MOVEMENT; NEURONS; PSYCHOMOTOR PERFORMANCE; REACTION TIME;

EID: 0037319180     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00638.2002     Document Type: Article

References (78)

1. Adams JA. A closed-loop theory of motor learning. J Mot Behav 3: 111-150, 1971.
2. Bach M and Krüger J. Correlated neuronal variability in monkey visual cortex revealed by a multi-microelectrode. Exp Brain Res 61: 451-456, 1986.
3. Bair W, Zohary E, and Newsome WT. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J Neurosci 21: 1676-1697, 2001.
4. Barone P and Joseph J-P. Prefrontal cortex and spatial sequencing in macaque monkey. Exp Brain Res 78: 447-464, 1989.
5. Bichot NP and Schall JD. Priming in macaque frontal cortex during popout visual search: feature-based facilitation and location-based inhibition of return. J Neurosci 22: 4675-4685, 2002.
6. Braitenberg V. Is the cerebellar cortex a biological clock in the millisecond range? Prog Brain Res 25: 334-346, 1967.
7. Brinkman C. Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4: 918-929, 1984.
8. Clower WT and Alexander GE. Movement sequence-related activity reflecting numerical order of components in supplementary and presupplementary motor areas. J Neurophysiol 80: 1562-1566, 1998.
9. Dassonville P, Lewis SM, Zhu X-H, Ugurbil K, Kim SG, and Ashe J. The effect of stimulus-response compatibility on cortical motor activation. Neuroimage 13: 1-14, 2001.
10. Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, and Frackowiak RS. Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84: 393-402, 1991.
11. Doyon J, Song AW, Karni A, Lalonde F, Adams MM, and Ungerleider LG. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc Natl Acad Sci USA 99: 1017-1022, 2002.
12. Eccles JC. The initiation of voluntary movements by the supplementary motor area. Arch Psychiatr Nervenkr 231: 423-441, 1982.
13. Fitts PM and Posner MI. Human Performance. Belmont, CA: Brooks/Cole, 1967.
14. Fu Q-G, Flament D, Coltz JD, and Ebner TJ. Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol 73: 836-854, 1995.
15. Fu Q-G, Flament D, Coltz JD, and Ebner TJ. Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J Neurophysiol 78: 478-491, 1997.
16. Fuji N, Mushiake H, and Tanji J. Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and pre-SMA of monkeys. J Neurophysiol 87: 2158-2166, 2002.
17. Goldberg G. Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8: 567-616, 1985.
18. Grafton ST, Hazeltine E, and Ivry R. Functional mapping of sequence learning in normal humans. J Cogn Neurosci 7: 497-510, 1995.
19. Grafton ST, Hazeltine E, and Ivry RB. Abstract and effector-specific representations of motor sequences identified with PET. J Neurosci 18: 9420-9428, 1998.
20. Halsband U, Ito N, Tanji J, and Freund H-J. The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 116: 243-266, 1993.
21. Hazeltine E, Grafton ST, and Ivry R. Attention and stimulus characteristics determine the locus of motor-sequence encoding: a PET study. Brain 120: 123-140, 1997.
22. Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, and Doya K. Parallel neural networks for learning sequential procedures. Trends Neurosci 22: 464-471, 1999.
23. Howard JH, Mutter SA, and Howard DV. Serial pattern learning by event observation. J Exp Psychol Learn Mem Cogn 18: 1029-1039, 1992.
24. Ivry RB, Keele SW, and Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res 73: 167-180, 1988.
25. Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RSJ, and Passingham RE. Motor sequence learning: a study with positron emission tomography. J Neurosci 14: 3775-3790, 1994.
26. Johnson MTV and Ebner TJ. Processing of multiple kinematic signals in the cerebellum and motor cortices. Brain Res Rev 33: 155-168, 2000.
27. Jueptner M, Frith CD, Brooks DJ, Frackowiak RSJ, and Passingham RE. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J Neurophysiol 77: 1325-1337, 1997a.
28. Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RSJ, and Passingham RE. Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol 77: 1313-1324, 1997b.
29. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, and Ungerleider LG. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377: 155-158, 1995.
30. Kermadi I and Joseph JP. Activity in the caudate nucleus of monkey during spatial sequencing. J Neurophysiol 74: 911-933, 1995.
31. Kurata K and Wise SP. Premotor and supplementary motor cortex in rhesus monkeys: neuronal activity during externally- and internally-instructed motor tasks. Exp Brain Res 72: 237-248, 1988.
32. Laplane D, Talairach J, Meininger V, Bancaud J, and Orgogozo JM. Clinical consequences of corticectomies involving the supplementary motor area in man. J Neurol Sci 34: 301-314, 1977.
33. Lee D and Malpeli JG. Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J Neurophysiol 79: 922-936, 1998.
34. Li L, Miller EK, and Desimone R. The representation of stimulus familiarity in anterior inferior temporal cortex. J Neurophysiol 69: 1918-1929, 1993.
35. Luppino G, Matelli M, Camarda R, and Rizzolatti G. Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338: 114-140, 1993.
36. Luppino G, Matelli M, and Rizzolatti G. Corticocortical connections of two electrophysiologically identified arm representations in the mesial agranular frontal cortex. Exp Brain Res 82: 214-218, 1990.
37. MacPherson JM and Aldridge JW. A quantitative method of computer analysis of spike train data collected from behaving animals. Brain Res 175: 183-187, 1979.
38. Matsuzaka Y, Aizawa H, and Tanji J. A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. J Neurophysiol 68: 653-662, 1992.
39. Matsuzaka Y and Tanji J. Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex. J Neurophysiol 76: 2327-2342, 1996.
40. Maylor E. Facilitatory and inhibitory components of orienting in visual space. Attention Perform 11: 189-204, 1985.
41. Meegan DV, Aslin RN, and Jacobs RA. Motor timing learned without motor training. Nat Neurosci 3: 860-862, 2000.
42. Mitz AR and Wise SP. The somatotopic organization of the supplementary motor area: intracortical microstimulation mapping. J Neurosci 7: 1010-1021, 1987.
43. Mushiake H, Inase M, and 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.
44. Mushiake H and Strick PL. Pallidal neuron activity during sequential arm movements. J Neurophysiol 74: 2754-2758, 1995.
45. Nakamura K, Sakai K, and Hikosaka O. Neuronal activity in medial frontal cortex during learning of sequential procedures. J Neurophysiol 80: 2671-2687, 1998.
46. Nissen MJ and Bullemer P. Attentional requirements of learning: evidence from performance measures. Cogn Psychol 19: 1-32, 1987.
47. Okano K and Tanji J. Neuronal activities in the primate motor fields of the agranular frontal cortex preceding visually triggered and self-paced movement. Exp Brain Res 66: 155-166, 1987.
48. Penfield W and Welch K. The supplementary motor area of the cerebral cortex. Arch Neurol Psychiatry 66: 289-317, 1951.
49. Petit L, Courtney SM, Ungerleider LG, and Haxby JV. Sustained activity in the medial wall during working memory delays. J Neurosci 18: 9429-9437, 1998.
50. Picard N and Strick PL. Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6: 342-353, 1996.
51. Posner MI and Cohen Y. Components of visual orienting. Attention Perform 10: 531-556, 1984.
52. Rauch SL, Savage CR, Brown HD, Curran T, Alpert NM, Kendrick A, Fischman AJ, and Kosslyn SM. A PET investigation of implicit and explicit sequence learning. Hum Brain Map 3: 271-286, 1995.
53. Rauch SL, Whalen PJ, Savage CR, Curran T, Kendrick A, Brown HD, Bush G, Breiter HC, and Rosen BR. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum Brain Map 5: 125-132, 1997.
54. Rizzolatti G, Matelli M, and Pavesi G. Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106: 655-673, 1983.
55. Roland PE, Larsen B, Lassen NA, and Skinhøj E. Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiol 43: 118-136, 1980.
56. Romo R and Schultz W. Neuronal activity preceding self-initiated or externally timed arm movements in area 6 of monkey cortex. Exp Brain Res 67: 656-662, 1987.
57. Rose D. An analysis of the variability of unit activity in the cat's visual cortex. Exp Brain Res 37: 595-604, 1979.
58. Sakai K, Hikosaka O, Miyauchi S, Sasaki Y, Fujimaki N, and Pütz B. Presupplementary motor area activation during sequence learning reflects visuo-motor association. J Neurosci 19: 1-6, 1999.
59. Sakai K, Hikosaka O, Miyauchi S, Takino R, Sasaki Y, and Pütz B. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. J Neurosci 18: 1827-1840, 1998.
60. Sakai K, Ramnani N, and Passingham RE. Learning of sequences of finger movements and timing: frontal lobe and action-oriented representation. J Neurophysiol 88: 2035-2046, 2002.
61. Seidler RD, Purushotham A, Kim S-G, Uǧurbil K, Willingham D, and Ashe J. Cerebellum activation associated with performance change but not motor learning. Science 296: 2043-2046, 2002.
62. Seitz RJ and Roland PE. Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study. Ear J Neurosci 4: 154-165, 1992.
63. Shidara M, Aigner TG, and Richmond BJ. Neuronal signals in the monkey ventral striatum related to progress through a predictable series of trials. J Neurosci 18: 2613-2625, 1998.
64. Shidara M and Richmond BJ. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296: 1709-1711, 2002.
65. Shima K, Mushiake H, Saito N, and Tanji J. Role for cells in the presupplementary motor area in updating motor plans. Proc Natl Acad Sci USA 93: 8694-8698, 1996.
66. Shima K and Tanji J. Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. J Neurophysiol 84: 2148-2160, 2000.
67. Snedecor GW and Cochran WG. Statistical Methods (8th ed.). Ames, IA: Iowa State University Press, 1989.
68. Stevens J. Applied Multivariate Statistics for the Social Sciences (3rd ed.). Mahwah. NJ: Erlbaum Associates, 1996.
69. Tanaka Y and Shimojo S. Location versus feature: reaction time reveals dissociation between two visual features. Vision Res 36: 2125-2140, 1996.
70. Tanaka Y and Shimojo S. Repetition priming reveals sustained facilitation and transient inhibition in reaction time. J Exp Psychol Hum Percept Perform 26: 1421-1435, 2000.
71. Tanji J. Sequential organization of multiple movements: involvement of cortical motor areas. Annu Rev Neurosci 24: 631-651, 2001.
72. Tanji J, Okano K, and Sato KC. Relation of neurons in the nonprimary motor cortex to bilateral hand movement. Nature 327: 618-619, 1987.
73. Tanji J, Okano K, and Sato KC. Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol 60: 325-343, 1988.
74. Tanji J and Shima K. Role for supplementary motor area cells in planning several movements ahead. Nature 371: 413-416, 1994.
75. Thaler DE, Rolls ET, and Passingham RE. Neuronal activity of the supplementary motor area (SMA) during internally and externally triggered wrist movements. Neurosci Lett 93: 264-269, 1988.
76. van Mier H, Tempel LW, Perlmutter JS, Raichle ME, and Petersen SE. Changes in brain activity during motor learning measured with PET: effects of hand of performance and practice. J Neurophysiol 80: 2177-2199, 1998.
77. Willingham DB, Salidis J, and Gabrieli JDE. Direct comparison of neural systems mediating conscious and unconscious skill learning. J Neurophysiol 88: 1451-1460, 2002.
78. Woolsey CN, Settlage PH, Meyer DR, Sencer W, Hamuy TP, and Travis AM. Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30: 238-264, 1952.