Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study

Brain

Volumn 121, Issue 11, 1998, Pages 2159-2173

  Honda, Manabu ^a,b   Deiber, Marie Pierre ^a   Ibáñez, Vicente ^a   Pascual Leone, Alvaro ^a,c   Zhuang, Ping ^a   Hallett, Mark ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Explicit learning; Implicit learning; Motor sequence; PET; Serial reaction time task

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN BLOOD FLOW; BRAIN CORTEX; FEMALE; FINGER; HUMAN; LEARNING; MALE; MENTAL PERFORMANCE; MOTOR CORTEX; NORMAL HUMAN; PARIETAL LOBE; PHOTON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; REACTION TIME; SENSORIMOTOR CORTEX;

ADULT; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CEREBELLUM; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; MIDDLE AGED; MOTOR ACTIVITY; PARIETAL LOBE; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SERIAL LEARNING; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0031736616     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/121.11.2159     Document Type: Article

References (74)

1. Barone P, Joseph JP. Prefrontal cortex and spatial sequencing in macaque monkey. Exp Brain Res 1989; 78: 447-64.
2. Brooks DJ. The role of the basal ganglia in motor control: contributions from PET. J Neurol Sci 1995; 128: 1-13.
3. Chen LL, Wise SP. Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 1995; 73: 1101-21.
4. Chen R, Gerloff C, Hallett M, Cohen LG. Involvement of the ipsilateral motor cortex in finger movements of different complexities. Ann Neurol 1997; 41: 247-54.
5. Cohen NJ, Squire LR. Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of 'knowing how' and 'knowing that'. Science 1980; 210: 207-10.
6. Cohen A, Ivry RI, Keele SW. Attention and structure in sequence learning. J Exp Psychol Learn Mem Cogn 1990; 16: 17-30.
7. Curran T, Keele SW. Attentional and nonattentional forms of sequence learning. J Exp Psychol Learn Mem Cogn 1993; 19: 189-202.
8. Doyon J, Owen AM, Petrides M, Sziklas V, Evans AC. Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography. Eur J Neurosci 1996; 8: 637-48.
9. 15O tissue activity. J Nucl Med 1989; 30: 141-9.
10. Fox PT, Raichle ME. Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J Neurophysiol 1984; 51: 1109-20.
11. 15O and positron emission tomography. J Cereb Blood Flow Metab 1984; 4: 329-33.
12. Frensch PA, Miner CS. Effects of presentation rate and individual differences in short-term memory capacity on an indirect measure of serial learning. Mem Cognit 1994; 22: 95-110.
13. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Comparing functional (PET) images: the assessment of significant change. J Cereb Blood Flow Metab 1991; 11: 690-9.
14. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 1993; 13: 5-14.
15. Friston KJ, Worsley KJ, Frackowiak RSJ, Mazziotta JC, Evans AC. Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1994; 1: 210-20.
16. Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RSJ. Spatial registration and normalization of images. Hum Brain Mapp 1995a; 3: 165-89.
17. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995b; 2: 189-210.
18. Graf P, Schacter DL. Implicit and explicit memory for new associations in normal and amnesic subjects. J Exp Psychol Learn Mem Cogn 1985; 11: 501-18.
19. Grafton ST, Mazziotta JC, Presty S, Friston KJ, Frackowiak RS, Phelps ME. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci 1992; 12: 2542-8.
20. Grafton ST, Woods RP, Mazziotta JC. Within-arm somatotopy in human motor areas determined by positron emission tomography imaging of cerebral blood flow. Exp Brain Res 1993; 95: 172-6.
21. Grafton ST, Woods RP, Tyszka M. Functional imaging of procedural motor learning: relating cerebral blood flow with individual subject performance. Hum Brain Mapp 1994; 1: 221-34.
22. Grafton ST, Hazeltine E, Ivry R. Functional mapping of sequence learning in normal humans. J Cogn Neurosci 1995; 7: 497-510.
23. Halsband U, Freund HJ. Premotor cortex and conditional motor learning in man. Brain 1990; 113: 207-22.
24. Hazeltine E, Grafton ST, Ivry R. Attention and stimulus characteristics determine the locus of motor-sequence encoding. Brain 1997; 120: 123-40.
25. Hikosaka O, Sakai K, Miyauchi S, Takino R, Sasaki Y, Putz B. Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study. J Neurophysiol 1996; 76: 617-21.
26. Ibáñez V, Deiber MP, Sadato N, Toro C, Grissom J, Woods RP, et al. Effects of stimulus rate on regional cerebral blood flow after median nerve stimulation. Brain 1995; 118: 1339-51.
27. Iriki A, Pavlides C, Keller A, Asanuma H. Long-term potentiation in the motor cortex. Science 1989; 245: 1385-7.
28. Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RS, Passingham RE. Motor sequence learning: a study with positron emission tomography. J Neurosci 1994; 14: 3775-90.
29. Joseph JP, Barone P. Prefrontal unit activity during a delayed oculomotor task in the monkey. Exp Brain Res 1987; 67: 460-8.
30. Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE, Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol 1997a; 77: 1313-24.
31. Jueptner M, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J Neurophysiol 1997b; 77: 1325-37.
32. 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 1995; 377: 155-8.
33. Keele SW, Jennings P, Jones S, Caulton D, Cohen A. On the modularity of sequence representation. J Mot Behav 1995; 27: 17-30.
34. Kettner RE, Marcario JK, Clark-Phelps MC. Control of remembered reaching sequences in monkey. I. Activity during movement in motor and premotor cortex. Exp Brain Res 1996a; 112: 335-46.
35. Kettner RE, Marcario JK, Port NL. Control of remembered reaching sequences in monkey. II. Storage and preparation before movement in motor and premotor cortex. Exp Brain Res 1996b; 112: 347-58.
36. Kitamura J, Shibasaki H, Takagi A, Nabeshima H, Yamaguchi A. Enhanced negative slope of cortical potentials before sequential as compared with simultaneous extensions of two fingers. Electroencephalogr Clin Neurophysiol 1993; 86: 176-82.
37. Knopman DS, Nissen MJ. Implicit learning in patients with probable Alzheimer's disease. Neurology 1987; 37: 784-8.
38. Luria AR. Higher cortical functions in man. New York: Basic Books; 1966.
39. Milner B, Corkin S, Teuber HL. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia 1968; 6: 215-34.
40. 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 1991; 66: 705-18.
41. Nissen MJ, Bullemer P. Attentional requirements of learning: evidence from performance measures. Cogn Psychol 1987; 19: 1-32.
42. Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 1971; 9: 97-113.
43. Pascual-Leone A, Torres F. Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 1993; 116: 39-52.
44. Pascual-Leone A, Cammarota A, Wassermann EM, Brasil-Neto JP, Cohen LG, Hallett M. Modulation of motor cortical ouptuts to the reading hand of Braille readers. Ann Neurol 1993; 34: 33-7.
45. Pascual-Leone A, Grafman J, Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge [see comments]. Science 1994; 263: 1287-9. Comment in: Science 1994; 265: 1600-1.
46. Pascual-Leone A, Grafman J, Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge [see comments]. Science 1994; 263: 1287-9. Comment in: Science 1994; 265: 1600-1.
47. 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 1995; 74: 1037-45.
48. Passingham RE. The frontal lobes and voluntary action. Oxford: Oxford University Press; 1993.
49. Pavlides C, Miyashita E, Asanuma H. Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J Neurophysiol 1993; 70: 733-41.
50. Perruchet P, Amorim M. Conscious knowledge and changes in performance in sequence learning: evidence against dissociation. J Exp Psychol Learn Mem Cogn 1992; 18: 785-800.
51. Petit L, Orssund C, Tzourio N, Crivello F, Berthoz A, Mazoyer B. Functional anatomy of a prelearned sequence of horizontal saccades in humans. J Neurosci 1996; 16: 3714-26.
52. Petrides M. Functional specialization within the dorsolateral frontal cortex for serial order memory. Proc R Soc Lond B Biol Sci 1991; 246: 299-306.
53. Picard N, Strick PL. Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 1996; 6: 342-53.
54. Price C, Wise R, Ramsay S, Fristen K, Howard D, Patterson K, et al. Regional response differences within the human auditory cortex when listening to words. Neurosci Lett 1992; 146: 179-82.
55. Rauch SL, Savage CR, Brown HD, Curran T, Alpert NM, Kendrick A, et al. A PET investigation of implicit and explicit sequence learning. Hum Brain Mapp 1995; 3: 271-86.
56. Sadato N, Campbell G, Ibáñez V, Deiber M, Hallett M. Complexity affects regional cerebral blood flow change during sequential finger movements. J Neurosci 1996a; 16: 2691-700.
57. Sadato N, Ibáñez V, Deiber MP, Campbell G, Leonardo M, Hallett M. Frequency-dependent changes of regional cerebral blood flow during finger movements. J Cereb Blood Fiow Metab 1996b; 16: 23-33.
58. Saint-Cyr JA, Taylor AE, Lang AE. Procedural learning and neostriatal dysfunction in man. Brain 1988; 111: 941-59.
59. Saint-Cyr JA, Taylor AE, Nicholson K. Behavior and the basal ganglia. Adv Neurol 1995; 65: 1-28.
60. Sakamoto T, Porter LL, Asanuma H. Long-lasting potentiation of synaptic potentials in the motor cortex produced by stimulation of the sensory cortex in the cat: a basis of motor learning. Brain Res 1987; 413: 360-4.
61. Sakamoto T, Arissian K, Asanuma H. Functional role of the sensory cortex in learning motor skills in cats. Brain Res 1989; 503: 258-64.
62. Schacter DL. Implicit knowledge: new perspectives on unconscious processes. Proc Natl Acad Sci USA 1992; 89: 11113-7.
63. Schacter DL, Chiu CY, Ochsner KN. Implicit memory: a selective review. Annu Rev Neurosci 1993; 16: 159-82.
64. Schlaug G, Knorr U, Seitz R. Inter-subject variability of cerebral activations in acquiring a motor skill: a study with positron emission tomography. Exp Brain Res 1994; 98: 523-34.
65. Schmidtke V, Heuer H. Task integration as a factor in secondary-task effects on sequence learning. Psychol Res 1997; 60: 53-71.
66. Shibasaki H, Sadato N, Lywhkow H, Yonekura Y, Honda M, Nagamine T, et al. Both primary motor cortex and supplementary motor area play an important role in complex finger movement. Brain 1993; 116: 1387-98.
67. Squire LR. Memory and brain. New York: Oxford University Press; 1987.
68. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human, brain.Stuttgart: Thieme; 1988.
69. Weiller C, Jüptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel, S et al. Brain representation of active and passive movements. Neuroimage 1996; 4: 105-10.
70. Willingham DB, Nissen MJ, Bullemer P. On the development of procedural knowledge. J Exp Psychol Learn Mem Cogn 1989; 15: 1047-60.
71. Worsley KJ, Evans AC, Marrett S, Neelin P. A three-dimensional statistical analysis for CBF activation studies in human brain [see comments]. J Cereb Blood Flow Metab 1992; 12: 900-18. Comment in: J Cereb Blood Flow Metab 1993; 13: 1040-2.
72. Worsley KJ, Evans AC, Marrett S, Neelin P. A three-dimensional statistical analysis for CBF activation studies in human brain [see comments]. J Cereb Blood Flow Metab 1992; 12: 900-18. Comment in: J Cereb Blood Flow Metab 1993; 13: 1040-2.
73. Zhang J, Riehle A, Requin J, Kornblum S. Dynamics of single neuron activity in monkey primary motor cortex related to sensorimotor transformation. J Neurosci 1997; 17: 2227-46.
74. Zhuang P, Toro C, Grafman J, Manganotti P, Leocani L, Hallett M. Event-related desynchronization (ERD) in the alpha frequency during development of implicit and explicit learning. Electroencephalogr Clin Neurophysiol 1997; 102: 374-81.