Patterns of regional brain activation associated with different forms of motor learning

Brain Research

Volumn 871, Issue 1, 2000, Pages 127-145

  Ghilardi, Maria Felice ^a,b   Ghez, Claude ^a   Dhawan, Vijay ^c,d   Moeller, James ^e   Mentis, Marc ^c,d   Nakamura, Toshitaka ^c,d   Antonini, Angelo ^c,d   Eidelberg, David ^c,d  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b CNR   (Italy)

^c NORTH SHORE UNIVERSITY HOSPITAL   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NONE   (United States)

Author keywords

Automaticity; Motor learning; Procedural learning; Reaching movements

Indexed keywords

ADAPTATION; ADULT; ARTICLE; BODY POSTURE; BRAIN BLOOD FLOW; ELECTROENCEPHALOGRAM; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MOTOR DEVELOPMENT; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL;

ADULT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; COGNITION; FEMALE; FUNCTIONAL LATERALITY; HUMANS; LEARNING; MALE; MIDDLE AGED; MOTOR ACTIVITY; ORGAN SPECIFICITY; OXYGEN RADIOISOTOPES; PSYCHOMOTOR PERFORMANCE; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 0034648097     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(00)02365-9     Document Type: Article

References (90)

1. G. Allen, R.B. Buxton, E.C. Wong, E. Courchesne, Attentional activation of the cerebellum independent of motor involvement, Science 275 (1997) 1940-1943.
2. N.C. Andreasen, D.S. O'Leary, S. Arndt, T. Cizadlo, R. Hurtig, K. Rezai, G.L. Watkins, L.L. Ponto, R.D. Hirchwa, Short-term and long-term verbal memory: A positron emission tomography study, Proc. Natl. Acad. Sci. USA 92 (1995) 5111-5115.
3. J.E. Birren, The Psychology of Aging, Prentice-Hall, Englewood Cliffs, NJ, 1964.
4. G. Bottini, R. Sterzi, E. Paulesu, G. Vallar, S. Cappa, F. Erminio, R.E. Passingham, C.D. Frith, R.S.J. Frackowiack, Identification of the central vestibular projections in man: a positron emission tomography activation study, Exp. Brain Res. 99 (1994) 164-169.
5. V.B. Brooks, W.T. Thach, Cerebellar control of posture and movement, in: V.B. Brooks (Ed.), Handbook of Physiology: Sec. 1. The Nervous System: Vol. 2. Motor Control, Part 2, American Physiological Society, Bethesda, MD, 1981, pp. 877-946.
6. P. Brotchie, R. Iansek, M.K. Home, Motor function of the monkey globus pallidus. 2. Cognitive aspects of movement and phasic neuronal activity, Brain 114 (1991) 1685-1702.
7. T.H. Carr, C. McCauley, R.D. Sperber, C.D. Parmalee, Words, pictures, and priming: On semantic activation, conscious identification, and the automaticity of information processing, Journal of Experimental Psychology: Human Perception and Performance (1982) 8757-777.
8. R.E. Clark, L.R. Squire, Classical conditioning and brain systems: the role of awareness, Science 280 (1998) 77-81.
9. D.M. Glower, J.M. Hoffman, J.R. Votaw, T.L. Faber, R. Woods, G.E. Alexander, Role of posterior parietal cortex in the recalibration of visually guided reaching, Nature 383 (1996) 618-621.
10. M. Corbetta, F.M. Miezin, S. Dobmeyer, G.L. Shulman, S.E. Petersen, Selective and divided attention during visual discrimination of shape, color and speed: functional anatomy by positron emission tomography, J. Neurosci. 11 (1991) 2383-2402.
11. M. Corbetta, G.L. Shulman, F.M. Miezin, S.E. Petersen, Superior parietal cortex activation during spatial attention shifts and visual feature conjunction, Science 270 (1995) 802-805.
12. H.A. Cunningham, Aiming error under transformed spatial mappings suggests a structure for visual-motor maps, J. Exp. Psychol.: Human Perception and Performance 15 (1989) 493-506.
13. M. D'Esposito, J.A. Detre, D.C. Alsop, R.K. Shin, S. Atlas, M. Grossman, The neural basis of the central executive system of working memory, Nature 378 (1995) 279-281.
14. T.R. DeGrado, T.G. Turkington, J.J. Williams, C.W. Stearns, Per formance characteristics of a whole-body PET scanner, J. Nucl. Med. 35 (1994) 1398-1406.
15. S.W.G. Derbyshire, B.A. Vogt, A.K.P. Jones, Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex, Exp. Brain Res. 118 (1998) 52-60.
16. V. Dhawan, K. Kazumata, W. Robeson, A. Belakhlef, C. Margouleff, T. Chaly, T. Nakamura, R. Dahl, D. Margouleff, D. Eideberg, Quantitative brain PET: Comparison of 2D and 3D acquisitions on the GE advance scanner, Clinical Positron Imaging 1 (1998) 135-144.
17. D. Eidelberg, A.M. Galaburda, Inferior parietal lobe, Arch. Neurol. 41 (1984) 843-852.
18. D. Ferrier, The Function of the Brain, Smith, Elder & Co, London, 1876.
19. G.R. Fink, P.W. Hlligan, J.C. Marshall, C.D. Frith, R.S.J. Frackowiack, R.J. Dolan, Where in the brain does visual attention select the forest and the three, Nature 382 (1996) 626-628.
20. P.C. Fletcher, C.D. Frith, P.M. Grasby, T. Shallice, R.S.J. Frackowiack, R.J. Dolan, Brain systems for encoding and retrieval of auditory-verbal memory, Brain 118 (1995).
21. P.C. Fletcher, T. Shallice, C.D. Frith, R.S.J. Frackowiack, R.J. Dolan, Brain activity during memory retrieval: the influence of imagery and semantic cueing, Brain 119 (1996) 1587-1596.
22. K. Friston, A.P. Holmes, K.J. Worsley, J.-P. Poline, C.D. Frith, R.S.J. Frackowiak, Statistical parametric maps in functional imaging: A general linear approach, Human Brain Mapping 2 (1995) 189-210.
23. K.J. Friston, C.D. Frith, P.F. Liddle, R. Frackowiak, Comparing functional (PET) images: the assessment of significant change, J. Cereb. Blood Flow Metab. 11 (1991) 690-699.
24. K.J. Friston, C.D. Frith, R.E. Passingham, P.F. Liddle, R.S. Frackowiak, Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study, Proc. R. Soc. Lond. [Biol.] 248 (1992) 223-228.
25. C.D. Frith, K. Friston, P.F. Liddle, R.S.J. Frackowiack, Willed action and the prefrontal cortex in man: a study with PET, Proc. R. Soc. Lond. B Biol. Sci. 244 (1991) 241-246.
26. J.-H. Gao, L.M. Parosns, J.M. Bower, J. Xiong, J. Li, P.T. Fox, Cerebellum implicated in sensory acquisition and discrimination rather than motor control, Science 272 (1996) 545-547.
27. C. Gerloff, N. Uenishi, T. Nagamine, T. Kunieda, M. Hallett, H. Shibasaki, Cortical activation during fast repetitive finger movements in humans: steady-state movement related magnetic fields and their cortical generators, Electroencephal. Clin. Neurophysiol. 109 (1998) 444-453.
28. C. Gerloff, L.G. Cohen, M.K. Floeter, R. Chen, B. Corwell, M. Hallett, Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract, J. Physiol. (London) 510 (1998) 249-259.
29. C. Ghez, Contributions of central programs to rapid limb movements in the cat, in: H. Asanuma, V.J. Wilson (Eds.), Integration in the Nervous System, Igaku-Shoin, Tokyo, 1979, pp. 305-320.
30. C. Ghez, J. Krakauer, R.L. Sainburg, M.F. Ghilardi, Spatial representations and internal models of limb dynamics in motor learning, in: G. M (Ed.), The Cognitive Neurosciences, 2nd Edition, MIT Press, Cambridge, MA, 1999, pp. 501-514.
31. C. Ghez, M. Favilla, M.F. Ghilardi, J. Gordon, R. Bermejo, S. Pullman, Discrete and continuous planning of hand movements and isometric force trajectories, Exp. Brain Res. 115 (1997) 217-233.
32. C. Ghez, D. Vicario, J.H. Martin, H. Yumiya, Sensory motor processing of targeted movements in motor cortex, in: J.E. Desmedt (Ed.), Advances in Neurology, Vol. 39: Motor Control Mechanisms in Health and Disease, Raven Press, New York, 1983, pp. 61-92.
33. M.A. Goodale, A.D. Milner, Separate visual pathways for perception and action, Trends Neurosci. 15 (1992) 20-25.
34. J. Gordon, C. Ghez, Trajectory control in targeted force impulses. III. Compensatory adjustments for initial errors, Exp. Brain Res. 67 (1987) 253-269.
35. C.L. Grady, A.R. McIntosh, B. Horwitz, J.M. Maisog, L.G. Ungerleider, M.J. Mentis, P. Pietrini, M.B. Schapiro, J.V. Haxby, Age-related reductions in human recognition memory due to impaired encoding, Science 269 (1995) 218-222.
36. S.T. Grafton, J.C. Mazziotta, S. Presty, K.H. Friston, R.S. Frackowiak, M.E. Phelps, Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET, J. Neurosci. 12 (1992) 2542-2548.
37. S.T. Grafton, J.C. Mazziotta, R.P. Woods, M.E. Phelps, Human functional anatomy of visually guided finger movements, Brain 115 (1992) 565-587.
38. M. Hariz, A. Eriksson, Reproducibility of repeated mountings of a noninvasive CT/MRI stereoadapter, Appl. Neurophysiol. 49 (1986) 336-347.
39. C. Harris, Perceptual adaptation to inverted reversed displaced vision, Psychol. Rev. 72 (1965) 419-444.
40. J.V. Haxby, L.G. Ungerleider, B. Horwitz, J.M. Maisog, S.I. Rapoport, C.L. Grady, Face encoding and recognition in the human brain, Proc. Natl. Acad. Sei. USA 93 (1996) 922-927.
41. J.V. Haxby, C.L. Grady, B. Horwitz, L. Ungerieider, M. Mishkin, R.E. Carson, P. Herscovitch, M. Schapiro, S. Rapoport, Dissociation of object and spatial virtual processing pathways in human extrastriate cortex, Proc. Natl. Acad. Sci. USA 88 (1991) 1621-1625.
42. K.M. Heilman, D. Bowers, E. Valenstein, R.T. Watson, Hemispace and hemispatial neglect, in: J. M (Ed.), Neurophysiological and Neuropsychological Aspects of Spatial Neglect, Elsevier Science, Amsterdam, 1987, pp. 115-150.
43. W. Hening, M. Favilla, C. Ghez, Trajectory control in targeted force impulses. V Gradual specification of response amplitude, Exp. Brain Res. 71 (1988) 116-128.
44. O. Hikosaka, K. Miyashita, S. Miyachi, K. Sakai, X. Lu, Differential roles of the frontal cortex, basal ganglia and cerebellum in visuomotor sequence learning, Neurobiol. Learning and Memory 70 (1998) 137-149.
45. J. Hodgkins, Influence of age on the speed of reaction and movements in female, J. Gerontol. 17 (1962) 385-389.
46. J. Hyvarinen, Posterior parietal lobe of the primate brain, Physiol. Rev. 62 (1982) 1060-1129.
47. K. Inoue, R. Kawashima, K. Satoh, S. Kinomura, R. Goto, M. Koyama, M. Sugiura, M. Ito, H. Fukuda, PET study of pointing with visual feedback of moving hand, J. Neurophysiol. 79 (1998) 117-125.
48. S. Jacobson, J.Q. Trojanowski, The cells of origin of the corpus callosum in rat, cat and rhesus monkey, Brain Res. 80 (1974) 395-411.
49. I.H. Jenkins, D.J. Brooks, P.D. Nixon, R.S.J. Frackowiak, R.E. Passingham, Motor sequence learning: a study with positron emission tomography, J. Neurosci. 16 (1994) 3775-3790.
50. J. Jonides, S. EE, R. Koeppe, E. Awh, S. Minoshima, M. Mintun, Spatial working memory in human as revealed by PET, Nature 363 (1993) 623-625.
51. M. Jueptner, K. Stephan, C. Frith, D. Brooks, R. Frackowiak, R. Passingham, The anatomy of motor learning. I. Frontal cortex and attention to action, J. Neurophysiol. 77 (1997) 1313-1324.
52. M. Jueptner, K. Stephan, C. Frith, D. Brooks, R. Frackowiak, R. Passingham, The anatomy of motor learning. II. Subcortical structures and learning by trial and error, J. Neurophysiol. 3 (1997) 1325-1337.
53. R. Kawashima, P.E. Roland, B.T. O'Sullivan, Fields in human motor areas involved in preparation for reaching, actual reaching, and visuomotor learning: a positron emission tomography study, J. Neurosci. 14 (1994) 3462-3474.
54. W.M. Kelley, F.M. Miezin, M.E. Raichle, N.J. Cohen, J.M. Ollinger, E. Akbudak, T.E. Conturo, A.Z. Snyder, S.E. Petersen, Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and non verbal memory encoding, Neuron 20 (1998) 927-936.
55. S.-G. Kim, K. Ugurbil, P.L. Strick, Activation of a cerebellar output nucleus during cognitive processing, Science 265 (1994) 949-951.
56. T. Klingberg, R. Kawashima, P.E. Roland, Activation of multimodal cortical areas underlies short-memory, Eur. J. Neurosci. 8 (1996) 1965-2019.
57. G.D. Logan, Attention in character classification: evidence for the automaticity of component stages, J. Exp. Psychol.: General 107 (1978) 32-63.
58. G.D. Logan, Attention and automaticity in Stroop and Priming tasks: theory and data, Cognitive Psychology 12 (1980) 523-553.
59. G.D. Logan, Toward an instance theory of automatization, Psychol. Rev. 95 (1988) 492-527.
60. A.R. McIntosh, C.L. Grady, L.G. Ungerleider, J.V. Haxby, S.I. Rapoport, B. Horwitz, Network analysis of cortical visual pathways mapped with PET, J. Neurosci. 14 (1994) 655-666.
61. A.R. McIntosh, M.N. Rajah, N.J. Lobaugh, Interactions of prefrontal cortex in relation to awareness in sensory learning, Science 284 (1999) 1531-1533.
62. D.E. Meyer, S. Kornblum, R.A. Abrams, C.E. Wright, J.E.K. Smith, Optimality in human motor performance: ideal control of rapid aimed movements, Psychol. Rev. 95 (1988) 340-370.
63. D.E. Meyer, J.E.K. Smith, S. Kornblum, R.A. Abrams, C.E. Wright, Speed-accuracy tradeoffs in aimed movements: Toward a theory of rapid voluntary action, in: M. Jeannerod (Ed.), Attention and Performance XIII: Motor Representation and Control, Lawrence Erlbaum, Hillsdale, NJ, 1990, pp. 173-226.
64. D.E. Meyer, J.E.K. Smith, C.E. Wright, Models for the speed and accuracy of aimed movements, Psychol. Rev. 89 (1982) 449-482.
65. F.A. Middleton, PL. Strick, Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function, Science 266 (1994) 458-461.
66. B. Milner, Interhemispheric differences in the localization of psychological processes in man, Br. Med. Bull. 27 (1971) 272-277.
67. M. Nissen, P. Bullemer, Attentional requirements of learning: Evidence from performance measures, Cognitive Psychology 19 (1987) 1-32.
68. C.E. Noble, Age, race and sex in the learning and performance of psychomotor skills, in: R.T. Osborne, C.E. Noble, N. Weyl (Eds.), Human Variation: the Biopsychology of Age, Race and Sex, Academic Press, New York, 1978.
69. D.N. Pandya, D. Gold, T. Berger, Interhemispheric connections in the precentral motor cortex in the rhesus monkey, Brain Res. 15 (1969) 594-596.
70. C.L. Pappas, PL. Strick, Anatomical demonstration of multiple representation of the forelimb region of the cat motor cortex, J. Comparative Neurol. 200 (1981) 491-500.
71. S.E. Petersen, P.T. Fox, M.I. Posner, M. Mintun, M.E. Raichle, Positron emission tomographic studies of the cortical anatomy of single-word processing, Nature 331 (1988) 585-589.
72. M. Petrides, B. Alivisatos, E. Meyer, A.C. Evans, Functional activation of the human frontal cortex during the performance of verbal working memory tasks, Proc. Natl. Acad. Sci. USA 90 (1993) 878-882.
73. Z.M. Pine, J. Krakauer, J. Gordon, C. Ghez, Learning of scaling factors and reference axes for reaching movements, NeuroReport 7 (1996) 2357-2361.
74. M.I. Posner, C.R.R. Snyder, Attention and cognitive control, in: S.R. L (Ed.), Information Processing and Cognition: the Loyola Symposium, Erlbaum, Hillsdale, NJ, 1975, pp. 55-85.
75. M.I. Posner, S.E. Petersen, The attention system of the human brain, Ann. Rev. Neurosci. 13 (1990) 25-42.
76. M.E. Raichle, J.A. Fiez, T.O. Videen, A.-M.K. Macleod, J.V. Pardo, P.T. Fox, S.E. Pertersen, Practice related changes in human brain functional anatomy during non motor learning, Cerebral Cortex 4 (1994) 8-26.
77. R.L. Sainburg, K. Faran, M. Rossi, M. Alberoni, M.F. Ghilardi, Learning of novel limb dynamics transfers to the contralateral arm, Soc. Neurosci. Abstr. 23 (1997) 203.
78. K. Sakai, O. Hikosaka, S. Miyauchi, R. Takino, Y. Sasaki, B. Putz, Transition of brain activation from frontal to parietal areas in visuomotor sequence learning, J. Neurosci. 18 (1998) 1827-1840.
79. W. Schneider, R.M. Shiffrin, Controlled and automatic human information processing. I. Detection, search and attention, Psychol. Rev. 84 (1977) 1-66.
80. W. Schultz, R. Romo, Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum, Exp. Brain Res. 91 (1992) 363-384.
81. R.J. Seitz, P.E. Roland, Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study, Eur. J. Neurosci. 4 (1992) 154-165.
82. R.J. Seitz, P.E. Roland, C. Bohm, T. Greitz, S. Stone-Elanders, Motor learning in man: a positron emission tomographic study, NeuroReport 1 (1990) 17-20, 57-60 ?.
83. T. Shallice, P. Fletcher, C.D. Frith, P.M. Grasby, R.S.J. Frackowiack, R.J. Dolan, Brain regions associated with acquisition and retrieval of verbal episodic memory, Nature 368 (1994) 633-635.
84. H. Shibasaki, N. Sadato, H. Lyshkow, Y. Yonekura, T. Nagamine, Y. Magata, A. Ikeda, M. Miyazaki, R. Asato, J. Konishi, Both primary motor cortex and supplementary motor area play an important role in complex finger movement, Brain 116 (1993) 1387-1398.
85. D. Silbersweig, E. Stern, C. Frith, C. Cahill, L. Schnorr, S. Grootoonk, T. Spinks, C. J, R. Frackowiak, T. Jones, Detection of thirty second cognitive activations in single subjects with positron emission tomography: A new low dose H2150 regional cerebral blood flow three dimensional imaging technique, J. Cereb. Blood Flow Metab. 13 (1993) 617-629.
86. L. Squire, Memory and the brain, Oxford University Press, New York, 1987.
87. J. Talairach, P. Tournoux, Co-planar Stereotaxic Atlas of the Human Brain, Thieme, New York, 1988.
88. A.E. Taylor, J.A. Saint-Cyr, A.E. Lang, Frontal lobe dysfunction in Parkinson's disease. The cortical focus of neostriatal outflow, Brain 109 (1986) 845-883.
89. E. Tulving, Memory: performance, knowledge, and experience, Eur. J. Cognitive Psychol. 1 (1989) 3-26.
90. E. Tulving, S. Kapur, F.I.M. Craik, H.J. Markowitch, S. Houle, Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings, Proc. Natl. Acad. Sci. USA 91 (1994) 2016-2020.