Non-invasive mapping of brain functions and brain recovery: Applying lessons from cognitive neuroscience to neurorehabilitation

Restorative Neurology and Neuroscience

Volumn 22, Issue 3-4, 2004, Pages 245-260

  Matthews, P M ^a,c   Johansen Berg, H ^a   Reddy, H ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

FMRI; Learning; Motor control; Neurorehabilitation; Transcranial magnetic stimulation

Indexed keywords

ADAPTATION; BRAIN FUNCTION; BRAIN INJURY; BRAIN MAPPING; COGNITION; HEALTH CARE COST; LEARNING; MICROANGIOPATHY; MOTOR CONTROL; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROREHABILITATION; NEUROSCIENCE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREMOTOR CORTEX; PRIORITY JOURNAL; REVIEW; STROKE; TRANSCRANIAL MAGNETIC STIMULATION;

BRAIN MAPPING; CEREBRAL CORTEX; COGNITION; HUMANS; NEURONAL PLASTICITY; NEUROSCIENCES; RECOVERY OF FUNCTION;

EID: 7944229225     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (129)

1. G. Alagona, V. Delvaux, P. Gerard, V. De, Pasqua, G. Pennisi, P.J. Delwaide, F. Nicoletti and Maertens, de Noordhout. Ipsilateral motor responses to focal transcranial magnetic stimulation in healthy subjects and acute-stroke patients, Stroke 32 (2001), 1304-1309.
2. D.L. Arnold, J.S. Wolinsky, P.M. Matthews and A. Falini, The use of magnetic resonance spectroscopy in the evaluation of the natural history of multiple sclerosis, J Neurol Neurosurg Psychiatry 64 (Suppl 1) (1998), S94-101.
3. D. Attwell and C. Iadecola, The neural basis of functional brain imaging signals, Trends Neurosci 25 (2002), 621-625.
4. M. Blinkenberg, C.V. Jensen, S. Holm, O.B. Paulson and P.S. Sorensen, A longitudinal study of cerebral glucose metabolism, MRI, and disability in patients with MS, Neurology 53 (1999), 149-153.
5. S. Boniface and U. Ziemann, Plasticity in the human nervous system: investigations with transcranial magnetic stimulation, 2003.
6. C.M. Butefisch, B.C. Davis, S.P. Wise, L. Sawaki, L. Kopylev, J. Classen and L.G. Cohen, Mechanisms of use-dependent plasticity in the human motor cortex. Proc. Natl. Acad. Sci. USA 97 (2000), 3661-3665.
7. F. Chollet, V. DiPiero, R.J. Wise, D.J. Brooks, R.J. Dolan and R.S. Frackowiak, The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography, Ann Neurol 29 (1991) 63-71.
8. A. Cifelli, M. Arridge, P. Jezzard, M.M. Esiri, J. Palace and P.M. Matthews, Thalamic neurodegeneration in multiple sclerosis, Ann Neurol 52 (2002), 650-653.
9. A. Cifelli and P.M. Matthews, Cerebral plasticity in multiple sclerosis: insights from fMRI, Mult. Scler. 8 (2002), 193-199.
10. M.C. Cirstea and M.F. Levin, Compensatory strategies for reaching in stroke, Brain 123(Pt 5) (2000), 940-953.
11. J. Cole and P. Glees, Ipsilateral impairment following area 4 lesions in monkeys, J Physiol 117 (1952), 54P.
12. M.C. Comelli, D. Guidolin, M.S. Seren, R. Zanoni, R. Canella, R. Rubini and H. Manev, Time course, localization and pharmacological modulation of immediate early inducible genes, brain-derived neurotrophic factor and trkB messenger RNAs in the rat brain following photochemical stroke, Neuroscience 55 (1993), 473-490.
13. S.C. Cramer, G. Nelles, R.R. Benson, J.D. Kaplan, R.A. Parker, K.K. Kwong, D.N. Kennedy, S.P. Finklestein and B.R. Rosen, A functional MRI study of subjects recovered from hemiparetic stroke, Stroke 28 (1997), 2518-2527.
14. B.L. Day, J.C. Rothwell, P.D. Thompson, Maertens, de Noordhout, K. Nakashima, K. Shannon and C.D. Marsden, Delay in the execution of voluntary movement by electrical or magnetic brain stimulation in intact man. Evidence for the storage of motor programs in the brain, Brain 112(Pt 3) (1989), 649-663.
15. N. De Stefano, P.M. Matthews and D.L. Arnold, Reversible decreases in N-acetylaspartate after acute brain injury, Magn Reson Med 34 (1995), 721-727.
16. P. De Weerd, K. Reinke, L. Ryan, T. McIsaac, P. Perschler, D. Schnyer, T. Trouard and A. Gmitro, Cortical mechanisms for acquisition and performance of bimanual motor sequences, Neuroimage 19(2003), 1405-1416.
17. J.P. Donoghue, S. Suner and J.N. Sanes, Dynamic organization of primary motor cortex output to target muscles in adult rats. II. Rapid reorganization following motor nerve lesions, Exp. Brain Res. 79 (1990), 492-503.
18. J. Doyon, A.W. Song, A. Karni, F. Lalonde, M.M. Adams, and L.G. Ungerleider, Experience-dependent changes in cerebellar contributions to motor sequence learning, Proc. Natl. Acad. Sci. USA 99 (22-1-2002), 1017-1022.
19. J. Driver and J.B. Mattingley, Parietal neglect and visual awareness, Nat. Neurosci. 1 (1998), 17-22.
20. R.P. Dum and P.L. Strick, Motor areas in the frontal lobe of the primate, Physiol Behav 77 (2002), 677-682.
21. J. Duncan, R.J. Seitz, J. Kolodny, D. Bor, H. Herzog, A. Ahmed, F.N. Newell and H. Emslie, A neural basis for general intelligence, Science 289 (2000), 457-460.
22. N. Evangelou, M.M. Esiri, S. Smith, J. Palace and P.M. Matthews, Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis, Ann Neurol 47 (2000), 391-395.
23. A. Feydy, R. Carlier, A. Roby-Brami, B. Bussel, F. Cazalis, L. Pierot, Y. Burnod and M.A. Maier, Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation, Stroke 33 (2002), 1610-1617.
24. M. Filippi, M. Bozzali, M. Rovaris, O. Gonen, C. Kesavadas, A. Ghezzi, V. Martinelli, R.I. Grossman, G. Scotti, G. Comi and A. Falini, Evidence for widespread axonal damage at the earliest clinical stage of multiple sclerosis, Brain 126 (2003), 433-437.
25. M. Filippi, M.A. Rocca, B. Colombo, A. Falini, M. Codella, G. Scotti and G. Comi, Functional magnetic resonance imaging correlates of fatigue in multiple sclerosis, Neuroimage 15 (2002), 559-567.
26. G.R. Fink, P.W. Halligan, J.C. Marshall, C.D. Frith, R.S. Frackowiak and R.J. Dolan, Where in the brain does visual attention select the forest and the trees? Nature 382 (1996), 626-628.
27. S.L. Florence, H.B. Taub and J.H. Kaas, Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys, Science 282 (1998), 1117-1121.
28. A. Floyer-Lea and P.M. Matthews, Transition of activity from prefrontal cortex to pre-SMA during early motor learning, Neuroimage 19(Part 2) (2003), 156.
29. K.M. Friel and R.J. Nudo, Recovery of motor function after focal cortical injury in primates: compensatory movement patterns used during rehabilitative training, Somatosens. Mot. Res. 15 (1998), 173-189.
30. K.J. Friston, L. Harrison and W. Penny, Dynamic causal modelling, Neuroimage 19 (2003), 1273-1302.
31. S.B. Frost, S. Barbay, K.M. Friel, E.J. Plautz and R.J. Nudo, Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery, J Neurophysiol 89 (2003), 3205-3214.
32. L. Fu, P.M. Matthews, N. De Stefano, K.J. Worsley, S. Narayanan, G.S. Francis, J.P. Antel, C. Wolfson and D.L. Arnold, Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 121 (1998), 103-113.
33. P.E. Garraghty and J.H. Kaas, Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury, Proc. Natl. Acad. Sci. USA 88 (1991), 6976-6980.
34. S.T. Grafton, J.C. Mazziotta, S. Presty, K.J. Friston, R.S. Frackowiak and M.E. Phelps, Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET, J Neurosci 12 (1992), 2542-2548.
35. C. Halfpenny, T. Benn and N. Scolding, Cell transplantation, myelin repair, and multiple sclerosis, Lancet Neurol 1 (2002), 31-40.
36. M. Hallett, Movement-related cortical potentials. Electromyogr, Clin. Neurophysiol. 34 (1994), 5-13.
37. E. Hoshi and J. Tanji, Integration of target and body-part information in the premotor cortex when planning action, Nature 408 (2000), 466-470.
38. K.M. Jacobs and J.P. Donoghue, Reshaping the cortical motor map by unmasking latent intracortical connections, Science 251 (1991), 944-947.
39. M. Jahanshahi and J. Rothwell, Transcranial magnetic stimulation studies of cognition: an emerging field, Exp Brain Res 131 (2000), 1-9.
40. S.H. Jang, Y.H. Kim, S.H. Cho, J.H. Lee, J.W. Park and Y.H. Kwon, Cortical reorganization induced by task-oriented training in chronic hemiplegic stroke patients, Neuroreport 14(1) (2003), 137-141.
41. W.M. Jenkins, M.M. Merzenich, M.T. Ochs, T. Allard and E. Guic-Robles, Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation, J Neurophysiol 63 (1990), 82-104.
42. P. Jezzard, P.M. Matthews and S.M. Smith, Functional MRI: an introduction to methods 2001.
43. H. Johansen-Berg, H. Dawes, C. Guy, S.M. Smith, D.T. Wade and P.M. Matthews, Correlation between motor improvements and altered fMRI activity after rehabilitative therapy, Brain 125(Pt. 12) (Dec. 2002), 2731-2742.
44. H. Johansen-Berg, M.F. Rushworth, M.D. Bogdanovic, U. Kischka, S. Wimalaratna and P.M. Matthews, The role of ipsilateral premotor cortex in hand movement after stroke, Proc. Natl. Acad. Sci. USA 99 (2002), 14518-14523.
45. S.H. Johnson-Frey, F.R. Maloof, R. Newman-Norlund, C. Fairer, S. Inati and S.T. Grafton, Actions or hand-object interactions? Human inferior frontal cortex and action observation, Neuron 39 (2003), 1053-1058.
46. M. Jueptner and C. Weiller, A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies, Brain 121(Pt 8) (1998), 1437-1449.
47. A. Karni, G. Meyer, P. Jezzard, M.M. Adams, R. Turner and L.G. Ungerleider, Functional MRI evidence for adult motor cortex plasticity during motor skill learning, Nature 377 (1995), 155-158.
48. T. Kawamata, W.D. Dietrich, T. Schallert, J.E. Gotts, R.R. Cocke, L.I. Benowitz and S.P. Finklestein, Intracisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction, Proc. Natl. Acad. Sci. USA 94 (1997), 8179-8184.
49. S.G. Kim, J. Ashe, K. Hendrich, J.M. Ellermann, H. Merkle, K. Ugurbil and A.P. Georgopoulos, Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness, Science 261 (1993), 615-617.
50. J.A. Kleim, S. Barbay and R.J. Nudo, Functional reorganization of the rat motor cortex following motor skill learning, J Neurophysiol 80 (1998), 3321-3325.
51. H.G. Kuypers and J. Brinkman, Precentral projections to different parts of the spinal intermediate zone in therhesus monkey, Brain Res 24 (1970), 29-48.
52. R. Laforce Jr. and J. Doyon, Distinct contribution of the striatum and cerebellum to motor learning, Brain Cogn 45 (2001), 189-211.
53. L. Lee, H.R. Siebner, J.B. Rowe, V. Rizzo, J.C. Rothwell, R.S. Frackowiak and K.J. Friston, Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation, J Neurosci 23 (2003), 5308-5318.
54. M. Lee, H. Reddy, H. Johansen-Berg, S. Pendlebury, M. Jenkinson, S. Smith, J. Palace and P.M. Matthews, The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis, Ann Neurol 47 (2000), 606-613.
55. M. Lee, H. Reddy, H. Johansen-Berg, S. Pendlebury, M. Jenkinson, S. Smith, J. Palace and P.M. Matthews, The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis, Ann Neurol 47 (2000), 606-613.
56. L.M. Levy, U. Ziemann, R. Chen and L.G. Cohen, Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation, Ann Neurol 52 (2002), 755-761.
57. J. Liepert, W.H. Miltner, H. Bauder, M. Sommer, C. Dettmers, E. Taub and C. Weiller, Motor cortex plasticity during constraint-induced movement therapy in stroke patients, Neurosci. Lett. 250 (1998), 5-8.
58. Y. Liu and E.M. Rouiller, Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys, Exp. Brain Res. 128 (1999), 149-159.
59. N.K. Logothetis, J. Pauls, M. Augath, T. Trinath and A. Oeltermann, Neurophysiological investigation of the basis of the fMRI signal, Nature 412 (2001), 150-157.
60. M. Lotze, C. Braun, N. Birbaumer, S. Anders and L.G. Cohen, Motor learning elicited by voluntary drive, Brain 126 (2003), 866-872.
61. I. Loubinoux, J. Pariente, O. Rascol, P. Celsis and F. Chollet, Selective serotonin reuptake inhibitor paroxetine modulates motor behavior through practice. A double-blind, placebo-controlled, multi-dose study in healthy subjects, Neuropsychologia 40 (2002), 1815-1821.
62. F. Malouin, C.L. Richards, P.L. Jackson, F. Dumas and J. Doyon, Brain activations during motor imagery of locomotor-related tasks: a PET study, Hum. Brain Mapp 19 (2003), 47-62.
63. R.S. Marshall, G.M.Perera, R.M. Lazar, J.W. Krakauer, R.C. Constantine and R.L. DeLaPaz, Evolution of cortical activation during recovery from corticospinal tract infarction, Stroke 31 (2000), 656-661.
64. R.E. Martin, B.G. Goodyear, J.S. Gati and R.S. Menon, Cerebral cortical representation of automatic and volitional swallowing in humans, J Neurophysiol 85 (2001), 938-950.
65. A.M. Martino and P.L. Strick, Corticospinal projections originate from the arcuate premotor area, Brain Res 404 (1987), 307-312.
66. P.M. Matthews and P. Jezzard, Functional magnetic resonance imaging, J Neurol Neurosurg. Psychiatry, In press, 2003.
67. M.M. Merzenich, J.H. Kaas, J. Wall, R.J. Nelson, M. Sur and D. Felleman, Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation, Neuroscience 8 (1983), 33-55.
68. R.C. Miall, G.Z. Reckess and H. Imamizu, The cerebellum coordinates eye and hand tracking movements, Nat. Neurosci 4 (2001), 638-4544.
69. J.R. Moffett, M.A. Namboodiri, C.B. Cangro and J.H. Neale, Immunohistochemical localization of N-acetylaspartate in rat brain, Neuroreport 2 (1991), 131-134.
70. D.J. Mort, P. Malhotra, S.K. Mannan, C. Rorden, A. Pambakian, C. Kennard and M. Husain, The anatomy of visual neglect, Brain 126 (2003), 1986-1997.
71. T. Neumann-Haefelin and O.W. Witte, Periinfarct and remote excitability changes after transient middle cerebral artery occlusion, J Cereb. Blood Flow Metab 20 (2000), 45-52.
72. R.J. Nudo, W.M. Jenkins and M.M. Merzenich, Repetitive microstimulation alters the cortical representation of movements in adult rats, Somatosens. Mot. Res. 7 (1990), 463-483.
73. R.J. Nudo, G.W. Milliken, W.M. Jenkins and M.M. Merzenich, Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys, J Neurosci 16 (1996), 785-807.
74. R.J. Nudo, E.J. Plautz, and S.B. Frost, Role of adaptive plasticity in recovery of function after damage to motor cortex, Muscle Nerve 24 (2001), 1000-1019.
75. R.J. Nudo, B.M. Wise, F. SiFuentes and G.W. Milliken, Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct, Science 272 (1996), 1791-1794.
76. S. Ogawa, T.M. Lee, A.S. Nayak and P. Glynn, Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields, Magn Reson Med 14 (1990), 68-78.
77. S. Ogawa, R.S. Menon, D.W. Tank, S.G. Kim, H. Merkle, J.M. Ellermann and K. Ugurbil, Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model, Biophys. J. 64 (1993), 803-812.
78. S. Ogawa, D.W. Tank, R. Menon, J.M. Ellermann, S.G. Kim, H. Merkle and K. Ugurbil, Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging, Proc. Natl. Acad. Sci. USA 89 (1992), 5951-5955.
79. P. Pantano, G.D. Iannetti, F. Caramia, C. Mainero, S. Di Legge, L. Bozzao, C. Pozzilli and G.L. Lenzi, Cortical motor reorganization after a single clinical attack of multiple sclerosis, Brain 125 (2002), 1607-1615.
80. I. Papathanassiou, S.R. Filipovic, R. Whurr and M. Jahanshahi, Plasticity of motor cortex excitability induced by rehabilitation therapy for writing, Neurology 61 (2003), 977-980.
81. J. Pariente, I. Loubinoux, C. Carel, J.F. Albucher, A. Leger, C. Manelfe, O. Rascol and F. Chollet, Fluoxetine modulates motor performance and cerebral activation of patients recovering from stroke, Ann Neurol 50 (2001), 718-729.
82. A.M. Parry, R.B. Scott, J. Palace, S. Smith and P.M. Matthews, Potentially adaptive functional changes in cognitive processing for patients with multiple sclerosis and their acute modulation by rivastigmine, Brain 126 (2003), 1-11.
83. A.J. Pearce, G.W. Thickbroom, M.L. Byrnes and F.L. Mastaglia, Functional reorganisation of the corticomotor projection to the hand in skilled racquet players, Exp. Brain Res. 130 (2000), 238-243.
84. I.K. Penner, M. Rausch, L. Kappos, K. Opwis and E.W Radu, Analysis of impairment related functional architecture in MS patients during performance of different attention tasks, J Neurol 250 (2003), 461-472.
85. J.W. Peterson, L. Bo, S. Mork, A. Chang and B.D. Trapp, Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions, Ann Neurol 50 (2001), 389-400.
86. C. Pittenger and K.R. Kandel, In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus, Philos. Trans. R. Soc. Lond B Biol. Sci. 358 (2003), 757-763.
87. E.J. Plautz, G.W. Milliken and R.J. Nudo, Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning, Neurobiol. Learn. Mem. 74 (2000), 27-55.
88. N. Ramnani, T.E.J. Behrens, H. Johansen-Berg, O. Ciccarelli, M. Woolrich, S.M. Smith, C.A.M. Wheeler-Kingshott, P.A. Boulby, G.J. Barker, A.J. Thompson and P.M. Matthews, Mapping corticocerebellar projections in the human brain: an 'in -vivo' diffusion imaging study, AbstractViewer/Itinerary Planner 2003; Washington, DC: Society for Neuroscience: 882.8
89. S.M. Rao, J.R. Binder, P.A. Bandettini, T.A. Hammeke, F.Z. Yetkin, A. Jesmanowicz, L.M. Lisk, G.L. Morris, W.M. Mueller and L.D. Estkowski, Functional magnetic resonance imaging of complex human movements, Neurology 43 (1993), 2311-2318.
90. H. Reddy, D. Bendahan, M.A. Lee, H. Johansen-Berg, M. Donaghy, D. Hilton-Jones and P.M. Matthews, An expanded cortical representation for hand movement after peripheral motordenervation, J Neurol Neurosurg Psychiatry 72 (2002), 203-210.
91. H. Reddy, N. De Stefano, M. Mortilla, A. Federico and P.M. Matthews, Functional reorganization of motor cortex increases with greater axonal injury from CADASIL, Stroke 33 (2002), 502-508.
92. H. Reddy, A. Floyer, M. Donaghy and P.M. Matthews, Altered cortical activation with finger movement after peripheral denervation: comparison of active and passive tasks, Exp. Brain Res. 138 (2001), 484-491.
93. H. Reddy, S. Narayanan, B. Arnoutelis, M. Jenkinson, J. Antel, P.M. Matthews and D.L. Arnold, Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis, Brain 123(Pt 11) (2000), 2314-2320.
94. H. Reddy, S. Narayanan, R. Arnoutelis, M. Jenkinson, J. Antel, P.M. Matthews and D.L. Arnold, Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis, Brain 123 (2000), 2314-2320.
95. H. Reddy, S. Narayanan, P.M. Matthews, R.D. Hoge, G.B. Pike, P. Duquette, J. Antel and D.L. Arnold, Relating axonal injury to functional recovery in MS, Neurology 54 (2000), 236-239.
96. H. Reddy, S. Narayanan, M. Woolrich, T. Mitsumori, Y. Lapierre, D.L. Arnold and P.M. Matthews, Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability, Brain 125 (2002), 2646-2657.
97. H. Reddy, S. Narayanan, M. Woolrich, T. Mitsumori, Y. Lapierre, D.L. Arnold and P.M. Matthews, Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability, Brain 125 (2002), 2646-2657.
98. C. Redecker, W. Wang, J.M. Fritschy and O.W. Witte, Widespread and long-lasting alterations in GABA(A)-receptor subtypes after focal cortical infarcts in rats: mediation by NMDA-dependent processes, J Cereb. Blood Flow Metab 22 (2002), 1463-1475.
99. M.A. Rocca, P.M. Matthews, D. Caputo, A. Ghezzi, A. Falini, G. Scotti, G. Comi and M. Filippi, Evidence for widespread movement-associated functional MRI changes in patients with PPMS, Neurology 58 (2002), 866-872.
100. M.A. Rocca, D.M. Mezzapesa, A. Falini, A. Ghezzi, V. Martinelli, G. Scotti, G. Comi and M. Filippi, Evidence for axonal pathology and adaptive cortical reorganization in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis, Neuroimage 18 (2003), 847-855.
101. M.A. Rocca, D.M. Mezzapesa, A. Falini, A. Ghezzi, V. Martinelli, G. Scotti, G. Comi and M. Filippi, Evidence for axonal pathology and adaptive cortical reorganization in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis, Neuroimage 18 (2003), 847-855.
102. P.E. Roland and K. Zilles, Functions and structures of the motor cortices in humans, Curr. Opin. Neurobiol. 6 (1996), 773-781.
103. M. Rovaris, G. Comi, D. Ladkani, J.S. Wolinsky and M. Filippi, Short-term correlations between clinical and MR imaging findings in relapsing-remitting multiple sclerosis, AJNR Am. J Neuroradiol 24 (2003), 75-81.
104. C. Sahyoun, A. Floyer, H. Johansen-Berg and P.M. Matthews, Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements, Neuroimage, in press, 2003.
105. W.R. Schabitz, S. Schwab, M. Spranger and W. Hacke, Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats, J Cereb. Blood Flow Metab 17 (1997), 500-506.
106. R.I. Schubotz and D.Y. von Cramon, A blueprint for target motion: fMRI reveals perceived sequential complexity to modulate premotor cortex, Neuroimage 16 (2002), 920-935.
107. F.J. Seil, Recovery and repair issues after stroke from the scientific perspective, Curr. Opin. Neurol 10 (1997), 49-51.
108. R.J. Seitz, Y. Huang, U. Knorr, L. Teilmann, H. Herzog, and H.J. Freund, Large-scale plasticity of the human motor cortex, Neuroreport 6 (1995), 742-744.
109. S.L. Small, P. Hlustik, D.C. Noll, C. Genovese and A. Solodkin, Cerebellar hemispheric activation ipsilateral to the paretic hand correlates with functional recovery after stroke, Brain 125 (2002), 1544-1557.
110. W. Staffen, A. Mair, H. Zauner, J. Unterrainer, H. Niederhofer, A. Kutzelnigg, S. Ritter, S. Golaszewski, B. Iglseder and G. Ladurner, Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task, Brain 125 (2002), 1275-1282.
111. X. Sun, M. Tanaka, S. Kondo, K. Okamoto and S. Hirai, Clinical significance of reduced cerebral metabolism in multiple sclerosis: a combined PET and MRI study, Ann Nucl. Med. 12 (1998), 89-94.
112. E. Taub, N.E. Miller, T.A. Novack, E.W. Cook, W.C. III, Fleming, C.S. Nepomuceno, J.S. Connell and J.E. Crago, Technique to improve chronic motor deficit after stroke, Arch. Phys. Med. Rehabil. 74 (1993), 347-354.
113. E. Taub, G. Uswatte and T. Elbert, New treatments in neurorehabilitation founded on basic research, Nat. Rev. Neurosci. 3 (2002), 228-236.
114. S. Tonegawa, K. Nakazawa and M.A. Wilson, Genetic neuroscience of mammalian learning and memory, Philos. Trans. R. Soc. Lond B Biol. Sci. 358 (2003), 787-795.
115. I. Toni, N. Ramnani, O. Josephs, J. Ashburner and R.E. Passingham, Learning arbitrary visuomotor associations: temporal dynamic of brain activity, Neuroimage 14 (2001), 1048-1057.
116. B.D. Trapp, J. Peterson, R.M. Ransohoff, R. Rudick, S. Mork and L. Bo, Axonal transection in the lesions of multiple sclerosis, N. Engl. J Med. 338 (1998), 278-285.
117. Y. Vandermeeren, E. Olivier, G. Sebire, G. Cosnard, A. Bol, M. Sibomana, C. Michel and A.G. De Voider, Increased FDG uptake in the ipsilesional sensorimotor cortex in congenital hemiplegia, Neuroimage 15 (2002), 949-960.
118. D.T. Wade, Measurement in neurologic rehabilitation, Curr. Opin. Neurol 6 (1993), 778-784.
119. V. Walsh and M.A. Rushworth, primer of magnetic stimulation as a tool for neuropsychology, Neuropsychologia 37 (1999), 125-135.
120. N.S. Ward, M.M. Brown, A.J. Thompson and R.S. Frackowiak, Neural correlates of outcome after stroke: a cross-sectional fMRI study, Brain 126 (2003), 1430-1448.
121. C. Weiller, F. Chollet, K.J. Fristen, R.J. Wise and R.S. Frackowiak, Functional reorganization of the brain in recovery from striatocapsular infarction in man, Ann Neurol 31 (1992), 463-472.
122. C. Weiller, M. Juptner, S. Fellows, M. Rijntjes, G. Leonhardt, S. Kiebel, S. Muller, H.C. Diener and A.F. Thilmann, Brain representation of active and passive movements, Neuroimage 4 (1996), 105-110.
123. K.J. Werhahn, A.B. Conforte, N. Kadom, M. Hallett and L.G. Cohen, Contribution of the ipsilateral motor cortex to recovery after chronic stroke, Ann Neurol 54 (2003), 464-472.
124. K.J. Werhahn, J. Mortensen, A. Kaelin-Lang, B. Boroojerdi and L.G. Cohen, Cortical excitability changes induced by deafferentation of the contralateral hemisphere, Brain 125 (2002), 1402-1413.
125. D.J. Werring, E.T. Bullmore, A.T. Toosy, D.H. Miller, G.J. Barker, D.G. MacManus, M.J. Brammer, V.P. Giampietro, A. Brusa, P.A. Brex, I.F. Moseley, G.T. Plant, W.I. McDonald and A.J. Thompson, Recovery from optic neuritis is associated with a change in the distribution of cerebral response to visual stimulation: a functional magnetic resonance imaging study, J Neurol Neurosurg. Psychiatry 68 (2000), 441-449.
126. O.W. Witte, Lesion-induced plasticity as a potential mechanism for recovery and rehabilitative training, Curr. Opin. Neurol 11 (1998), 655-662.
127. O.W. Witte, H.J. Bidmon, K. Schiene, C. Redecker, and G. Hagemann, Functional differentiation of multiple perilesional zones after focal cerebral ischemia, J Cereb. Blood Flow Metab 20 (2000), 1149-1165.
128. M. Wylezinska, A. Cifelli, P. Jezzard, J. Palace, M. Alecci and P.M. Matthews, Thalamic neurodegeneration in relapsing-remitting multiple sclerosis, Neurology 60 (2003), 1949-1954.
129. T.A. Yousry, I. Berry and M. Filippi, Functional magnetic resonance imaging in multiple sclerosis, J Neurol Neurosurg. Psychiatry 64(Suppl 1) (1998), S85-S87.