Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson's disease

Clinical Neurophysiology

Volumn 115, Issue 11, 2004, Pages 2530-2541

  Lefaucheur, Jean Pascal ^a,b   Drouot, Xavier ^a,b   Von Raison, Florian ^a   Ménard Lefaucheur, Isabelle ^a   Cesaro, Pierre ^a   Nguyen, Jean Paul ^a  

^a HENRI MONDOR HOSPITAL   (France)

^b FACULTÉ DE MÉDECINE   (France)

Author keywords

Cortical excitability; Intracortical facilitation; Intracortical inhibition; Motor evoked potentials; Silent period

Indexed keywords

LEVODOPA;

ADULT; AGED; ARTICLE; BRADYKINESIA; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; FACILITATION; FEMALE; HUMAN; MALE; MOTOR ACTIVITY; MOTOR CORTEX; MOTOR PERFORMANCE; NEUROMODULATION; NEUROPHYSIOLOGY; PARKINSON DISEASE; PRIORITY JOURNAL; TRANSCRANIAL MAGNETIC STIMULATION;

AGED; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; MOVEMENT; PARKINSON DISEASE; PHYSICAL STIMULATION; SEVERITY OF ILLNESS INDEX; TRANSCRANIAL MAGNETIC STIMULATION; TREATMENT OUTCOME;

EID: 4644236972     PISSN: 13882457     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clinph.2004.05.025     Document Type: Article

References (80)

1. Alexander G.E., Crutcher M.D., DeLong M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, prefrontal and limbic functions. Prog Brain Res. 85:1990;119-146
2. Boylan L.S., Pullman S.L., Lisanby S.H., Spicknall K.E., Sackeim H.A. Repetitive transcranial magnetic stimulation to SMA worsens complex movements in Parkinson's disease. Clin Neurophysiol. 112:2001;259-264
3. Buhmann C., Glauche V., Stürenburg H.J., Oechsner M., Weiller C., Büchel C. Pharmacologically modulated fMRI-cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain. 126:2003;451-461
4. Canavero S., Paolotti R., Bonicalzi V., Castellano G., Greco-Crasto S., Rizzo L., Davini O., Zenga F., Ragazzi P. Extradural motor cortex stimulation for advanced Parkinson disease. Report of two cases. J Neurosurg. 97:2002;1208-1211
5. Cantello R., Gianelli M., Bettucci D., Civardi C., De Angelis M.S., Mutani R. Parkinson's disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology. 41:1991;1449-1456
6. Cantello R., Tarletti R., Civardi C. Transcranial magnetic stimulation and Parkinson's disease. Brain Res Rev. 38:2002;309-327
7. Cassidy M., Mazzone P., Oliviero A., Insola A., Tonali P., Di Lazzaro V., Brown P. Movement-related changes in synchronization in the human basal ganglia. Brain. 125:2002;1235-1246
8. Ceballos-Baumann A.O., Boecker H., Bartenstein P., von Falkenhayn I., Riescher H., Conrad B., Moringlane J.R., Alesch F. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson's disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol. 56:1999;997-1003
9. Chen R., Tam A., Butefisch C., Corwell B., Ziemann U., Rothwell J.C., Cohen L.G. Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol. 80:1998;2870-2881
10. Chen R., Kumar S., Garg R.R., Lang A.E. Impairment of motor cortex activation and deactivation in Parkinson's disease. Clin Neurophysiol. 112:2001;600-607
11. Cunic D., Roshan L., Khan F.I., Lozano A.M., Lang A.E., Chen R. Effects of subthalamic nucleus stimulation on motor cortex excitability in Parkinson's disease. Neurology. 58:2002;1665-1672
12. Cunnington R., Iansek R., Thickbroom G.W., Laing B.A., Mastaglia F.L., Bradshaw J.L., Phillips J.G. Effects of magnetic stimulation over supplementary motor area on movement in Parkinson's disease. Brain. 119:1996;815-822
13. Dauper J., Peschel T., Schrader C., Kohlmetz C., Joppich G., Nager W., Dengler R., Rollnik J.D. Effects of subthalamic nucleus (STN) stimulation on motor cortex excitability. Neurology. 59:2002;700-706
14. Defer G.L., Widner H., Marie R.M., Remy P., Levivier M. Core assessment program for surgical interventional therapies in Parkinson's disease (CAPSIT-PD). Mov Disord. 14:1999;572-584
15. Devanne H., Lavoie B., Capaday C. Input-output properties and gain changes in human corticospinal pathway. Exp Brain Res. 114:1997;329-338
16. Devos D., Labyt E., Derambure P., Bourriez J.L., Cassim F., Reyns N., Blond S., Guieu J.D., Destée A., Defebvre L. Subthalamic nucleus stimulation modulates motor cortex oscillatory activity in Parkinson's disease. Brain. 127:2004;408-419
17. Drouot X., Oshino S., Lefaucheur J.P., Besret L., Conde F., Keravel Y., Peschanski M., Hantraye P., Palfi S. Electrical neuromodulation of motor cortex facilitates locomotor activity in a primate model of Parkinson's disease. Proceedings of the Annual Meeting of the Society for Neuroscience, November 2002, Orlando. 2002
18. Feigin A., Fukuda M., Dhawan V., Przedborski S., Jackson-Lewis V., Mentis M.J., Moeller J.R., Eidelberg D. Metabolic correlates of levodopa response in Parkinson's disease. Neurology. 57:2001;2083-2088
19. Fitzgerald P.B., Brown T.L., Daskalakis Z.J., Chen R., Kulkarni J. Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol. 113:2002;1136-1141
20. Fox P., Ingham R., George M.S., Mayberg H., Ingham J., Roby J., Martin C., Jerabek P. Imaging human intra-cerebral connectivity by PET during TMS. NeuroReport. 8:1997;2787-2791
21. Gangitano M., Valero-Cabré A., Tormos J.M., Mottaghy F.M., Romero J.R., Pascual-Leone A. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol. 113:2002;1249-1257
22. George M.S., Nahas Z., Molloy M., Speer A.M., Oliver N.C., Li X.B., Arana G.W., Risch S.C., Ballenger J.C. A controlled trial of daily left prefrontal cortex TMS for treating depression. Biol Psychiatry. 48:2000;962-970
23. Ghabra M.B., Hallett M., Wassermann E.M. Simultaneous repetitive transcranial magnetic stimulation does not speed fine movement in PD. Neurology. 52:1999;768-770
24. Gibbs W.R., Lees A.J. The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J Neurol Neurosurg Psychiatry. 51:1988;745-752
25. Gilio F, Curra A, Inghilleri M, Lorenzano C, Manfredi M, Berardelli A. Repetitive magnetic stimulation of cortical motor areas in Parkinson's disease: implications for the pathophysiology of cortical function. Mov Disord 2002;17:467-73.
26. Gorsler A., Baumer T., Weiller C., Munchau A., Liepert J. Interhemispheric effects of high and low frequency rTMS in healthy humans. Clin Neurophysiol. 114:2003;1800-1807
27. Hanajima R., Ugawa Y., Terao Y., Ogata K., Kanazawa I. Ipsilateral cortico-cortical inhibition of the motor cortex in various neurological disorders. J Neurol Sci. 140:1996;109-116
28. Haslinger B., Erhard P., Kämpfe N., Boecker H., Rummeny E., Schwaiger M., Conrad B., Ceballos-Baumann A.O. Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain. 124:2001;558-570
29. Haug B.A., Schonle P.W., Knobloch C., Kohne M. Silent period measurement revives as a valuable diagnostic tool with transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 85:1992;158-160
30. Ikeguchi M., Touge T., Nishiyama Y., Takeuchi H., Kuriyama S., Ohkawa M. Effects of successive repetitive transcranial magnetic stimulation on motor performances and brain perfusion in idiopathic Parkinson's disease. J Neurol Sci. 209:2003;41-46
31. Ilic T.V., Meintzschel F., Cleff U., Ruge D., Kessler K.R., Ziemann U. Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol (Lond). 545:2002;153-167
32. Kaneko K., Kawaii S., Fuchigami Y., Morita H., Ofuji A. The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. Electroencephalogr Clin Neurophysiol. 101:1996;478-482
33. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., Wroe S., Asselman P., Marsden C.D. Corticocortical inhibition in human motor cortex. J Physiol (Lond). 471:1993;501-519
34. Kumar R., Lozano A.M., Sime E., Halket E., Lang A.E. Comparative effects of unilateral and bilateral subthalamic nucleus deep brain stimulation. Neurology. 53:1999;561-566
35. Lee L., Siebner H.R., Rowe J.B., Rizzo V., Rothwell J.C., Frackowiak R.S.J., Friston K.J. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci. 23:2003;5308-5318
36. Lefaucheur J.P., Drouot X., Nguyen J.P. Interventional neurophysiology for pain control: duration of pain relief following repetitive transcranial magnetic stimulation of the motor cortex. Neurophysiol Clin. 31:2001;247-252
37. Limousin P., Pollak P., Benazzouz A., Hoffmann D., Le Bas J.F., Broussolle E., Perret J.E., Benabid A.L. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet. 345:1995;91-95
38. Limousin P., Greene J., Pollak P., Rothwell J., Benabid A.L., Frackowiak R. Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol. 42:1997;283-291
39. Limousin P., Krack P., Pollak P., Benazzouz A., Ardouin C., Hoffmann D., Benabid A.L. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med. 339:1998;1105-1111
40. Loo C.K., Taylor J.L., Gandevia S.C., McDarmont B.N., Mitchell P.B., Sachdev P.S. Transcranial magnetic stimulation (TMS) in controlled treatment studies: are some 'sham' forms active? Biol Psychiatry. 47:2000;325-331
41. Lozano A.M., Lang A.E., Galvez-Jimenez N., Miyasaki J., Duff J., Hutchinson W.D., Dostrovsky J.O. Effect of GPi pallidotomy on motor function in Parkinson's disease. Lancet. 346:1995;1383-1387
42. Maeda F., Keenan J.P., Tormos J.M., Topka H., Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol. 111:2000;800-805
43. Mally J., Stone T.W. Therapeutic and 'dose-dependent' effect of repetitive microelectroshock induced by transcranial magnetic stimulation in Parkinson's disease. J Neurosci Res. 57:1999;935-940
44. Mally J., Stone T.W. Improvement in Parkinsonian symptoms after repetitive transcranial magnetic stimulation. J Neurol Sci. 162:1999;179-184
45. Manfredi L., Garavaglia P., Beretta S., Pellegrini G. Increased cortical inhibition induced by apomorphine in patients with Parkinson's disease. Neurophysiol Clin. 28:1998;31-38
46. Marchese R., Trompetto C., Buccolieri A., Abbruzzese G. Abnormalities of motor cortical excitability are not correlated with clinical features in atypical parkinsonism. Mov Disord. 15:2000;1210-1214
47. Nakashima K., Wang Y., Shimoda M., Sakuma K., Takahashi K. Shortened silent period produced by magnetic cortical stimulation in patients with Parkinson's disease. J Neurol Sci. 130:1995;209-214
48. Ogawa A., Ukai S., Shinosaki K., Yamamoto M., Kawaguchi S., Ishii R., Takeda M. Slow repetitive transcranial magnetic stimulation increases somatosensory high-frequency oscillations in humans. Neurosci Lett. 358:2004;193-196
49. Okabe S., Ugawa Y., Kanazawa I. 0.2-Hz repetitive transcranial magnetic stimulation has no add-on effects as compared to a realistic sham stimulation in Parkinson's disease. Mov Disord. 18:2003;382-388
50. Pascual-Leone A., Valls-Sole J., Brasil-Neto J.P., Cammarota A., Grafman J., Hallett M. Akinesia in Parkinson's disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology. 44:1994;892-898
51. Peinemann A., Lehner C., Mentschel C., Munchau A., Conrad B., Siebner H.R. Subthreshold 5-Hz repetitive transcranial magnetic stimulation of the human primary motor cortex reduces intracortical paired-pulse inhibition. Neurosci Lett. 296:2000;21-24
52. Pierantozzi M., Palmieri M.G., Marciani M.G., Bernardi G., Giacomini P., Stanzione P. Effect of apomorphine on cortical inhibition in Parkinson's disease patients: a transcranial magnetic stimulation study. Exp Brain Res. 141:2001;52-62
53. Pierantozzi M., Palmieri M.G., Mazzone P., Marciani M.G., Rossini P.M., Stefani A., Giacomini P., Peppe A., Stanzione P. Deep brain stimulation of both subthalamic nucleus and internal globus pallidus restores intracortical inhibition in Parkinson's disease paralleling apomorphine effects: a paired magnetic stimulation study. Clin Neurophysiol. 113:2002;108-113
54. Plewnia C., Lotze M., Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. NeuroReport. 14:2003;609-612
55. Priori A., Berardelli A., Inghilleri M., Accornero N., Manfredi M. Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson's disease and drug-induced parkinsonism. Brain. 117:1994;317-323
56. Ridding M.C., Inzelberg R., Rothwell J.C. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol. 37:1995;181-188
57. Romeo S., Gilio F., Pedace F., Ozkaynak S., Inghilleri M., Manfredi M., Berardelli A. Changes in the cortical silent period after repetitive magnetic stimulation of cortical motor areas. Exp Brain Res. 135:2000;504-510
58. Romero J.R., Anschel D., Sparing R., Gangitano M., Pascual-Leone A. Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol. 113:2002;101-107
59. Rossini P.M., Barker A.T., Berardelli A., Caramia M.D., Caruso G., Cracco R.Q., Dimitrijevic M.R., Hallett M., Katayama Y., Lücking C.H., Maertens de Noordhout A.L., Marsden C.D., Murray N.M.F., Rothwell J.C., Swash M., Tomberg C. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 91:1994;79-92
60. Sabatini U., Boulanouar K., Fabre N., Martin F., Carel C., Colonnese C., Bozzao L., Berry I., Montastruc J.L., Chollet F., Rascol O. Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain. 123:2000;394-403
61. Samuel M., Ceballos-Baumann A.O., Blin J., Uema T., Boecker H., Passingham R.E., Brooks D.J. Evidence for lateral premotor and parietal overactivity in Parkinson's disease during sequential and bimanual movements: a PET study. Brain. 120:1997;963-976
62. Sanger T.D., Garg R.R., Chen R. Interactions between two different inhibitory systems in the human motor cortex. J Physiol (Lond). 530:2001;307-317
63. Shimamoto H., Takasaki K., Shigemori M., Imaizumi T., Ayabe M., Shoji H. Therapeutic effect and mechanism of repetitive transcranial magnetic stimulation in Parkinson's disease. J Neurol. 248:2001;48-52
64. Siebner H.R., Tormos J.M., Ceballos-Baumann A.O., Auer C., Catala M.D., Conrad B., Pascual-Leone A. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp. Neurology. 52:1999;529-537
65. Siebner H.R., Mentschel C., Auer C., Conrad B. Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson's disease. NeuroReport. 10:1999;589-594
66. Siebner H.R., Mentschel C., Auer C., Lehner C., Conrad B. Repetitive transcranial magnetic stimulation causes a short-term increase in the duration of the cortical silent period in patients with Parkinson's disease. Neurosci Lett. 284:2000;147-150
67. Siebner H.R., Rossmeier C., Mentschel C., Peinemann A., Conrad B. Short-term motor improvement after sub-threshold 5-Hz repetitive transcranial magnetic stimulation of the primary motor hand area in Parkinson's disease. J Neurol Sci. 178:2000;91-94
68. Siebner H.R., Peller M., Willoch F., Minoshima S., Boecker H., Auer C., Drzezga A., Conrad B., Bartenstein P. Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology. 54:2000;956-963
69. Sommer M, Kamm T, Tergau F, Ulm G, Paulus W. Repetitive paired-pulse transcranial magnetic stimulation affects corticospinal excitability and finger tapping in Parkinson's disease. Clin Neurophysiol 2002;113:944-50.
70. Strafella A.P., Valzania F., Nassetti S.A., Tropeani A., Bisulli A., Santangelo M., Tassinari C.A. Effects of chronic levodopa and pergolide treatment on cortical excitability in patients with Parkinson's disease: a transcranial magnetic stimulation study. Clin Neurophysiol. 111:2000;1198-1202
71. Strafella A.P., Paus T., Fraraccio M., Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. 126:2003;2609-2615
72. Tergau F., Wassermann E.M., Paulus W., Ziemann U. Lack of clinical improvement in patients with Parkinson's disease after low and high frequency repetitive transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Suppl. 51:1999;281-288
73. Thobois S., Dominey P.F., Decety J., Pollak P., Gregoire M.C., Le Bars D., Broussolle E. Motor imagery in normal subjects and in asymmetrical Parkinson's disease: a PET study. Neurology. 55:2000;996-1002
74. Thobois S., Dominey P., Fraix V., Mertens P., Guenot M., Zimmer L., Pollak P., Benabid A.L., Broussolle E. Effects of subthalamic nucleus stimulation on actual and imagined movement in Parkinson's disease: a PET study. J Neurol. 249:2002;1689-1698
75. Touge T., Gerschlager W., Brown P., Rothwell J.C. Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol. 112:2001;2138-2145
76. Valls-Sole J., Pascual-Leone A., Brasil-Neto J.P., Cammarota A., McShane L., Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson's disease. Neurology. 44:1994;735-741
77. Wassermann E.M., Wedegaertner F.R., Ziemann U., George M.S., Chen R. Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett. 250:1998;141-144
78. Wu T., Sommer M., Tergau F., Paulus W. Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett. 287:2000;37-40
79. Young M.S., Triggs W.J., Bowers D., Greer M., Friedman W.A. Stereotactic pallidotomy lengthens the transcranial magnetic cortical stimulation silent period in Parkinson's disease. Neurology. 49:1997;1278-1283
80. Ziemann U., Rothwell J.C., Ridding M.C. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol. 496:1996;873-881