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Neurotherapeutics. 2008 April; 5(2): 345–361.
PMCID: PMC3270324
NIHMSID: NIHMS230186

Noninvasive brain stimulation for Parkinson’s disease and dystonia

Summary

Repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) are promising noninvasive cortical stimulation methods for adjunctive treatment of movement disorders. They avoid surgical risks and provide theoretical advantages of specific neural circuit neuromodulation. Neuromodulatory effects depend on extrinsic stimulation factors (cortical target, frequency, intensity, duration, number of sessions), intrinsic patient factors (disease process, individual variability and symptoms, state of medication treatment), and outcome measures. Most studies to date have shown beneficial effects of rTMS or tDCS on clinical symptoms in Parkinson’s disease (PD) and support the notion of spatial specificity to the effects on motor and nonmotor symptoms. Stimulation parameters have varied widely, however, and some studies are poorly controlled. Studies of rTMS or tDCS in dystonia have provided abundant data on physiology, but few on clinical effects. Multiple mechanisms likely contribute to the clinical effects of rTMS and tDCS in movement disorders, including normalization of cortical excitability, rebalancing of distributed neural network activity, and induction of dopamine release. It remains unclear how to individually adjust rTMS or tDCS factors for the most beneficial effects on symptoms of PD or dystonia. Nonetheless, the noninvasive nature, minimal side effects, positive effects in preliminary clinical studies, and increasing evidence for rational mechanisms make rTMS and tDCS attractive for ongoing investigation.

Key Words: Parkinson’s disease, dystonia, transcranial magnetic stimulation, transcranial direct current stimulation, cortical stimulation

References

1. Mink JW. The basal ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol. 2003;60:1365–1368. doi: 10.1001/archneur.60.10.1365. [PubMed] [Cross Ref]
2. Pahwa R, Factor SA, Lyons KE, et al. Practice Parameter: treatment of Parkinson disease with motor fluctuations and dyskinesia (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology. 2006;66:983–995. doi: 10.1212/01.wnl.0000215250.82576.87. [PubMed] [Cross Ref]
3. Jankovic J. Treatment of dystonia. Lancet Neurol. 2006;5:864–872. doi: 10.1016/S1474-4422(06)70574-9. [PubMed] [Cross Ref]
4. Weintraub D, Moberg PJ, Duda JE, Katz IR, Stern MB. Effect of psychiatric and other nonmotor symptoms on disability in Parkinson’s disease. J Am Geriatr Soc. 2004;52:784–788. doi: 10.1111/j.1532-5415.2004.52219.x. [PubMed] [Cross Ref]
5. Skidmore FM, Rodriguez RL, Fernandez HH, Goodman WK, Foote KD, Okun MS. Lessons learned in deep brain stimulation for movement and neuropsychiatric disorders. CNS Spectr. 2006;11:521–536. [PubMed]
6. Albanese A, Barnes MP, Bhatia KP, et al. A systematic review on the diagnosis and treatment of primary (idiopathic) dystonia and dystonia plus syndromes: report of an EFNS/MDS-ES Task Force. Eur J Neurol. 2006;13:433–444. doi: 10.1111/j.1468-1331.2006.01537.x. [PubMed] [Cross Ref]
7. Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9:527–565. doi: 10.1146/annurev.bioeng.9.061206.133100. [PubMed] [Cross Ref]
8. Quartarone A, Siebner HR, Rothwell JC. Task-specific hand dystonia: can too much plasticity be bad for you? Trends Neurosci. 2006;29:192–199. doi: 10.1016/j.tins.2006.02.007. [PubMed] [Cross Ref]
9. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol. 1992;9:132–136. doi: 10.1097/00004691-199201000-00014. [PubMed] [Cross Ref]
10. Romero JR, 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. 2002;113:101–107. doi: 10.1016/S1388-2457(01)00693-9. [PubMed] [Cross Ref]
11. Peinemann A, Reimer B, Loer C, et al. Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex. Clin Neurophysiol. 2004;115:1519–1526. doi: 10.1016/j.clinph.2004.02.005. [PubMed] [Cross Ref]
12. Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W. Modulation of cortical excitability by weak direct current stimulation: technical, safety and functional aspects. Suppl Clin Neurophysiol. 2003;56:255–276. doi: 10.1016/S1567-424X(09)70230-2. [PubMed] [Cross Ref]
13. Helmich RC, Siebner HR, Bakker M, Münchau A, Bloem BR. Repetitive transcranial magnetic stimulation to improve mood and motor function in Parkinson’s disease. J Neurol Sci. 2006;248:84–96. doi: 10.1016/j.jns.2006.05.009. [PubMed] [Cross Ref]
14. Pascual-Leone A, Valls-Solé J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain. 1994;117:847–858. doi: 10.1093/brain/117.4.847. [PubMed] [Cross Ref]
15. Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–1403. [PubMed]
16. Touge T, Gerschlager W, Brown P, Rothwell JC. Are the aftereffects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol. 2001;112:2138–2145. doi: 10.1016/S1388-2457(01)00651-4. [PubMed] [Cross Ref]
17. Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J. Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol. 2002;113:1136–1141. doi: 10.1016/S1388-2457(02)00145-1. [PubMed] [Cross Ref]
18. Antal A, Nitsche MA, Paulus W. External modulation of visual perception in humans. Neuroreport. 2001;12:3553–3555. doi: 10.1097/00001756-200111160-00036. [PubMed] [Cross Ref]
19. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527:633–639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x. [PubMed] [Cross Ref]
20. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57:1899–1901. [PubMed]
21. Wang H, Wang X, Scheich H. LTD and LTP induced by transcranial magnetic stimulation in auditory cortex. Neuroreport. 1996;7:521–525. doi: 10.1097/00001756-199601310-00035. [PubMed] [Cross Ref]
22. Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol. 2002;543:699–708. doi: 10.1113/jphysiol.2002.023317. [PubMed] [Cross Ref]
23. Baumer T, Demiralay C, Hidding U, et al. Abnormal plasticity of the sensorimotor cortex to slow repetitive transcranial magnetic stimulation in patients with writer’s cramp. Mov Disord. 2007;22:81–90. doi: 10.1002/mds.21219. [PubMed] [Cross Ref]
24. Siebner HR, Filipovic SR, Rowe JB, et al. Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain. 2003;126:2710–2725. doi: 10.1093/brain/awg282. [PubMed] [Cross Ref]
25. Buhmann C, Gorsler A, Bäumer T, et al. Abnormal excitability of premotor—motor connections in de novo Parkinson’s disease. Brain. 2004;127:2732–2746. doi: 10.1093/brain/awh321. [PubMed] [Cross Ref]
26. Lomarev MP, Kanchana S, Bara-Jimenez W, Iyer M, Wassermann EM, Hallett M. Placebo-controlled study of rTMS for the treatment of Parkinson’s disease. Mov Disord. 2006;21:325–331. doi: 10.1002/mds.20713. [PubMed] [Cross Ref]
27. Khedr EM, Farweez HM, Islam H. Therapeutic effect of repetitive transcranial magnetic stimulation on motor function in Parkinson’s disease patients. Eur J Neurol. 2003;10:567–572. doi: 10.1046/j.1468-1331.2003.00649.x. [PubMed] [Cross Ref]
28. Fregni F, Ono CR, Santos CM, et al. Effects of antidepressant treatment with rTMS and fluoxetine on brain perfusion in PD. Neurology. 2006;66:1629–1637. doi: 10.1212/01.wnl.0000218194.12054.60. [PubMed] [Cross Ref]
29. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res. 2000;133:425–430. doi: 10.1007/s002210000432. [PubMed] [Cross Ref]
30. Kleim JA, Chan S, Ringle E, et al. BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci. 2006;9:735–737. doi: 10.1038/nn1699. [PubMed] [Cross Ref]
31. Gilio F, Currà 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;17:467–473. doi: 10.1002/mds.1255. [PubMed] [Cross Ref]
32. Fierro B, Brighina F, D’Amelio M, et al. Motor intracortical inhibition in PD: L-DOPA modulation of high-frequency rTMS effects. Exp Brain Res. 2008;184:521–528. doi: 10.1007/s00221-007-1121-y. [PubMed] [Cross Ref]
33. Gilio F, Currà A, Lorenzano C, Modugno N, Manfredi M, Berardelli A. Effects of botulinum toxin type A on intracortical inhibition in patients with dystonia. Ann Neurol. 2000;48:20–26. doi: 10.1002/1531-8249(200007)48:1<20::AID-ANA5>3.0.CO;2-U. [PubMed] [Cross Ref]
34. Fregni F, Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology: perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol. 2007;3:383–393. doi: 10.1038/ncpneuro0530. [PubMed] [Cross Ref]
35. Hallett M. Transcranial magnetic stimulation: a primer. Neuron. 2007;55:187–199. doi: 10.1016/j.neuron.2007.06.026. [PubMed] [Cross Ref]
36. Ziemann U. TMS and drugs. Clin Neurophysiol. 2004;115:1717–1729. doi: 10.1016/j.clinph.2004.03.006. [PubMed] [Cross Ref]
37. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517:591–597. doi: 10.1111/j.1469-7793.1999.0591t.x. [PubMed] [Cross Ref]
38. Di Lazzaro V, Oliviero A, Meglio M, et al. Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol. 2000;111:794–799. doi: 10.1016/S1388-2457(99)00314-4. [PubMed] [Cross Ref]
39. Paus T, Castro-Alamancos MA, Petrides M. Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci. 2001;14:1405–1411. doi: 10.1046/j.0953-816x.2001.01757.x. [PubMed] [Cross Ref]
40. Lang N, Siebner HR, Ward NS, et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci. 2005;22:495–504. doi: 10.1111/j.1460-9568.2005.04233.x. [PMC free article] [PubMed] [Cross Ref]
41. van Eimeren T, Siebner HR. An update on functional neuroimaging of parkinsonism and dystonia. Curr Opin Neurol. 2006;19:412–419. doi: 10.1097/01.wco.0000236623.68625.54. [PubMed] [Cross Ref]
42. Siebner HR, Peller M, Willoch F, et al. Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology. 2000;54:956–963. [PubMed]
43. Rounis E, Lee L, Siebner HR, et al. Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage. 2005;26:164–176. doi: 10.1016/j.neuroimage.2005.01.037. [PubMed] [Cross Ref]
44. Strafella AP, Paus T, Barrett J, Dagher A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci. 2001;21:RC157–RC157. [PubMed]
45. Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. 2003;126:2609–2615. doi: 10.1093/brain/awg268. [PubMed] [Cross Ref]
46. Koch G, Brusa L, Caltagirone C, et al. rTMS of supplementary motor area modulates therapy-induced dyskinesias in Parkinson disease. Neurology. 2005;65:623–625. doi: 10.1212/01.wnl.0000172861.36430.95. [PubMed] [Cross Ref]
47. Fregni F, Boggio PS, Bermpohl F, et al. Immediate placebo effect in Parkinson’s disease: is the subjective relief accompanied by objective improvement? Eur Neurol. 2006;56:222–229. doi: 10.1159/000096490. [PubMed] [Cross Ref]
48. de la Fuente-Fernandez R. Uncovering the hidden placebo effect in deep-brain stimulation for Parkinson’s disease. Parkinsonism Relat Disord. 2004;10:125–127. doi: 10.1016/j.parkreldis.2003.10.003. [PubMed] [Cross Ref]
49. Loo CK, Taylor JL, Gandevia SC, McDarmont BN, Mitchell PB, Sachdev PS. Transcranial magnetic stimulation (TMS) in controlled treatment studies: are some “sham” forms active? Biol Psychiatry. 2000;47:325–331. doi: 10.1016/S0006-3223(99)00285-1. [PubMed] [Cross Ref]
50. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006;117:845–850. doi: 10.1016/j.clinph.2005.12.003. [PubMed] [Cross Ref]
51. Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol. 1998;108:1–16. doi: 10.1016/S0168-5597(97)00096-8. [PubMed] [Cross Ref]
52. Belmaker B, Fitzgerald P, George MS, et al. Managing the risks of repetitive transcranial stimulation. CNS Spectr. 2003;8:489–489. [PubMed]
53. Machii K, Cohen D, Ramos-Estebanez C, Pascual-Leone A. Safety of rTMS to non-motor cortical areas in healthy participants and patients. Clin Neurophysiol. 2006;117:455–471. doi: 10.1016/j.clinph.2005.10.014. [PubMed] [Cross Ref]
54. Boylan LS, Pullman SL, Lisanby SH, Spicknall KE, Sackeim HA. Repetitive transcranial magnetic stimulation to SMA worsens complex movements in Parkinson’s disease. Clin Neurophysiol. 2001;112:259–264. doi: 10.1016/S1388-2457(00)00519-8. [PubMed] [Cross Ref]
55. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45:201–206. doi: 10.1016/j.neuron.2004.12.033. [PubMed] [Cross Ref]
56. Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K. Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res. 2004;318:121–134. doi: 10.1007/s00441-004-0956-9. [PubMed] [Cross Ref]
57. Lefaucheur JP. Motor cortex dysfunction revealed by cortical excitability studies in Parkinson’s disease: influence of antiparkinsonian treatment and cortical stimulation. Clin Neurophysiol. 2005;116:244–253. doi: 10.1016/j.clinph.2004.11.017. [PubMed] [Cross Ref]
58. Grafton ST. Contributions of functional imaging to understanding parkinsonian symptoms. Curr Opin Neurobiol. 2004;14:715–719. doi: 10.1016/j.conb.2004.10.010. [PubMed] [Cross Ref]
59. Strafella AP, Ko JH, Grant J, Fraraccio M, Monchi O. Corticostriatal functional interactions in Parkinson’s disease: a rTMS/[11C]raclopride PET study. Eur J Neurosci. 2005;22:2946–2952. doi: 10.1111/j.1460-9568.2005.04476.x. [PMC free article] [PubMed] [Cross Ref]
60. Strafella AP, Ko JH, Monchi O. Therapeutic application of transcranial magnetic stimulation in Parkinson’s disease: the contribution of expectation. Neuroimage. 2006;31:1666–1672. doi: 10.1016/j.neuroimage.2006.02.005. [PMC free article] [PubMed] [Cross Ref]
61. 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. 2001;248(Suppl 3):III48–III52. [PubMed]
62. Parkinson Study Group Cerebrospinal fluid homovanillic acid in the DATATOP study on Parkinson’s disease. Arch Neurol. 1995;52:237–245. [PubMed]
63. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Foly N, Hamdy A. Dopamine levels after repetitive transcranial magnetic stimulation of motor cortex in patients with Parkinson’s disease: preliminary results. Mov Disord. 2007;22:1046–1050. doi: 10.1002/mds.21460. [PubMed] [Cross Ref]
64. Haslinger B, Erhard P, Kampfe N, et al. Event-related functional magnetic resonance imaging in Parkinson’s disease before and after levodopa. Brain. 2001;124:558–570. doi: 10.1093/brain/124.3.558. [PubMed] [Cross Ref]
65. Sabatini U, Boulanouar K, Fabre N, et al. Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain. 2000;123:394–403. doi: 10.1093/brain/123.2.394. [PubMed] [Cross Ref]
66. Berardelli A, Rothwell JC, Thompson PD, Hallett M. Pathophysiology of bradykinesia in Parkinson’s disease. Brain. 2001;124:2131–2146. doi: 10.1093/brain/124.11.2131. [PubMed] [Cross Ref]
67. Grafton ST, Turner RS, Desmurget M, et al. Normalizing motor-related brain activity: subthalamic nucleus stimulation in Parkinson disease. Neurology. 2006;66:1192–1199. doi: 10.1212/01.wnl.0000214237.58321.c3. [PubMed] [Cross Ref]
68. Cantello R, Gianelli M, Bettucci D, Civardi C, De Angelis MS, Mutani R. Parkinson’s disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology. 1991;41:1449–1456. [PubMed]
69. Valls-Solé J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, McShane L, Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson’s disease. Neurology. 1994;44:735–741. [PubMed]
70. Chen R, Kumar S, Garg RR, Lang AE. Impairment of motor cortex activation and deactivation in Parkinson’s disease. Clin Neurophysiol. 2001;112:600–607. doi: 10.1016/S1388-2457(01)00466-7. [PubMed] [Cross Ref]
71. Wu AD, Petzinger GM, Lin CH, Kung M, Fisher B. Asymmetric corticomotor excitability correlations in early Parkinson’s disease. Mov Disord. 2007;22:1587–1593. doi: 10.1002/mds.21565. [PubMed] [Cross Ref]
72. Priori A, Berardelli A, Inghilleri M, Accomero 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. 1994;117:317–323. doi: 10.1093/brain/117.2.317. [PubMed] [Cross Ref]
73. Chen R, Garg RR, Lozano AM, Lang AE. Effects of internal globus pallidus stimulation on motor cortex excitability. Neurology. 2001;56:716–723. [PubMed]
74. Ellaway PH, Davey NJ, Maskill DW, Dick JP. The relation between bradykinesia and excitability of the motor cortex assessed using transcranial magnetic stimulation in normal and parkinsonian subjects. Electroencephalogr Clin Neurophysiol. 1995;97:169–178. doi: 10.1016/0924-980X(94)00336-6. [PubMed] [Cross Ref]
75. Málly J, Farkas R, Tóthfalusi L, Stone TW. Long-term follow-up study with repetitive transcranial magnetic stimulation (rTMS) in Parkinson’s disease. Brain Res Bull. 2004;64:259–263. doi: 10.1016/j.brainresbull.2004.07.004. [PubMed] [Cross Ref]
76. Dragaševic N, Potrebić A, Damjanović A, Stefanova E, Kostić VS. Therapeutic efficacy of bilateral prefrontal slow repetitive transcranial magnetic stimulation in depressed patients with Parkinson’s disease: an open study. Mov Disord. 2002;17:528–532. doi: 10.1002/mds.10109. [PubMed] [Cross Ref]
77. Okabe S, Hanajima R, Ohnishi T, et al. Functional connectivity revealed by single-photon emission computed tomography (SPECT) during repetitive transcranial magnetic stimulation (rTMS) of the motor cortex. Clin Neurophysiol. 2003;114:450–457. doi: 10.1016/S1388-2457(02)00408-X. [PubMed] [Cross Ref]
78. Fregni F, Santos CM, Myczkowski ML, et al. Repetitive transcranial magnetic stimulation is as effective as fluoxetine in the treatment of depression in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2004;75:1171–1174. doi: 10.1136/jnnp.2003.027060. [PMC free article] [PubMed] [Cross Ref]
79. Epstein CM, Evatt ML, Funk A, et al. An open study of repetitive transcranial magnetic stimulation in treatment-resistant depression with Parkinson’s disease. Clin Neurophysiol. 2007;118:2189–2194. doi: 10.1016/j.clinph.2007.07.010. [PMC free article] [PubMed] [Cross Ref]
80. Brusa L, Versace V, Koch G, et al. Low frequency rTMS of the SMA transiently ameliorates peak-dose LID in Parkinson’s disease. Clin Neurophysiol. 2006;117:1917–1921. doi: 10.1016/j.clinph.2006.03.033. [PubMed] [Cross Ref]
81. Tergau F, Wassermann EM, 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. 1999;51:281–288. [PubMed]
82. 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. 2003;18:382–388. doi: 10.1002/mds.10370. [PubMed] [Cross Ref]
83. Mir P, Matsunaga K, Gilio F, Quinn NP, Siebner HR, Rothwell JC. Dopaminergic drugs restore facilitatory premotor—motor interactions in Parkinson disease. Neurology. 2005;64:1906–1912. doi: 10.1212/01.WNL.0000163772.56128.A8. [PubMed] [Cross Ref]
84. Fregni F, Simon DK, Wu A, Pascual-Leone A. Non-invasive brain stimulation for Parkinson’s disease: a systematic review and meta-analysis of the literature. J Neurol Neurosurg Psychiatry. 2005;76:1614–1623. doi: 10.1136/jnnp.2005.069849. [PMC free article] [PubMed] [Cross Ref]
85. Pascual-Leone A, Valls-Solé J, Brasil-Neto JP, Cammarota A, Grafman J, Hallett M. Akinesia in Parkinson’s disease. II. Effects of subthreshold repetitive transcranial motor cortex stimulation. Neurology. 1994;44:892–898. [PubMed]
86. Ghabra MB, Hallett M, Wassermann EM. Simultaneous repetitive transcranial magnetic stimulation does not speed fine movement in PD. Neurology. 1999;52:768–770. [PubMed]
87. Siebner HR. Simultaneous repetitive transcranial magnetic stimulation does not speed fine movement in PD [Comment on: Neurology 1999;52:768-770] Neurology. 2000;54:272–272. [PubMed]
88. Siebner HR, 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. 2000;284:147–150. doi: 10.1016/S0304-3940(00)00990-3. [PubMed] [Cross Ref]
89. Siebner HR, 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. 2000;178:91–94. doi: 10.1016/S0022-510X(00)00370-1. [PubMed] [Cross Ref]
90. Siebner HR, Mentschel C, Auer C, Conrad B. Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson’s disease. Neuroreport. 1999;10:589–594. doi: 10.1097/00001756-199902250-00027. [PubMed] [Cross Ref]
91. Lefaucheur JP, Drouot X, Von Raison F, Ménard-Lefaucheur I, Cesaro P, Nguyen JP. Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson’s disease. Clin Neurophysiol. 2004;115:2530–2541. doi: 10.1016/j.clinph.2004.05.025. [PubMed] [Cross Ref]
92. Börnke C, Schulte T, Przuntek H, Müller T. Clinical effects of repetitive transcranial magnetic stimulation versus acute levodopa challenge in Parkinson’s disease. J Neural Transm Suppl 2004:61–67. [PubMed]
93. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Hamdy A. Effect of daily repetitive transcranial magnetic stimulation on motor performance in Parkinson’s disease. Mov Disord. 2006;21:2201–2205. doi: 10.1002/mds.21089. [PubMed] [Cross Ref]
94. 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. 2003;209:41–46. doi: 10.1016/S0022-510X(02)00459-8. [PubMed] [Cross Ref]
95. Shimamoto H, Morimitsu H, Sugita S, Nakahara K, Shigemori M. Therapeutic effect of repetitive transcranial magnetic stimulation in Parkinson’s disease. Rinsho Shinkeigaku. 1999;39:1264–1267. [PubMed]
96. del Olmo MF, Bello O, Cudeiro J. Transcranial magnetic stimulation over dorsolateral prefrontal cortex in Parkinson’s disease. Clin Neurophysiol. 2007;118:131–139. doi: 10.1016/j.clinph.2006.09.002. [PubMed] [Cross Ref]
97. Dias AE, Barbosa ER, Coracini K, Maia F, Marcolin MA, Fregni F. Effects of repetitive transcranial magnetic stimulation on voice and speech in Parkinson’s disease. Acta Neurol Scand. 2006;113:92–99. doi: 10.1111/j.1600-0404.2005.00558.x. [PubMed] [Cross Ref]
98. Cardoso EF, Fregni F, Martins Maia F, et al. rTMS treatment for depression in Parkinson’s disease increases BOLD responses in the left prefrontal cortex. Int J Neuropsychopharmacol 2007:1-11. [PubMed]
99. Turner RS, Grafton ST, McIntosh AR, DeLong MR, Hoffman JM. The functional anatomy of parkinsonian bradykinesia. Neuroimage. 2003;19:163–179. doi: 10.1016/S1053-8119(03)00171-X. [PubMed] [Cross Ref]
100. Brooks DJ, Piccini P, Turjanski N, Samuel M. Neuroimaging of dyskinesia. Ann Neurol. 2000;47:S154–S158. [PubMed]
101. Rascol O, Sabatini U, Brefel C, et al. Cortical motor overactivation in parkinsonian patients with L-dopa-induced peak-dose dyskinesia. Brain. 1998;121:527–533. doi: 10.1093/brain/121.3.527. [PubMed] [Cross Ref]
102. Fregni F, Boggio PS, Santos MC, et al. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord. 2006;21:1693–1702. doi: 10.1002/mds.21012. [PubMed] [Cross Ref]
103. Nitsche MA, Seeber A, Frommann K, et al. Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex. J Physiol. 2005;568:291–303. doi: 10.1113/jphysiol.2005.092429. [PubMed] [Cross Ref]
104. Boggio PS, Ferrucci R, Rigonatti SP, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci. 2006;249:31–38. doi: 10.1016/j.jns.2006.05.062. [PubMed] [Cross Ref]
105. Fahn S, Bressman SB, Marsden CD. Classification of dystonia. Adv Neurol. 1998;78:1–10. [PubMed]
106. Berardelli A, Rothwell JC, Hallett M, Thompson PD, Manfredi M, Marsden CD. The pathophysiology of primary dystonia. Brain. 1998;121:1195–1212. doi: 10.1093/brain/121.7.1195. [PubMed] [Cross Ref]
107. Hallett M. Pathophysiology of dystonia. J Neural Transm Suppl 2006:485–488. [PubMed]
108. Ceballos-Baumann AO, Brooks DJ. Basal ganglia function and dysfunction revealed by PET activation studies. Adv Neurol. 1997;74:127–139. [PubMed]
109. Lerner A, Shill H, Hanakawa T, Bushara K, Goldfine A, Hallett M. Regional cerebral blood flow correlates of the severity of writer’s cramp symptoms. Neuroimage. 2004;21:904–913. doi: 10.1016/j.neuroimage.2003.10.019. [PubMed] [Cross Ref]
110. Hu XY, Wang L, Liu H, Zhang SZ. Functional magnetic resonance imaging study of writer’s cramp. Chin Med J (Engl) 2006;119:1263–1271. [PubMed]
111. Reibisch C, Berg D, Hofmann E, Solymosi L, Naumann M. Cerebral activation patterns in patients with writer’s cramp: a functional magnetic resonance imaging study. J Neurol. 2001;248:10–17. doi: 10.1007/s004150170263. [PubMed] [Cross Ref]
112. Odergren T, Stone-Elander S, Ingvar M. Cerebral and cerebellar activation in correlation to the action-induced dystonia in writer’s cramp. Mov Disord. 1998;13:497–508. doi: 10.1002/mds.870130321. [PubMed] [Cross Ref]
113. Ibáñez V, Sadato N, Karp B, Deiber MP, Hallett M. Deficient activation of the motor cortical network in patients with writer’s cramp. Neurology. 1999;53:96–105. [PubMed]
114. Oga T, Honda M, Toma K, et al. Abnormal cortical mechanisms of voluntary muscle relaxation in patients with writer’s cramp: an fMRI study. Brain. 2002;125:895–903. doi: 10.1093/brain/awf083. [PubMed] [Cross Ref]
115. Filipović SR, Ljubisavljević M, Svetel M, Milanović S, Kacar A, Kostić VS. Impairment of cortical inhibition in writer’s cramp as revealed by changes in electromyographic silent period after transcranial magnetic stimulation. Neurosci Lett. 1997;222:167–170. doi: 10.1016/S0304-3940(97)13370-5. [PubMed] [Cross Ref]
116. Ridding MC, Sheean G, Rothwell JC, Inzelberg R, Kujirai T. Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry. 1995;59:493–498. doi: 10.1136/jnnp.59.5.493. [PMC free article] [PubMed] [Cross Ref]
117. Siebner HR, Tormos JM, Ceballos-Baumann AO, et al. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology. 1999;52:529–537. [PubMed]
118. Tinazzi M, Farina S, Edwards M, et al. Task-specific impairment of motor cortical excitation and inhibition in patients with writer’s cramp. Neurosci Lett. 2005;378:55–58. doi: 10.1016/j.neulet.2004.12.015. [PubMed] [Cross Ref]
119. Sohn YH, Hallett M. Disturbed surround inhibition in focal hand dystonia. Ann Neurol. 2004;56:595–599. doi: 10.1002/ana.20270. [PubMed] [Cross Ref]
120. Gilio F, Currà A, Inghilleri M, et al. Abnormalities of motor cortex excitability preceding movement in patients with dystonia. Brain. 2003;126:1745–1754. doi: 10.1093/brain/awg188. [PubMed] [Cross Ref]
121. Kessler KR, Rüge D, Ilić TV, Ziemann U. Short latency afferent inhibition and facilitation in patients with writer’s cramp. Mov Disord. 2005;20:238–242. doi: 10.1002/mds.20295. [PubMed] [Cross Ref]
122. Quartarone A, Bagnato S, Rizzo V, et al. Abnormal associative plasticity of the human motor cortex in writer’s cramp. Brain. 2003;126:2586–2596. doi: 10.1093/brain/awg273. [PubMed] [Cross Ref]
123. Rosenkranz K, Altenmüller E, Siggelkow S, Dengler R. Alteration of sensorimotor integration in musician’s cramp: impaired focusing of proprioception. Clin Neurophysiol. 2000;111:2040–2045. doi: 10.1016/S1388-2457(00)00460-0. [PubMed] [Cross Ref]
124. Edwards MJ, Huang YZ, Mir P, Rothwell JC, Bhatia KP. Abnormalities in motor cortical plasticity differentiate manifesting and nonmanifesting DYT1 carriers. Mov Disord. 2006;21:2181–2186. doi: 10.1002/mds.21160. [PubMed] [Cross Ref]
125. Murase N, Rothwell JC, Kaji R, et al. Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer’s cramp. Brain. 2005;128:104–115. doi: 10.1093/brain/awh315. [PubMed] [Cross Ref]
126. Lefaucheur JP, Fénelon G, Ménard-Lefaucheur I, Wendling S, Nguyen JP. Low-frequency repetitive TMS of premotor cortex can reduce painful axial spasms in generalized secondary dystonia: a pilot study of three patients. Neurophysiol Clin. 2004;34:141–145. doi: 10.1016/j.neucli.2004.07.003. [PubMed] [Cross Ref]
127. Allam N, Brasil-Neto JP, Brandao P, Weiler F, Barros Filho J, Tomaz C. Relief of primary cervical dystonia symptoms by low frequency transcranial magnetic stimulation of the premotor cortex: case report. Arq Neuropsiquiatr. 2007;65:697–699. [PubMed]
128. Siebner HR, Auer C, Conrad B. Abnormal increase in the corticomotor output to the affected hand during repetitive transcranial magnetic stimulation of the primary motor cortex in patients with writer’s cramp. Neurosci Lett. 1999;262:133–136. doi: 10.1016/S0304-3940(99)00056-7. [PubMed] [Cross Ref]
129. Stinear CM, Byblow WD. Impaired modulation of corticospinal excitability following subthreshold rTMS in focal hand dystonia. Hum Mov Sci. 2004;23:527–538. doi: 10.1016/j.humov.2004.08.022. [PubMed] [Cross Ref]
130. Gilio F, Suppa A, Bologna M, Lorenzano C, Fabbrini G, Berardelli A. Short-term cortical plasticity in patients with dystonia: a study with repetitive transcranial magnetic stimulation. Mov Disord. 2007;22:1436–1443. doi: 10.1002/mds.21465. [PubMed] [Cross Ref]
131. Quartarone A, Rizzo V, Bagnato S, et al. Homeostatic-like plasticity of the primary motor hand area is impaired in focal hand dystonia. Brain. 2005;128:1943–1950. doi: 10.1093/brain/awh527. [PubMed] [Cross Ref]
132. Rizzo V, Siebner HR, Modugno N, et al. Shaping the excitability of human motor cortex with premotor rTMS. J Physiol. 2004;554:483–495. doi: 10.1113/jphysiol.2003.048777. [PubMed] [Cross Ref]
133. Gerschlager W, Siebner HR, Rothwell JC. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology. 2001;57:449–455. [PubMed]
134. Huang YZ, Edwards MJ, Bhatia KP, Rothwell JC. One-Hz repetitive transcranial magnetic stimulation of the premotor cortex alters reciprocal inhibition in DYT1 dystonia. Mov Disord. 2004;19:54–59. doi: 10.1002/mds.10627. [PubMed] [Cross Ref]
135. Málly J, Stone TW. Improvement in parkinsonian symptoms after repetitive transcranial magnetic stimulation. J Neurol Sci. 1999;162:179–184. doi: 10.1016/S0022-510X(98)00318-9. [PubMed] [Cross Ref]
136. Málly J, Stone TW. Therapeutic and “dose-dependent” effect of repetitive microelectroshock induced by transcranial magnetic stimulation in Parkinson’s disease. J Neurosci Res. 1999;57:935–940. doi: 10.1002/(SICI)1097-4547(19990915)57:6<935::AID-JNR19>3.0.CO;2-8. [PubMed] [Cross Ref]

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