CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2021; 79(07): 630-646
DOI: 10.1590/0004-282X-ANP-2020-0381
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Use of non-invasive stimulation in movement disorders: a critical review

O uso da estimulação não-invasiva em distúrbios do movimento: uma revisão crítica
1   Universidade Federal do Rio Grande do Norte, Departamento de Medicina Integrada, Natal RN, Brazil.
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2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia, Centro de Distúrbios do Movimento, São Paulo SP, Brazil.
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2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia, Centro de Distúrbios do Movimento, São Paulo SP, Brazil.
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3   Universidade Estadual de Campinas, São Paulo SP, Brazil.
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4   Hospital do Servidor Público Estadual, São Paulo SP, Brazil.
5   Universidade Federal de São Paulo, São Paulo SP, Brazil.
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6   Universidade Federal de Minas Gerais, Departamento de Medicina Interna, Unidade de Distúrbios do Movimento, Belo Horizonte MG, Brazil.
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7   Universidade de Brasília, Laboratório de Neurociências e Comportamento, Brasília DF, Brazil.
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7   Universidade de Brasília, Laboratório de Neurociências e Comportamento, Brasília DF, Brazil.
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8   Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre RS, Brazil.
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9   Hospital Governador Celso Ramos, Serviço de Neurologia, Florianópolis SC, Brazil.
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2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia, Centro de Distúrbios do Movimento, São Paulo SP, Brazil.
10   Radboud University Medical Centre, Donders Institute for Brain, Cognition and Behavior, Department of Neurology, Nijmegen, Netherlands.
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11   Universidade do Estado do Rio de Janeiro, Unidade de Distúrbios do Movimento, Rio de Janeiro RJ, Brazil.
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4   Hospital do Servidor Público Estadual, São Paulo SP, Brazil.
5   Universidade Federal de São Paulo, São Paulo SP, Brazil.
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12   Instituto de Neurologia de Curitiba, Curitiba PR, Brazil.
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5   Universidade Federal de São Paulo, São Paulo SP, Brazil.
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13   Hospital Santa Marcelina, Departamento de Neurologia e Neurocirurgia Funcional, São Paulo SP, Brazil.
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6   Universidade Federal de Minas Gerais, Departamento de Medicina Interna, Unidade de Distúrbios do Movimento, Belo Horizonte MG, Brazil.
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14   Universidade Estadual de Londrina, Serviço de Neurologia, Londrina PR, Brazil.
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15   Hospital da Criança de Brasília José Alencar, Unidade Pediátrica de Distúrbios do Movimento, Brasília DF, Brazil.
,
R.R. Magno  Júnior
16   Universidade Federal do Maranhão, Hospital Universitário, São Luís MA, Brazil.
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17   Santa Casa de Misericórdia de Porto Alegre, Departamento de Neurologia, Porto Alegre RS, Brazil.
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18   Hospital Mãe de Deus, Serviço de Neurologia, Porto Alegre RS, Brazil.
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2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia, Centro de Distúrbios do Movimento, São Paulo SP, Brazil.
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19   University of Toronto, Toronto Western Hospital - UHN, Division of Neurology, Morton and Gloria Shulman Movement Disorders Centre and Edmond J. Safra Program in Parkinson’s Disease, Toronto ON, Canada.
20   Krembil Brain Institute, Toronto ON, Canada.
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21   Universidade do Estado do Amazonas, Manaus AM, Brazil.
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2   Universidade de São Paulo, Faculdade de Medicina, Departamento de Neurologia, Centro de Distúrbios do Movimento, São Paulo SP, Brazil.
,
on behalf of Neuromodulation for Movement Disorders Study Group, Brazilian Academy of Neurology › Author Affiliations

Abstract

Background: Noninvasive stimulation has been widely used in the past 30 years to study and treat a large number of neurological diseases, including movement disorders. Objective: In this critical review, we illustrate the rationale for use of these techniques in movement disorders and summarize the best medical evidence based on the main clinical trials performed to date. Methods: A nationally representative group of experts performed a comprehensive review of the literature in order to analyze the key clinical decision-making factors driving transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS) in movement disorders. Classes of evidence and recommendations were described for each disease. Results: Despite unavoidable heterogeneities and low effect size, TMS is likely to be effective for treating motor symptoms and depression in Parkinson’s disease (PD). The efficacy in other movement disorders is unclear. TMS is possibly effective for focal hand dystonia, essential tremor and cerebellar ataxia. Additionally, it is likely to be ineffective in reducing tics in Tourette syndrome. Lastly, tDCS is likely to be effective in improving gait in PD. Conclusions: There is encouraging evidence for the use of noninvasive stimulation on a subset of symptoms in selected movement disorders, although the means to optimize protocols for improving positive outcomes in routine clinical practice remain undetermined. Similarly, the best stimulation paradigms and responder profile need to be investigated in large clinical trials with established therapeutic and assessment paradigms that could also allow genuine long-term benefits to be determined.

Resumo

Introdução: A estimulação não-invasiva tem sido amplamente utilizada nos últimos 30 anos no estudo e no tratamento de um grande número de doenças neurológicas, incluindo distúrbios do movimento. Objetivos: Nesta revisão crítica, discutimos o embasamento científico do uso da estimulação não-invasiva em distúrbios do movimento e as evidências científicas dos principais ensaios clínicos realizados. Métodos: Um grupo de especialistas realizou uma revisão crítica abrangente da literatura a fim de analisar as principais aplicações da estimulação magnética transcraniana (EMT) e da estimulação transcraniana por corrente contínua (ETCC) em distúrbios do movimento. As classes de evidência e de recomendação foram descritas para cada doença. Resultados: Apesar da grande variabilidade da metodologia e baixo efeito clínico, a EMT é provavelmente eficaz para o tratamento dos sintomas motores e da depressão na doença de Parkinson. A eficácia em outros distúrbios do movimento ainda é incerta. A EMT é possivelmente eficaz para o tratamento da distonia focal da mão, do tremor essencial e da ataxia cerebelar. No entanto, é provavelmente ineficaz na redução dos tiques na síndrome de Tourette. Finalmente, a ETCC é provavelmente eficaz na melhora da marcha na doença de Parkinson. Conclusões: As evidências até o momento sugerem que a estimulação não-invasiva pode ser benéfica para o alívio de alguns sintomas em determinados distúrbios do movimento como a doença de Parkinson, o tremor essencial, a distonia e a ataxia. Os protocolos de aplicação e paradigmas de estimulação ainda precisam ser investigados em ensaios clínicos maiores, assim como os seus efeitos a longo prazo.

Authors’ contributions:

CG, RGC: conceptualization, validation, writing - original draft; RBC, CF: writing - original draft; FS, RS, DM, PB, NA, CRMR, FCF, TC, MS, DDF, MC, BAAGV, MSGR, RM, LBM, PDSM, MRRJ, LHTF, CEM, ERB, RPM, MVDC: conceptualization, review and editing.




Publication History

Received: 13 August 2020

Accepted: 21 October 2020

Article published online:
10 July 2023

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  • References

  • 1 Edwards MJ, Talelli P, Rothwell JC. Clinical applications of transcranial magnetic stimulation in patients with movement disorders. Lancet Neurol. 2008 Sep;7(9):827-40. https://doi.org/10.1016/S1474-4422(08)70190-X
  • 2 Salinas FS, Lancaster JL, Fox PT. Detailed 3D models of the induced electric field of transcranial magnetic stimulation coils. Phys Med Biol. 2007 May 21;52(10):2879-92. https://doi.org/10.1088/0031-9155/52/10/016
  • 3 Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004 Sep 30;44(1):5-21. https://doi.org/10.1016/j.neuron.2004.09.012
  • 4 Latorre A, Rocchi L, Berardelli A, et al. The use of transcranial magnetic stimulation as a treatment for movement disorders: a critical review. Mov Disord. 2019 Jun;34(6):769-82. https://doi.org/10.1002/mds.27705
  • 5 Antal A, Paulus W. Transcranial alternating current stimulation (tACS). Front Hum Neurosci. 2013 Jun 28;7:317. https://doi.org/10.3389/fnhum.2013.00317
  • 6 Kim SJ, Paeng SH, Kang SY. Stimulation in supplementary motor area versus motor cortex for freezing of gait in Parkinson’s disease. J Clin Neurol. 2018 Jul;14(3):320-6. https://doi.org/10.3988/jcn.2018.14.3.320
  • 7 Cury RG, Carra R, Reis J, Barbosa ER. Optimizing noninvasive stimulation to treat gait problems in Parkinson disease. Arch Phys Med Rehabil. 2020 Jun;101(6):1097-8. https://doi.org/10.1016/j.apmr.2019.10.198
  • 8 Horn A, Reich M, Vorwerk J, et al. Connectivity predicts deep brain stimulation outcome in Parkinson disease. Ann Neurol. 2017 Jul;82(1):67-78. https://doi.org/10.1002/ana.24974
  • 9 Brito M, Teixeira MJ, Mendes MM, et al. Exploring the clinical outcomes after deep brain stimulation in Tourette syndrome. J Neurol Sci. 2019 Jul 15;402:48-51. https://doi.org/10.1016/j.jns.2019.05.011
  • 10 Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain. 2003 Dec;126(12):2609-15. https://doi.org/10.1093/brain/awg268
  • 11 Watanabe T, Hanajima R, Shirota Y, et al. Effects of rTMS of pre-supplementary motor area on fronto basal ganglia network activity during stop-signal task. J Neurosci. 2015 Mar 25;35(12):4813-23. https://doi.org/10.1523/JNEUROSCI.3761-14.2015
  • 12 Gaynor LMFD, Kühn AA, Dileone M, et al. Suppression of beta oscillations in the subthalamic nucleus following cortical stimulation in humans. Eur J Neurosci. 2008 Oct;28(8):1686-95. https://doi.org/10.1111/j.1460-9568.2008.06363.x
  • 13 Campos TF, Beckenkamp PR, Moseley AM. Usage evaluation of a resource to support evidence-based physiotherapy: the Physiotherapy Evidence Database (PEDro). Physiotherapy. 2013 Sep;99(3):252-7. https://doi.org/10.1016/j.physio.2012.12.001
  • 14 American Academy of Neurology. Appendix C: AAN Classification of evidence for the rating of a therapeutic study. Continuum (Minneap Minn). 2015 Aug;21(4):1169. https://doi.org/10.1212/01.CON.0000470920.20859.fe
  • 15 Li S, Jiao R, Zhou X, Chen S. Motor recovery and antidepressant effects of repetitive transcranial magnetic stimulation on Parkinson disease: a PRISMA-compliant meta-analysis. Medicine (Baltimore). 2020 May;99(18):e19642. https://doi.org/10.1097/MD.202003810000019642
  • 16 Yang C, Guo Z, Peng H, et al. Repetitive transcranial magnetic stimulation therapy for motor recovery in Parkinson’s disease: a Meta-analysis. Brain Behav. 2018 Nov;8(11):e01132. https://doi.org/10.1002/brb3.1132
  • 17 Khedr EM, Mohamed KO, Ali AM, Hasan AM. The effect of repetitive transcranial magnetic stimulation on cognitive impairment in Parkinson’s disease with dementia: pilot study. Restor Neurol Neurosci. 2020 Feb 11;38(1):55-66. https://doi.org/10.3233/RNN-190956
  • 18 Mi T-M, Garg S, Ba F, et al. High-frequency rTMS over the supplementary motor area improves freezing of gait in Parkinson’s disease: a randomized controlled trial. Parkinsonism Relat Disord. 2019 Nov;68:85-90. https://doi.org/10.1016/j.parkreldis.2019.10.009
  • 19 Khedr EM, Al-Fawal B, Wraith AA, et al. The effect of 20 Hz versus 1 Hz repetitive transcranial magnetic stimulation on motor dysfunction in Parkinson’s disease: which is more beneficial? J Parkinsons Dis. 2019 May 23;9(2):379-87. https://doi.org/10.3233/JPD-181540
  • 20 Hanoğlu L, Saricaoglu M, Toprak G, et al. Preliminary findings on the role of high-frequency (5Hz) rTMS stimulation on M1 and pre-SMA regions in Parkinson’s disease. Neurosci Lett. 2020 Apr 17;724:134837. https://doi.org/10.1016/j.neulet.2020.134837
  • 21 Khedr EM, Mohamed KO, Soliman RK, et al. The effect of high-frequency repetitive transcranial magnetic stimulation on advancing Parkinson’s disease with dysphagia: double blind randomized clinical trial. Neurorehabil Neural Repair. 2019 Jun;33(6):442-52. https://doi.org/10.1177/1545968319847968
  • 22 França C, de Andrade DC, Teixeira MJ, et al. Effects of cerebellar neuromodulation in movement disorders: a systematic review. Brain Stimulat. 2018 Mar-Apr;11(2):249-60. https://doi.org/10.1016/j.brs.2017.11.015
  • 23 Hai-Jiao W, Ge T, Li-na Z, et al. The efficacy of repetitive transcranial magnetic stimulation for Parkinson disease patients with depression. Int J Neurosci. 2020 Jan;130(1):19-27. https://doi.org/10.1080/00207454.2018.1495632
  • 24 Goodwill AM, Lum JAG, Hendy AM, et al. Using non-invasive transcranial stimulation to improve motor and cognitive function in Parkinson’s disease: a systematic review and meta-analysis. Sci Rep. 2017 Nov 1;7(1):14840. https://doi.org/10.1038/s41598-017-13260-z
  • 25 Eggers C, Günther M, Rothwell J, et al. Theta burst stimulation over the supplementary motor area in Parkinson’s disease. J Neurol. 2015 Feb;262(2):357-64. https://doi.org/10.1007/s00415-014-7572-8
  • 26 Tard C, Devanne H, Defebvre L, Delval A. Single session intermittent theta-burst stimulation on the left premotor cortex does not alleviate freezing of gait in Parkinson’s disease. Neurosci Lett. 2016 Aug 15;628:1-9. https://doi.org/10.1016/j.neulet.2016.05.061
  • 27 Hill AT, McModie S, Fung W, et al. Impact of prefrontal intermittent theta-burst stimulation on working memory and executive function in Parkinson’s disease: A double-blind sham-controlled pilot study. Brain Res. 2020 Jan 1;1726:146506. https://doi.org/10.1016/j.brainres.2019.146506
  • 28 Orrù G, Baroni M, Cesari V, et al. The effect of single and repeated tDCS sessions on motor symptoms in Parkinson’s disease: a systematic review. Arch Ital Biol. 2019 Sep 30;157(2-3):89-101. https://doi.org/10.12871/aib.v157i2-3.4707
  • 29 Simpson MW, Mak M. The effect of transcranial direct current stimulation on upper limb motor performance in Parkinson’s disease: a systematic review. J Neurol. 2020 Dec;267(12):3479-88. https://doi.org/10.1007/s00415-019-09385-y
  • 30 Lee HK, Ahn SJ, Shin YM, et al. Does transcranial direct current stimulation improve functional locomotion in people with Parkinson’s disease? a systematic review and meta-analysis. J Neuroeng Rehabil. 2019 Jul 8;16(1):84. https://doi.org/10.1186/s12984-019-0562-4
  • 31 Albanese A, Bhatia K, Bressman SB, et al. Phenomenology and classification of dystonia: a consensus update. Mov Disord. 2013 Jun 15;28(7)863-73. https://doi.org/10.1002/mds.25475
  • 32 Thompson VB, Jinnah HA, Hess EJ. Convergent mechanisms in etiologically-diverse dystonias. Expert Opin Ther Targets. 2011 Dec;15(12):1387-403. https://doi.org/10.1517/14728222.2011.641533
  • 33 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 Dec;126(12):2710-25. https://doi.org/10.1093/brain/awg282
  • 34 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 Feb;52(3):529-37. https://doi.org/10.1212/WNL.52.3.529
  • 35 Kimberley TJ, Borich MR, Arora S, Siebner HR. Multiple sessions of low-frequency repetitive transcranial magnetic stimulation in focal hand dystonia: clinical and physiological effects. Restor Neurol Neurosci. 2013;31(5):533-42. https://doi.org/10.3233/RNN-120259
  • 36 Bradnam LV, Graetz LJ, McDonnell MN, Ridding MC. Anodal transcranial direct current stimulation to the cerebellum improves handwriting and cyclic drawing kinematics in focal hand dystonia. Front Hum Neurosci. 2015 May 18;9:286. https://doi.org/10.3389/fnhum.2015.00286
  • 37 Rosset-Llobet J, Fàbregas-Molas S, Pascual-Leone Á. Effect of transcranial direct current stimulation on neurorehabilitation of task-specific dystonia: a double-blind, randomized clinical trial. Med Probl Perform Art. 2015 Sep 1;30(3):178-84. https://doi.org/10.21091/mppa.2015.3033
  • 38 Furuya S, Nitsche MA, Paulus W, Altenmüller E. Surmounting retraining limits in musicians’ dystonia by transcranial stimulation. Ann Neurol. 2014 May;75(5):700-7. https://doi.org/10.1002/ana.24151
  • 39 Buttkus F, Weidenmüller M, Schneider S, et al. Failure of cathodal direct current stimulation to improve fine motor control in musician’s dystonia: cathodal tDCS as a treatment for focal dystonia? Mov Disord. 2010 Feb 15;25(3):389-94. https://doi.org/10.1002/mds.22938
  • 40 Buttkus F, Baur V, Jabusch H-C, et al. Single-session tDCS-supported retraining does not improve fine motor control in musician’s dystonia. Restor Neurol Neurosci. 2011;29(2):85-90. https://doi.org/10.3233/RNN-2011-0582
  • 41 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 Jan;128(1):104-15. https://doi.org/10.1093/brain/awh315
  • 42 Borich M, Arora S, Kimberley TJ. Lasting effects of repeated rTMS application in focal hand dystonia. Restor Neurol Neurosci. 2009 Jan 1;27(1):55-65. https://doi.org/10.3233/RNN-2009-0461
  • 43 Huang Y-Z, Lu C-S, Rothwell JC, et al. Modulation of the disturbed motor network in dystonia by multisession suppression of premotor cortex. PLoS One. 2012 Oct 10;7(10):e47574. https://doi.org/10.1371/journal.pone.0047574
  • 44 Havrankova P, Jech R, Walker ND, et al. Repetitive TMS of the somatosensory cortex improves writer’s cramp and enhances cortical activity. Neuro Endocrinol Lett. 2010;31(1):73-86.
  • 45 Koch G, Porcacchia P, Ponzo V, et al. Effects of two weeks of cerebellar theta burst stimulation in cervical dystonia patients. Brain Stimul. 2014 Jul-Aug;7(4):564-72. https://doi.org/10.1016/j.brs.2014.05.002
  • 46 Richardson SP, Tinaz S, Chen R. Repetitive transcranial magnetic stimulation in cervical dystonia: effect of site and repetition in a randomized pilot trial. PLoS One. 2015 Apr 29;10(4):e0124937. https://doi.org/10.1371/journal.pone.0124937
  • 47 Kranz G, Shamim EA, Lin PT, et al. Transcranial magnetic brain stimulation modulates blepharospasm: a randomized controlled study. Neurology. 2010 Oct 19;75(16):1465-71. https://doi.org/10.1212/WNL.0b013e3181f8814d
  • 48 Gironell A, Kulisevsky J, Lorenzo J, et al. Transcranial magnetic stimulation of the cerebellum in essential tremor: a controlled study. Arch Neurol. 2002 Mar;59(3):413-7. https://doi.org/10.1001/archneur.59.3.413
  • 49 Avanzino L, Bove M, Tacchino A, et al. Cerebellar involvement in timing accuracy of rhythmic finger movements in essential tremor. Eur J Neurosci. 2009 Nov;30(10):1971-9. https://doi.org/10.1111/j.1460-9568.2009.06984.x
  • 50 Hellriegel H, Schulz EM, Siebner HR, et al. Continuous theta-burst stimulation of the primary motor cortex in essential tremor. Clin Neurophysiol. 2012 May;123(5):1010-5. https://doi.org/10.1016/j.clinph.2011.08.033
  • 51 Popa T, Russo M, Vidailhet M, et al. Cerebellar rTMS stimulation may induce prolonged clinical benefits in essential tremor, and subjacent changes in functional connectivity: an open label trial. Brain Stimul. 2013 Mar 1;6(2):175-9. https://doi.org/10.1016/j.brs.2012.04.009
  • 52 Gironell A, Martínez-Horta S, Aguilar S, et al. Transcranial direct current stimulation of the cerebellum in essential tremor: a controlled study. Brain Stimul. 2014 May 1;7(3):491-2. https://doi.org/10.1016/j.brs.2014.02.001
  • 53 Chuang W-L, Huang Y-Z, Lu C-S, Chen R-S. Reduced cortical plasticity and GABAergic modulation in essential tremor. Mov Disord. 2014 Apr;29(4):501-7. https://doi.org/10.1002/mds.25809
  • 54 Bologna M, Rocchi L, Leodori G, et al. Cerebellar continuous theta burst stimulation in essential tremor. Cerebellum. 2015 Apr;14(2):133-41. https://doi.org/10.1007/s12311-014-0621-0
  • 55 Badran BW, Glusman CE, Austelle CW, et al. A double-blind, sham-controlled pilot trial of pre-supplementary motor area (Pre-SMA) 1 Hz rTMS to treat essential tremor. Brain Stimul. 2016 Nov 1;9(6):945-7. https://doi.org/10.1016/j.brs.2016.08.003
  • 56 Shin H-W, Hallett M, Sohn YH. Cerebellar repetitive transcranial magnetic stimulation for patients with essential tremor. Parkinsonism Relat Disord. 2019 Jul 1;64:304-7. https://doi.org/10.1016/j.parkreldis.2019.03.019
  • 57 Manor B, Greenstein PE, Davila-Perez P, et al. Repetitive transcranial magnetic stimulation in spinocerebellar ataxia: a pilot randomized controlled trial. Front Neurol. 2019 Feb 12;10:73. https://doi.org/10.3389/fneur.2019.00073
  • 58 Benussi A, Dell’Era V, Cantoni V, et al. Cerebello-spinal tDCS in ataxia: a randomized, double-blind, sham-controlled, crossover trial. Neurology. 2018 Sep 18;91(12):e1090-101. https://doi.org/10.1212/WNL.20200381202003816210
  • 59 Benussi A, Koch G, Cotelli M, et al. Cerebellar transcranial direct current stimulation in patients with ataxia: a double-blind, randomized, sham-controlled study. Mov Disord. 2015 Oct;30(12):1701-5. https://doi.org/10.1002/mds.26356
  • 60 Bonnì S, Ponzo V, Caltagirone C, Koch G. Cerebellar theta burst stimulation in stroke patients with ataxia. Funct Neurol. 2014 Jan-Mar;29(1):41-5.
  • 61 Kim W-S, Jung SH, Oh MK, et al. Effect of repetitive transcranial magnetic stimulation over the cerebellum on patients with ataxia after posterior circulation stroke: a pilot study. J Rehabil Med. 2014 May;46(5):418-23. https://doi.org/10.2340/16501977-1802
  • 62 Koch G, Rossi S, Prosperetti C, et al. Improvement of hand dexterity following motor cortex rTMS in multiple sclerosis patients with cerebellar impairment. Mult Scler. 2008 Aug;14(7):995-8. https://doi.org/10.1177/1352458508088710
  • 63 Grecco L, Duarte NAC, Marques V, et al. Cerebellar transcranial direct current stimulation in a child with ataxic cerebral palsy: a case report. Gait Posture. 2015 Sep;42 Suppl 1:S93-4. https://doi.org/10.1016/j.gaitpost.2015.06.171
  • 64 Shimizu H, Tsuda T, Shiga Y, et al. Therapeutic efficacy of transcranial magnetic stimulation for hereditary spinocerebellar degeneration. Tohoku J Exp Med. 1999 Nov;189(3):203-11. https://doi.org/10.1620/tjem.189.203
  • 65 Shiga Y, Tsuda T, Itoyama Y, et al. Transcranial magnetic stimulation alleviates truncal ataxia in spinocerebellar degeneration. J Neurol Neurosurg Psychiatry. 2002 Jan;72(1):124-6. https://doi.org/10.1136/jnnp.72.1.124
  • 66 Ihara Y, Takata H, Tanabe Y, et al. Influence of repetitive transcranial magnetic stimulation on disease severity and oxidative stress markers in the cerebrospinal fluid of patients with spinocerebellar degeneration. Neurol Res. 2005 Apr;27(3):310-3. https://doi.org/10.1179/016164105X39897
  • 67 Grimaldi G, Manto M. Anodal transcranial direct current stimulation (tDCS) decreases the amplitudes of long-latency stretch reflexes in cerebellar ataxia. Ann Biomed Eng. 2013 Nov;41(11):2437-47. https://doi.org/10.1007/s10439-013-0846-y
  • 68 Benussi A, Dell’Era V, Cotelli MS, et al. Long term clinical and neurophysiological effects of cerebellar transcranial direct current stimulation in patients with neurodegenerative ataxia. Brain Stimul. 2017 Mar 1;10(2):242-50. https://doi.org/10.1016/j.brs.2016.11.001
  • 69 Benussi A, Dell’Era V, Cantoni V, et al. Cerebello-spinal tDCS in ataxia: a randomized, double-blind, sham-controlled, crossover trial. Neurology. 2018 Sep 18;91(12):e1090-101. https://doi.org/10.1212/WNL.20200381202003816210
  • 70 Grados M, Huselid R, Duque-Serrano L. Transcranial magnetic stimulation in tourette syndrome: a historical perspective, its current use and the influence of comorbidities in treatment response. Brain Sci. 2018 Jul 6;8(7):129. https://doi.org/10.3390/brainsci8070129
  • 71 Le K, Liu L, Sun M, et al. Transcranial magnetic stimulation at 1Hertz improves clinical symptoms in children with Tourette syndrome for at least 6 months. J Clin Neurosci. 2013 Feb 1;20(2):257-62. https://doi.org/10.1016/j.jocn.2012.01.049
  • 72 Kwon HJ, Lim WS, Lim MH, et al. 1-Hz low frequency repetitive transcranial magnetic stimulation in children with Tourette’s syndrome. Neurosci Lett. 2011 Mar 29;492(1):1-4. https://doi.org/10.1016/j.neulet.2011.01.007
  • 73 Wu SW, Maloney T, Gilbert DL, et al. Functional MRI-navigated repetitive transcranial magnetic stimulation over supplementary motor area in Chronic Tic Disorders. Brain Stimulat. 2014 Mar-Apr;7(2):212-8. https://doi.org/10.1016/j.brs.2013.10.005
  • 74 Landeros-Weisenberger A, Mantovani A, Motlagh MG, et al. Randomized sham controlled double-blind trial of repetitive transcranial magnetic stimulation for adults with severe Tourette syndrome. Brain Stimulat. 2015 May 1;8(3):574-81. https://doi.org/10.1016/j.brs.2014.11.015
  • 75 Orth M, Kirby R, Richardson MP, et al. Subthreshold rTMS over pre-motor cortex has no effect on tics in patients with Gilles de la Tourette syndrome. Clin Neurophysiol. 2005 Apr;116(4):764-8. https://doi.org/10.1016/j.clinph.2004.10.003
  • 76 Munchau A, Bloem BR, Thilo KV, et al. Repetitive transcranial magnetic stimulation for Tourette syndrome. Neurology. 2002 Dec 10;59(11):1789-91. https://doi.org/10.1212/01.WNL.0000036615.25044.50
  • 77 Dyke K, Jackson GM, Nixon E, Jackson SR. Effects of single-session cathodal transcranial direct current stimulation on tic symptoms in Tourette’s syndrome. Exp Brain Res. 2019 Nov;237(11):2853-63. https://doi.org/10.1007/s00221-019-05637-5