Generic placeholder image

Current Neuropharmacology

Author(s): Roberta Ferrucci*, Tommaso Bocci, Francesca Cortese, Fabiana Ruggiero and Alberto Priori

DOI: 10.2174/1570159X15666171114142422

DownloadDownload PDF Flyer Cite As
Noninvasive Cerebellar Stimulation as a Complement Tool to Pharmacotherapy

Page: [14 - 20] Pages: 7

  • * (Excluding Mailing and Handling)

Abstract

Background: Cerebellar ataxias represent a wide and heterogeneous group of diseases characterized by balance and coordination disturbance, dysarthria, dyssynergia and adyadococinesia, caused by a dysfunction in the cerebellum. In recent years there has been growing interest in discovering therapeutical strategy for specific forms of cerebellar ataxia. Together with pharmacological studies, there has been growing interest in non-invasive cerebellar stimulation techniques to improve ataxia and limb coordination. Both transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS) are non-invasive techniques to modulate cerebro and cerebellar cortex excitability using magnetic or electric fields.

Methods: Here we aim to review the most relevant studies regarding the application of TMS and tDCS for the treatment of cerebellar ataxia.

Conclusion: As pharmacological strategies were shown to be effective in specific forms of cerebellar ataxia and are not devoid of collateral effects, non-invasive stimulation may represent a promising strategy to improve residual cerebellar circuits functioning and a complement tool to pharmacotherapy.

Keywords: tDCS, cerebellar tDCS, cerebellar TMS, ataxia, non invasive neuromodulation, cerebellum.

Graphical Abstract

[1]
Bird, T.D. Hereditary Ataxia Overview., 1993. [Epub a head of print]
[2]
Feil, K.; Bremova, T.; Muth, C.; Schniepp, R.; Teufel, J.; Strupp, M. Update on the pharmacotherapy of cerebellar ataxia and nystagmus. Cerebellum, 2016, 15(1), 38-42. [http://dx.doi.org/10. 1007/s12311-015-0733-1]. [PMID: 26519380].
[3]
Kearney, M.; Orrell, R.W.; Fahey, M.; Pandolfo, M. Antioxidants and other pharmacological treatments for Friedreich ataxia. Cochrane Database Syst. Rev., 2012, 18(4), CD007791. [PMID: 22513953].
[4]
Li, Y.; Polak, U.; Bhalla, A.D.; Rozwadowska, N.; Butler, J.S.; Lynch, D.R.; Dent, S.Y.R.; Napierala, M. Excision of expanded GAA repeats alleviates the molecular phenotype of Friedreich’s Ataxia. Mol. Ther., 2015, 23(6), 1055-1065. [http://dx.doi.org/10. 1038/mt.2015.41]. [PMID: 25758173].
[5]
Elincx-Benizri, S.; Glik, A.; Merkel, D.; Arad, M.; Freimark, D.; Kozlova, E.; Cabantchik, I.; Hassin-Baer, S. Clinical experience with deferiprone treatment for Friedreich ataxia. J. Child Neurol., 2016, 31(8), 1036-1040. [http://dx.doi.org/10.1177/0883073816636087]. [PMID: 27029487].
[6]
Saccà, F.; Puorro, G.; Marsili, A.; Antenora, A.; Pane, C.; Casali, C.; Marcotulli, C.; Defazio, G.; Liuzzi, D.; Tatillo, C.; Cambriglia, D.M.; Schiano di Cola, G.; Giuliani, L.; Guardasole, V.; Salzano, A.; Ruvolo, A.; De Rosa, A.; Cittadini, A.; De Michele, G.; Filla, A. Long-term effect of epoetin alfa on clinical and biochemical markers in friedreich ataxia. Mov. Disord., 2016, 31(5), 734-741. [http://dx.doi.org/10.1002/mds.26552]. [PMID: 26879839].
[7]
Calap-Quintana, P.; Soriano, S.; Llorens, J.V.; Al-Ramahi, I.; Botas, J.; Moltó, M.D.; Martínez-Sebastián, M.J. TORC1 inhibition by rapamycin promotes antioxidant defences in a Drosophila model of Friedreich’s Ataxia. PLoS One, 2015, 10(7), e0132376. [http://dx.doi.org/10.1371/journal.pone.0132376]. [PMID: 26158631].
[8]
Bürk, K. Friedreich Ataxia: current status and future prospects. Cerebellum Ataxias, 2017, 4, 4. [http://dx.doi.org/10.1186/s40673-017-0062-x]. [PMID: 28405347].
[9]
Mitoma, H.; Hadjivassiliou, M.; Honnorat, J. Guidelines for treatment of immune-mediated cerebellar ataxias. Cerebellum Ataxias, 2015, 2, 14. [http://dx.doi.org/10.1186/s40673-015-0034-y]. [PMID: 26561527].
[10]
Gungor, S.; Kilic, B.; Arslan, M.; Ozgen, U. Hodgkin’s lymphoma associated with paraneoplastic cerebellar degeneration in children: a case report and review of the literature. Childs Nerv. Syst., 2017, 33(3), 509-512. [http://dx.doi.org/10.1007/s00381-016-3284-y]. [PMID: 27796550].
[11]
Ferrucci, R.; Bocci, T.; Cortese, F.; Ruggiero, F.; Priori, A. Cerebellar transcranial direct current stimulation in neurological disease. Cerebellum Ataxias, 2016, 3(1), 16. [http://dx.doi.org/ 10.1186/s40673-016-0054-2]. [PMID: 27595007].
[12]
Groiss, S.J.; Ugawa, Y. Cerebellar stimulation in ataxia. Cerebellum, 2012, 11(2), 440-442. [http://dx.doi.org/10.1007/s12311-011-0329-3]. [PMID: 22116658].
[13]
Pope, P.A.; Miall, R.C. Restoring cognitive functions using non-invasive brain stimulation techniques in patients with cerebellar disorders. Front. Psychiatry, 2014, 5, 33. [http://dx.doi.org/10. 3389/fpsyt.2014.00033]. [PMID: 24765079].
[14]
Grimaldi, G.; Argyropoulos, G.P.; Boehringer, A.; Celnik, P.; Edwards, M.J.; Ferrucci, R.; Galea, J.M.; Groiss, S.J.; Hiraoka, K.; Kassavetis, P.; Lesage, E.; Manto, M.; Miall, R.C.; Priori, A.; Sadnicka, A.; Ugawa, Y.; Ziemann, U. Non-invasive cerebellar stimulation--a consensus paper. Cerebellum, 2014, 13(1), 121-138. [http://dx.doi.org/10.1007/s12311-013-0514-7]. [PMID: 23943521].
[15]
Abele, M.; Bürk, K.; Andres, F.; Topka, H.; Laccone, F.; Bösch, S.; Brice, A.; Cancel, G.; Dichgans, J.; Klockgether, T. Autosomal dominant cerebellar ataxia type I. Nerve conduction and evoked potential studies in families with SCA1, SCA2 and SCA3. Brain, 1997, 120(Pt 12), 2141-2148. [http://dx.doi.org/10.1093/brain/120. 12.2141]. [PMID: 9448569].
[16]
Schöls, L.; Amoiridis, G.; Büttner, T.; Przuntek, H.; Epplen, J.T.; Riess, O. Autosomal dominant cerebellar ataxia: phenotypic differences in genetically defined subtypes? Ann. Neurol., 1997, 42(6), 924-932. [http://dx.doi.org/10.1002/ana.410420615]. [PMID: 9403486].
[17]
Schwenkreis, P.; Tegenthoff, M.; Witscher, K.; Börnke, C.; Przuntek, H.; Malin, J.P.; Schöls, L. Motor cortex activation by transcranial magnetic stimulation in ataxia patients depends on the genetic defect. Brain, 2002, 125(Pt 2), 301-309. [http://dx.doi.org/10.1093/ brain/awf023]. [PMID: 11844730].
[18]
Ganos, C.; Zittel, S.; Minnerop, M.; Schunke, O.; Heinbokel, C.; Gerloff, C.; Zühlke, C.; Bauer, P.; Klockgether, T.; Münchau, A.; Bäumer, T. Clinical and neurophysiological profile of four German families with spinocerebellar ataxia type 14. Cerebellum, 2014, 13(1), 89-96. [http://dx.doi.org/10.1007/s12311-013-0522-7]. [PMID: 24030789].
[19]
Farzan, F.; Wu, Y.; Manor, B.; Anastasio, E.M.; Lough, M.; Novak, V.; Greenstein, P.E.; Pascual-Leone, A. Cerebellar TMS in treatment of a patient with cerebellar ataxia: evidence from clinical, biomechanics and neurophysiological assessments. Cerebellum, 2013, 12(5), 707-712. [http://dx.doi.org/10.1007/s12311-013-0485-8]. [PMID: 23625327].
[20]
Koch, G.; D’Angelo, E. Magnetic stimulation of the cerebellum. Moving towards the clinic. Funct. Neurol., 2014, 29(1), 5. [PMID: 25014043].
[21]
Shiga, Y.; Tsuda, T.; Itoyama, Y.; Shimizu, H.; Miyazawa, K.I.; Jin, K.; Yamazaki, T. Transcranial magnetic stimulation alleviates truncal ataxia in spinocerebellar degeneration. J. Neurol. Neurosurg. Psychiatry, 2002, 72(1), 124-126. [http://dx.doi.org/10.1136/ jnnp.72.1.124]. [PMID: 11784843].
[22]
Benussi, A.; Dell’Era, V.; Cotelli, M.S.; Turla, M.; Casali, C.; Padovani, A.; Borroni, B. Long term clinical and neurophysiological effects of cerebellar transcranial direct current stimulation in patients with neurodegenerative ataxia. Brain Stimul., 2017, 10(2), 242-250. [http://dx.doi.org/10.1016/j.brs.2016.11.001]. [PMID: 27838276].
[23]
Benussi, A.; Koch, G.; Cotelli, M.; Padovani, A.; Borroni, B. Cerebellar transcranial direct current stimulation in patients with ataxia: A double-blind, randomized, sham-controlled study. Mov. Disord., 2015, 30(12), 1701-1705. [http://dx.doi.org/10.1002/mds.26356]. [PMID: 26274840].
[24]
Bodranghien, F.; Oulad Ben Taib, N.; Van Maldergem, L.; Manto, M. A postural tremor highly responsive to transcranial cerebello-cerebral DCS in ARCA3. Front. Neurol., 2017, 8(71), 71. [PMID: 28316589].
[25]
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, 41(11), 2437-2447. [http://dx.doi.org/10.1007/s10439-013-0846-y]. [PMID: 23780473].
[26]
Grimaldi, G.; Oulad Ben Taib, N.; Manto, M.; Bodranghien, F. Marked reduction of cerebellar deficits in upper limbs following transcranial cerebello-cerebral DC stimulation: tremor reduction and re-programming of the timing of antagonist commands. Front. Syst. Neurosci., 2014, 8, 9. [http://dx.doi.org/10.3389/fnsys.2014. 00009]. [PMID: 24523678].
[27]
Shimizu, H.; Tsuda, T.; Shiga, Y.; Miyazawa, K.; Onodera, Y.; Matsuzaki, M.; Nakashima, I.; Furukawa, K.; Aoki, M.; Kato, H.; Yamazaki, T.; Itoyama, Y. Therapeutic efficacy of transcranial magnetic stimulation for hereditary spinocerebellar degeneration. Tohoku J. Exp. Med., 1999, 189(3), 203-211. [http://dx.doi.org/10. 1620/tjem.189.203]. [PMID: 10674722].
[28]
Ihara, Y.; Takata, H.; Tanabe, Y.; Nobukuni, K.; Hayabara, T. 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, 27(3), 310-313. [http://dx.doi.org/10.1179/016164105X39897]. [PMID: 15845214].
[29]
Kim, W-S.; Jung, S.H.; Oh, M.K.; Min, Y.S.; Lim, J.Y.; Paik, N.J. Effect of repetitive transcranial magnetic stimulation over the cerebellum on patients with ataxia after posterior circulation stroke: A pilot study. J. Rehabil. Med., 2014, 46(5), 418-423. [http://dx.doi. org/10.2340/16501977-1802]. [PMID: 24658396].
[30]
Bonnì, S.; Ponzo, V.; Caltagirone, C.; Koch, G. Cerebellar theta burst stimulation in stroke patients with ataxia. Funct. Neurol., 2014, 29(1), 41-45. [PMID: 25014048].
[31]
Cury, R.G.; Teixeira, M.J.; Galhardoni, R.; Barboza, V.R.; Alho, E.; Seixas, C.M.; Lepski, G.; Ciampi de Andrade, D. Neuronavigation-guided transcranial magnetic stimulation of the dentate nucleus improves cerebellar ataxia: A sham-controlled, double-blind n = 1 study. Parkinsonism Relat. Disord., 2015, 21(8), 999-1001. [http://dx.doi.org/10.1016/j.parkreldis.2015.05.010]. [PMID: 26022755].
[32]
Rüb, U.; de Vos, R.A.; Schultz, C.; Brunt, E.R.; Paulson, H.; Braak, H. Spinocerebellar ataxia type 3 (Machado-Joseph disease): severe destruction of the lateral reticular nucleus. Brain, 2002, 125(Pt 9), 2115-2124. [http://dx.doi.org/10.1093/brain/awf208]. [PMID: 12183356].
[33]
Zee, D.S.; Yamazaki, A.; Butler, P.H.; Gücer, G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J. Neurophysiol., 1981, 46(4), 878-899. [http://dx.doi.org/10.1152/jn. 1981.46.4.878]. [PMID: 7288469].
[34]
Shin, M.; Moghadam, S.H.; Sekirnjak, C.; Bagnall, M.W.; Kolkman, K.E.; Jacobs, R.; Faulstich, M.; du Lac, S. Multiple types of cerebellar target neurons and their circuitry in the vestibulo-ocular reflex. J. Neurosci., 2011, 31(30), 10776-10786. [http://dx.doi.org/ 10.1523/JNEUROSCI.0768-11.2011]. [PMID: 21795530].
[35]
Sönmezoğlu, K.; Sperling, B.; Henriksen, T.; Tfelt-Hansen, P.; Lassen, N.A. Reduced contralateral hemispheric flow measured by SPECT in cerebellar lesions: crossed cerebral diaschisis. Acta Neurol. Scand., 1993, 87(4), 275-280. [http://dx.doi.org/10.1111/j. 1600-0404.1993.tb05507.x]. [PMID: 8503255].
[36]
Farias da Guarda, S.N.; Cohen, L.G.; da Cunha Pinho, M.; Yamamoto, F.I.; Marchiori, P.E.; Scaff, M.; Conforto, A.B. Interhemispheric asymmetry of corticomotor excitability after chronic cerebellar infarcts. Cerebellum, 2010, 9(3), 398-404. [http://dx.doi.org/ 10.1007/s12311-010-0176-7]. [PMID: 20461489].
[37]
Priori, A.; Ciocca, M.; Parazzini, M.; Vergari, M.; Ferrucci, R. Transcranial cerebellar direct current stimulation and transcutaneous spinal cord direct current stimulation as innovative tools for neuroscientists. J. Physiol., 2014, 592(16), 3345-3369. [http://dx. doi.org/10.1113/jphysiol.2013.270280]. [PMID: 24907311].