Skip to main content
Top

02-05-2024 | Spinocerebellar Ataxia | Research

Single-Session Cerebellar Transcranial Direct Current Stimulation Improves Postural Stability and Reduces Ataxia Symptoms in Spinocerebellar Ataxia

Authors: Rodrigo Brito, João Victor Fabrício, Aurine Araujo, Gabriel Barreto, Adriana Baltar, Kátia Monte-Silva

Published in: The Cerebellum

Login to get access

Abstract

Spinocerebellar ataxia (SCA) results in balance and coordination impairment, and current treatments have limited efficacy. Recent evidence suggests that combining postural training with cerebellar transcranial direct current stimulation (ctDCS) can improve these symptoms. However, the combined effects of ctDCS and postural training on individuals with spinocerebellar ataxia remain underexplored. Ten volunteers with (SCA type 3) participated in a triple-blind, randomized, crossover study to receive a single session of ctDCS (2 mA for 20 min) and a sham ctDCS session separated by at least one week. The Biodex Balance System was used to assess balance at each session, measuring overall stability index, anteroposterior stability index, and medial-lateral stability index. As secondary outcomes, cerebellar ataxia symptoms were evaluated using the 8-item Scale for Assessment and Rating of Ataxia. The assessments were conducted before and after each session. The results indicated that ctDCS enhanced the overall stability index when compared to sham ctDCS (Z = -2.10, p = 0.03), although it did not significantly affect the anteroposterior or medial-lateral stability indices. Compared to the baseline, a single session of ctDCS reduced appendicular symptoms related to cerebellar ataxia, as evidenced by improvements in the nose-finger test (Z = -2.07, p = 0.04), fast alternating hand movements (Z = -2.15, p = 0.03), and heel-to-shin slide (Z = -1.91, p = 0.05). In conclusion, our study suggests that a single session of ctDCS, in combination with postural training, can enhance balance and alleviate ataxia symptoms in individuals with cerebellar ataxia. This study was approved by the local research ethics committee (No. 2.877.813) and registered on clinicaltrials.org (NCT04039048 - https://​www.​clinicaltrials.​gov/​study/​NCT04039048) on 2019-07-28.
Literature
1.
go back to reference Katagiri N, Kawakami S, Okuyama S, Koseki T, Kudo D, Namba S, et al. Single-session cerebellar transcranial direct current stimulation affects postural control learning and cerebellar brain inhibition in healthy individuals. Cerebellum. 2021;20:203–11.CrossRefPubMed Katagiri N, Kawakami S, Okuyama S, Koseki T, Kudo D, Namba S, et al. Single-session cerebellar transcranial direct current stimulation affects postural control learning and cerebellar brain inhibition in healthy individuals. Cerebellum. 2021;20:203–11.CrossRefPubMed
2.
go back to reference Benussi A, Dell’Era V, Cotelli MS, Turla M, Casali C, Padovani A, et al. Long term clinical and neurophysiological effects of cerebellar transcranial direct current stimulation in patients with neurodegenerative ataxia. Brain Stimul. 2017;10:242–50.CrossRefPubMed Benussi A, Dell’Era V, Cotelli MS, Turla M, Casali C, Padovani A, et al. Long term clinical and neurophysiological effects of cerebellar transcranial direct current stimulation in patients with neurodegenerative ataxia. Brain Stimul. 2017;10:242–50.CrossRefPubMed
3.
go back to reference 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;30:1701–5.CrossRefPubMed 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;30:1701–5.CrossRefPubMed
4.
go back to reference Benussi A, Dell’Era V, Cantoni V, Bonetta E, Grasso R, Manenti R, et al. Cerebello-spinal tDCS in ataxia: a randomized, double-blind, sham-controlled, crossover trial. Neurology. 2018;91:e1090–101.CrossRefPubMed Benussi A, Dell’Era V, Cantoni V, Bonetta E, Grasso R, Manenti R, et al. Cerebello-spinal tDCS in ataxia: a randomized, double-blind, sham-controlled, crossover trial. Neurology. 2018;91:e1090–101.CrossRefPubMed
5.
go back to reference Ferrucci R, Marceglia S, Vergari M, Cogiamanian F, Mrakic-Sposta S, Mameli F, et al. Cerebellar transcranial direct current stimulation impairs the practice-dependent proficiency increase in working memory. J Cogn Neurosci. 2008;20:1687–97.CrossRefPubMed Ferrucci R, Marceglia S, Vergari M, Cogiamanian F, Mrakic-Sposta S, Mameli F, et al. Cerebellar transcranial direct current stimulation impairs the practice-dependent proficiency increase in working memory. J Cogn Neurosci. 2008;20:1687–97.CrossRefPubMed
6.
go back to reference Galea JM, Jayaram G, Ajagbe L, Celnik P. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci. 2009;29:9115–22.CrossRefPubMedPubMedCentral Galea JM, Jayaram G, Ajagbe L, Celnik P. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci. 2009;29:9115–22.CrossRefPubMedPubMedCentral
7.
go back to reference Grimaldi G, Argyropoulos GP, Bastian A, Cortes M, Davis NJ, Edwards DJ, et al. Cerebellar transcranial direct current stimulation (ctDCS): a novel approach to understanding cerebellar function in health and disease. Neuroscientist. 2016;22:83–97.CrossRefPubMedPubMedCentral Grimaldi G, Argyropoulos GP, Bastian A, Cortes M, Davis NJ, Edwards DJ, et al. Cerebellar transcranial direct current stimulation (ctDCS): a novel approach to understanding cerebellar function in health and disease. Neuroscientist. 2016;22:83–97.CrossRefPubMedPubMedCentral
8.
go back to reference Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol. 1995;37:703–13.CrossRefPubMed Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol. 1995;37:703–13.CrossRefPubMed
9.
go back to reference Ferrucci R, Brunoni AR, Parazzini M, Vergari M, Rossi E, Fumagalli M, et al. Modulating human procedural learning by cerebellar transcranial direct current stimulation. Cerebellum. 2013;12:485–92.CrossRefPubMed Ferrucci R, Brunoni AR, Parazzini M, Vergari M, Rossi E, Fumagalli M, et al. Modulating human procedural learning by cerebellar transcranial direct current stimulation. Cerebellum. 2013;12:485–92.CrossRefPubMed
10.
go back to reference Poortvliet P, Hsieh B, Cresswell A, Au J, Meinzer M. Cerebellar transcranial direct current stimulation improves adaptive postural control. Clin Neurophysiol. 2018;129:33–41.CrossRefPubMed Poortvliet P, Hsieh B, Cresswell A, Au J, Meinzer M. Cerebellar transcranial direct current stimulation improves adaptive postural control. Clin Neurophysiol. 2018;129:33–41.CrossRefPubMed
11.
go back to reference Yosephi MH, Ehsani F, Zoghi M, Jaberzadeh S. Multi-session anodal tDCS enhances the effects of postural training on balance and postural stability in older adults with high fall risk: primary motor cortex versus cerebellar stimulation. Brain Stimul. 2018;11:1239–50.CrossRefPubMed Yosephi MH, Ehsani F, Zoghi M, Jaberzadeh S. Multi-session anodal tDCS enhances the effects of postural training on balance and postural stability in older adults with high fall risk: primary motor cortex versus cerebellar stimulation. Brain Stimul. 2018;11:1239–50.CrossRefPubMed
12.
go back to reference Mendonça MS, Goulardins JB, Souza C, de O, Monte- Silva K, Tanaka C. Aplicação simultânea de estimulação transcraniana por corrente contínua cerebelar anódica para reabilitação do equilíbrio na ataxia cerebelar: relato de caso. Rev Pesqui em Fisioter. 2021;11:427–34.CrossRef Mendonça MS, Goulardins JB, Souza C, de O, Monte- Silva K, Tanaka C. Aplicação simultânea de estimulação transcraniana por corrente contínua cerebelar anódica para reabilitação do equilíbrio na ataxia cerebelar: relato de caso. Rev Pesqui em Fisioter. 2021;11:427–34.CrossRef
13.
go back to reference Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1:206–23.CrossRefPubMed Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1:206–23.CrossRefPubMed
14.
go back to reference Arnold BL, Schmitz RJ. Examination of balance measures produced by the biodex stability system. J Athl Train. 1998;33:323–7.PubMedPubMedCentral Arnold BL, Schmitz RJ. Examination of balance measures produced by the biodex stability system. J Athl Train. 1998;33:323–7.PubMedPubMedCentral
15.
go back to reference Schmitz-Hübsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006;66:1717–20.CrossRefPubMed Schmitz-Hübsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006;66:1717–20.CrossRefPubMed
16.
go back to reference Schober P, Boer C, Schwarte LA. Correlation coefficients: appropriate use and interpretation. Anesth Analg. 2018;126:1763–8.CrossRefPubMed Schober P, Boer C, Schwarte LA. Correlation coefficients: appropriate use and interpretation. Anesth Analg. 2018;126:1763–8.CrossRefPubMed
18.
go back to reference Ivanenko Y, Gurfinkel VS. Human postural control. Front Neurosci. 2018;12:171.CrossRef Ivanenko Y, Gurfinkel VS. Human postural control. Front Neurosci. 2018;12:171.CrossRef
19.
go back to reference Woollacott MH, Shumway-Cook A, Nashner LM. Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev. 1986;23:97–114.CrossRefPubMed Woollacott MH, Shumway-Cook A, Nashner LM. Aging and posture control: changes in sensory organization and muscular coordination. Int J Aging Hum Dev. 1986;23:97–114.CrossRefPubMed
20.
go back to reference Behrens M, Mau-Moeller A, Lischke A, Katlun F, Gube M, Zschorlich V, et al. Mental fatigue increases gait variability during dual-task walking in old adults. J Gerontol Biol Sci Med Sci. 2018;73:792–7.CrossRef Behrens M, Mau-Moeller A, Lischke A, Katlun F, Gube M, Zschorlich V, et al. Mental fatigue increases gait variability during dual-task walking in old adults. J Gerontol Biol Sci Med Sci. 2018;73:792–7.CrossRef
21.
go back to reference Brahms M, Heinzel S, Rapp M, Mückstein M, Hortobágyi T, Stelzel C, et al. The acute effects of mental fatigue on balance performance in healthy young and older adults - a systematic review and meta-analysis. Acta Psychol. 2022;225:103540.CrossRef Brahms M, Heinzel S, Rapp M, Mückstein M, Hortobágyi T, Stelzel C, et al. The acute effects of mental fatigue on balance performance in healthy young and older adults - a systematic review and meta-analysis. Acta Psychol. 2022;225:103540.CrossRef
22.
go back to reference Nardone A, Tarantola J, Giordano A, Schieppati M. Fatigue effects on body balance. Electroencephalogr Clin Neurophysiol. 1997;105:309–20.CrossRefPubMed Nardone A, Tarantola J, Giordano A, Schieppati M. Fatigue effects on body balance. Electroencephalogr Clin Neurophysiol. 1997;105:309–20.CrossRefPubMed
23.
go back to reference Malek N, Makawita C, Al-Sami Y, Aslanyan A, de Silva R. A systematic review of the spectrum and prevalence of non-motor symptoms in adults with hereditary cerebellar ataxias. Mov Disord Clin Pract. 2022;9:1027–39.CrossRefPubMedPubMedCentral Malek N, Makawita C, Al-Sami Y, Aslanyan A, de Silva R. A systematic review of the spectrum and prevalence of non-motor symptoms in adults with hereditary cerebellar ataxias. Mov Disord Clin Pract. 2022;9:1027–39.CrossRefPubMedPubMedCentral
24.
go back to reference Martinez ARM, Nunes MB, Faber I, D’Abreu A, Lopes-Cendes Í, França MC Jr. Fatigue and its associated factors in spinocerebellar ataxia type 3/Machado-Joseph disease. Cerebellum. 2017;16:118–21.CrossRefPubMed Martinez ARM, Nunes MB, Faber I, D’Abreu A, Lopes-Cendes Í, França MC Jr. Fatigue and its associated factors in spinocerebellar ataxia type 3/Machado-Joseph disease. Cerebellum. 2017;16:118–21.CrossRefPubMed
25.
go back to reference Brusse E, Brusse-Keizer MGJ, Duivenvoorden HJ, van Swieten JC. Fatigue in spinocerebellar ataxia: patient self-assessment of an early and disabling symptom. Neurology. 2011;76:953–9.CrossRefPubMedPubMedCentral Brusse E, Brusse-Keizer MGJ, Duivenvoorden HJ, van Swieten JC. Fatigue in spinocerebellar ataxia: patient self-assessment of an early and disabling symptom. Neurology. 2011;76:953–9.CrossRefPubMedPubMedCentral
26.
go back to reference Gorniak SL. The relationship between task difficulty and motor performance complexity. Atten Percept Psychophys. 2019;81:12–9.CrossRefPubMed Gorniak SL. The relationship between task difficulty and motor performance complexity. Atten Percept Psychophys. 2019;81:12–9.CrossRefPubMed
27.
go back to reference Singer RN, Gerson RF. Task classification and strategy utilization in motor skills. Res Q Exerc Sport. 1981;52:100–16.CrossRefPubMed Singer RN, Gerson RF. Task classification and strategy utilization in motor skills. Res Q Exerc Sport. 1981;52:100–16.CrossRefPubMed
28.
go back to reference MacLullich AMJ, Edmond CL, Ferguson KJ, Wardlaw JM, Starr JM, Seckl JR, et al. Size of the neocerebellar vermis is associated with cognition in healthy elderly men. Brain Cogn. 2004;56:344–8.CrossRefPubMed MacLullich AMJ, Edmond CL, Ferguson KJ, Wardlaw JM, Starr JM, Seckl JR, et al. Size of the neocerebellar vermis is associated with cognition in healthy elderly men. Brain Cogn. 2004;56:344–8.CrossRefPubMed
29.
31.
go back to reference 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;41:2437–47.CrossRefPubMed 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;41:2437–47.CrossRefPubMed
32.
go back to reference Maas RPPWM, Teerenstra S, Toni I, Klockgether T, Schutter DJLG, van de Warrenburg BPC. Cerebellar transcranial direct current stimulation in spinocerebellar ataxia type 3: a randomized, double-blind, sham-controlled trial. Neurotherapeutics. 2022;19:1259–72.CrossRefPubMedPubMedCentral Maas RPPWM, Teerenstra S, Toni I, Klockgether T, Schutter DJLG, van de Warrenburg BPC. Cerebellar transcranial direct current stimulation in spinocerebellar ataxia type 3: a randomized, double-blind, sham-controlled trial. Neurotherapeutics. 2022;19:1259–72.CrossRefPubMedPubMedCentral
35.
go back to reference Tezenas du Montcel S, Petit E, Olubajo T, Faber J, Lallemant-Dudek P, Bushara K, et al. Baseline clinical and blood biomarkers in patients with preataxic and early-stage disease spinocerebellar ataxia 1 and 3. Neurology. 2023;100:e1836–48.CrossRefPubMedPubMedCentral Tezenas du Montcel S, Petit E, Olubajo T, Faber J, Lallemant-Dudek P, Bushara K, et al. Baseline clinical and blood biomarkers in patients with preataxic and early-stage disease spinocerebellar ataxia 1 and 3. Neurology. 2023;100:e1836–48.CrossRefPubMedPubMedCentral
37.
go back to reference Diallo A, Jacobi H, Schmitz-Hübsch T, Cook A, Labrum R, Durr A, et al. Body mass index decline is related to spinocerebellar ataxia disease progression. Mov Disord Clin Pract. 2017;4:689–97.CrossRefPubMedPubMedCentral Diallo A, Jacobi H, Schmitz-Hübsch T, Cook A, Labrum R, Durr A, et al. Body mass index decline is related to spinocerebellar ataxia disease progression. Mov Disord Clin Pract. 2017;4:689–97.CrossRefPubMedPubMedCentral
38.
go back to reference Yang J-S, Chen P-P, Lin M-T, Qian M-Z, Lin H-X, Chen X-P, et al. Association between body mass index and disease severity in chinese spinocerebellar ataxia type 3 patients. Cerebellum. 2018;17:494–8.CrossRefPubMed Yang J-S, Chen P-P, Lin M-T, Qian M-Z, Lin H-X, Chen X-P, et al. Association between body mass index and disease severity in chinese spinocerebellar ataxia type 3 patients. Cerebellum. 2018;17:494–8.CrossRefPubMed
39.
go back to reference Roeske S, Filla I, Heim S, Amunts K, Helmstaedter C, Wüllner U, et al. Progressive cognitive dysfunction in spinocerebellar ataxia type 3. Mov Disord. 2013;28:1435–8.CrossRefPubMed Roeske S, Filla I, Heim S, Amunts K, Helmstaedter C, Wüllner U, et al. Progressive cognitive dysfunction in spinocerebellar ataxia type 3. Mov Disord. 2013;28:1435–8.CrossRefPubMed
40.
go back to reference Benussi A, Cantoni V, Manes M, Libri I, Dell’Era V, Datta A, et al. Motor and cognitive outcomes of cerebello-spinal stimulation in neurodegenerative ataxia. Brain. 2021;144:2310–21.CrossRefPubMed Benussi A, Cantoni V, Manes M, Libri I, Dell’Era V, Datta A, et al. Motor and cognitive outcomes of cerebello-spinal stimulation in neurodegenerative ataxia. Brain. 2021;144:2310–21.CrossRefPubMed
Metadata
Title
Single-Session Cerebellar Transcranial Direct Current Stimulation Improves Postural Stability and Reduces Ataxia Symptoms in Spinocerebellar Ataxia
Authors
Rodrigo Brito
João Victor Fabrício
Aurine Araujo
Gabriel Barreto
Adriana Baltar
Kátia Monte-Silva
Publication date
02-05-2024
Publisher
Springer US
Published in
The Cerebellum
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-024-01696-9