Skip to main content

Advertisement

SpringerLink
Log in

Consensus Paper: Novel Directions and Next Steps of Non-invasive Brain Stimulation of the Cerebellum in Health and Disease

  • Consensus paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

The cerebellum is involved in multiple closed-loops circuitry which connect the cerebellar modules with the motor cortex, prefrontal, temporal, and parietal cortical areas, and contribute to motor control, cognitive processes, emotional processing, and behavior. Among them, the cerebello-thalamo-cortical pathway represents the anatomical substratum of cerebellum-motor cortex inhibition (CBI). However, the cerebellum is also connected with basal ganglia by disynaptic pathways, and cerebellar involvement in disorders commonly associated with basal ganglia dysfunction (e.g., Parkinson’s disease and dystonia) has been suggested. Lately, cerebellar activity has been targeted by non-invasive brain stimulation (NIBS) techniques including transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS) to indirectly affect and tune dysfunctional circuitry in the brain. Although the results are promising, several questions remain still unsolved. Here, a panel of experts from different specialties (neurophysiology, neurology, neurosurgery, neuropsychology) reviews the current results on cerebellar NIBS with the aim to derive the future steps and directions needed. We discuss the effects of TMS in the field of cerebellar neurophysiology, the potentials of cerebellar tDCS, the role of animal models in cerebellar NIBS applications, and the possible application of cerebellar NIBS in motor learning, stroke recovery, speech and language functions, neuropsychiatric and movement disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

The concept reported in this manuscript is not associated with raw data.

Code Availability

There is no software application or custom code used in this paper.

References

  1. Baumann O, Borra RJ, Bower JM, Cullen KE, Habas C, Ivry RB, et al. Consensus Paper: The Role of the Cerebellum in Perceptual Processes. Cerebellum. 2015;14(2):197.

    Article  PubMed  Google Scholar 

  2. Allen GI, Tsukahara N. Cerebrocerebellar communication systems. Vol. 54, Physiological Reviews. Physiol Rev; 1974. p. 957–1006.

  3. Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden CD. Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol. 1991;29(4):418–27.

    Article  CAS  PubMed  Google Scholar 

  4. Thach WT. Cerebellar inputs to motor cortex. Vol. 132, Ciba Foundation symposium. Ciba Found Symp; 1987. p. 201–20.

  5. Ugawa Y, Day BL, Rothwell JC, Thompson PD, Merton PA, Marsden CD. Modulation of motor cortical excitability by electrical stimulation over the cerebellum in man. J Physiol. 1991;441(1):57–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol. 1995;37(6):703–13.

    Article  CAS  PubMed  Google Scholar 

  7. Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Vol. 32, Annual Review of Neuroscience. Annu Rev Neurosci; 2009. p. 413–34.

  8. Groiss SJ, Ugawa Y. Cerebellum. In: Handbook of Clinical Neurology. Elsevier B.V.; 2013. p. 643–53.

  9. Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46(7):831–44.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Koch G. The new era of TMS-EEG: Moving towards the clinical practice. Clin Neurophysiol. 2019;130(5):791–2.

    Article  PubMed  Google Scholar 

  11. Casula EP, Pellicciari MC, Ponzo V, Stampanoni Bassi M, Veniero D, Caltagirone C, et al. Cerebellar theta burst stimulation modulates the neural activity of interconnected parietal and motor areas. Sci Rep. 2016;6(1):1–10.

    Article  Google Scholar 

  12. Koch G, Esposito R, Motta C, Casula EP, Di Lorenzo F, Bonnì S, et al. Improving visuo-motor learning with cerebellar theta burst stimulation: Behavioral and neurophysiological evidence. Neuroimage. 2020;208:116424.

  13. Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8(11):1491–3.

    Article  CAS  PubMed  Google Scholar 

  14. Prudente CN, Hess EJ, Jinnah HA. Dystonia as a network disorder: What is the role of the cerebellum? Vol. 260, Neuroscience. Elsevier Ltd; 2014. p. 23–35.

  15. Wu T, Hallett M. The cerebellum in Parkinson’s disease. Vol. 136, Brain. Oxford University Press; 2013. p. 696–709.

  16. Grimaldi G, Argyropoulos GP, Boehringer A, Celnik P, Edwards MJ, Ferrucci R, et al. Non-invasive cerebellar stimulation - A consensus paper. Vol. 13, Cerebellum. Springer New York LLC; 2014. p. 121–38.

  17. Galea JM, Jayaram G, Ajagbe L, Celnik P. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci. 2009;29(28):9115–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Doeltgen SH, Young J, Bradnam LV. Anodal Direct Current Stimulation of the Cerebellum Reduces Cerebellar Brain Inhibition but Does Not Influence Afferent Input from the Hand or Face in Healthy Adults. Cerebellum. 2016;15(4):466–74.

    Article  PubMed  Google Scholar 

  19. Zang Y, De Schutter E. Climbing Fibers Provide Graded Error Signals in Cerebellar Learning. Front Syst Neurosci. 2019;11:46.

    Article  Google Scholar 

  20. Mitoma H, Manto M. The Era of Cerebellar Therapy. Curr Neuropharmacol. 2018;17(1):3–6.

    Article  Google Scholar 

  21. Cook AA, Fields E, Watt AJ. Losing the Beat: Contribution of Purkinje Cell Firing Dysfunction to Disease, and Its Reversal. Neuroscience. 2021;10(462):247–61.

    Article  Google Scholar 

  22. 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. Vol. 22, Neuroscientist. SAGE Publications Inc.; 2016. p. 83–97.

  23. Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kineses ZT, et al. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci. 2009;29(16):5202–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Amassian VE, Cracco RQ, Maccabee PJ, Cracco JB. Cerebello-frontal cortical projections in humans studied with the magnetic coil. Electroencephalogr Clin Neurophysiol Evoked Potentials. 1992;85(4):265–72.

    Article  CAS  PubMed  Google Scholar 

  25. Ugawa Y, Genba-Shimizu K, Rothwell JC, Iwata M, Kanazawa I. Suppression of motor cortical excitability by electrical stimulation over the cerebellum in ataxia. Ann Neurol. 1994;36(1):90–6.

    Article  CAS  PubMed  Google Scholar 

  26. Di Lazzaro V, Molinari M, Restuccia D, Leggio MG, Nardone r., Fogli D, et al. Cerebro-cerebellar interactions in man: neurophysiological studies in patients with focal cerebellar lesions. Electroencephalogr Clin Neurophysiol Evoked Potentials. 1994;93(1):27–34.

  27. Ugawa Y, Terao Y, Hanajima R, Sakai K, Furubayashi T, Machii K, et al. Magnetic stimulation over the cerebellum in patients with ataxia. Electroencephalogr Clin Neurophysiol - Evoked Potentials. 1997;104(5):453–8.

    Article  CAS  PubMed  Google Scholar 

  28. Jayaram G, Galea JM, Bastian AJ, Celnik P. Human locomotor adaptive learning is proportional to depression of cerebellar excitability. Cereb Cortex. 2011;21(8):1901–9.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Spampinato DA, Block HJ, Celnik PA. Cerebellar–M1 connectivity changes associated with motor learning are somatotopic specific. J Neurosci. 2017;37(9):2377–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shirota Y, Hamada M, Hanajima R, Terao Y, Matsumoto H, Ohminami S, et al. Cerebellar dysfunction in progressive supranuclear palsy: A transcranial magnetic stimulation study. Mov Disord. 2010;25(14):2413–9.

    Article  PubMed  Google Scholar 

  31. Hanajima R, Tsutsumi R, Shirota Y, Shimizu T, Tanaka N, Ugawa Y. Cerebellar dysfunction in essential tremor. Mov Disord. 2016;31(8):1230–4.

    Article  PubMed  Google Scholar 

  32. Meyer BU, Röricht S, Machetanz J. Reduction of corticospinal excitability by magnetic stimulation over the cerebellum in patients with large defects of one cerebellar hemisphere. Electroencephalogr Clin Neurophysiol Evoked Potentials. 1994;93(5):372–9.

    Article  CAS  PubMed  Google Scholar 

  33. Werhahn KJ, Taylor J, Ridding M, Meyer BU, Rothwell JC. Effect of transcranial magnetic stimulation over the cerebellum on the excitability of human motor cortex. Electroencephalogr Clin Neurophysiol - Electromyogr Mot Control. 1996;101(1):58–66.

    Article  CAS  Google Scholar 

  34. Fernandez L, Major BP, Teo WP, Byrne LK, Enticott PG. Assessing cerebellar brain inhibition (CBI) via transcranial magnetic stimulation (TMS): A systematic review. Vol. 86, Neuroscience and Biobehavioral Reviews. Elsevier Ltd; 2018. p. 176–206.

  35. Fisher KM, Lai HM, Baker MR, Baker SN. Corticospinal activation confounds cerebellar effects of posterior fossa stimuli. Clin Neurophysiol. 2009;120(12):2109–13.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ugawa Y. Can we see the cerebellar activation effect by TMS over the back of the head? Vol. 120, Clinical Neurophysiology. Clin Neurophysiol; 2009. p. 2006–7.

  37. Harvey RJ, Porter R, Rawson JA. Discharges of intracerebellar nuclear cells in monkeys. J Physiol. 1979;297(1):559–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Soteropoulos DS, Baker SN. Bilateral representation in the deep cerebellar nuclei. J Physiol. 2008;586(4):1117–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nashef A, Cohen O, Israel Z, Harel R, Prut Y. Cerebellar Shaping of Motor Cortical Firing Is Correlated with Timing of Motor Actions. Cell Rep. 2018;23(5):1275–85.

    Article  CAS  PubMed  Google Scholar 

  40. Hardwick RM, Lesage E, Miall RC. Cerebellar transcranial magnetic stimulation: The role of coil geometry and tissue depth. Brain Stimul. 2014;7(5):643–9.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Spampinato D, Ibáñez J, Spanoudakis M, Hammond P, Rothwell JC. Cerebellar transcranial magnetic stimulation: The role of coil type from distinct manufacturers. Brain Stimul. 2020;13(1):153–6.

    Article  PubMed  Google Scholar 

  42. Hashimoto M, Ohtsuka K. Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain. 1995;118(5):1185–93.

    Article  PubMed  Google Scholar 

  43. Miyaguchi S, Inukai Y, Matsumoto Y, Miyashita M, Takahashi R, Otsuru N, et al. Effects on motor learning of transcranial alternating current stimulation applied over the primary motor cortex and cerebellar hemisphere. J Clin Neurosci. 2020;1(78):296–300.

    Article  Google Scholar 

  44. Naro A, Leo A, Russo M, Cannavò A, Milardi D, Bramanti P, et al. Does Transcranial Alternating Current Stimulation Induce Cerebellum Plasticity? Feasibility, Safety and Efficacy of a Novel Electrophysiological Approach. Brain Stimul. 2016;9(3):388–95.

    Article  PubMed  Google Scholar 

  45. Spampinato D, Celnik P. Deconstructing skill learning and its physiological mechanisms. Cortex. 2018;1(104):90–102.

    Article  Google Scholar 

  46. Pleger B, Timmann D. The role of the human cerebellum in linguistic prediction, word generation and verbal working memory: evidence from brain imaging, non-invasive cerebellar stimulation and lesion studies. Neuropsychologia. 2018;1(115):204–10.

    Article  Google Scholar 

  47. Spampinato D, Celnik P. Temporal dynamics of cerebellar and motor cortex physiological processes during motor skill learning. 2017;7(1):1–12.

  48. Galea JM, Vazquez A, Pasricha N, Orban De Xivry JJ, Celnik P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: The motor cortex retains what the cerebellum learns. Cereb Cortex. 2011;21(8):1761–70.

  49. Penhune VB, Doyon J. Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage. 2005;26(3):801–12.

    Article  CAS  PubMed  Google Scholar 

  50. D’Angelo E. Physiology of the cerebellum. In: Handbook of Clinical Neurology. Elsevier B.V.; 2018. p. 85–108.

  51. Apps R, Hawkes R, Aoki S, Bengtsson F, Brown AM, Chen G, et al. Cerebellar Modules and Their Role as Operational Cerebellar Processing Units. Vol. 17, Cerebellum. Springer New York LLC; 2018. p. 654–82.

  52. Bareš M, Apps R, Avanzino L, Breska A, D’Angelo E, Filip P, et al. Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications Cerebellum. 2019;18(2):266–86.

    PubMed  Google Scholar 

  53. Liebrand M, Karabanov A, Antonenko D, Flöel A, Siebner HR, Classen J, et al. Beneficial effects of cerebellar tDCS on motor learning are associated with altered putamen-cerebellar connectivity: A simultaneous tDCS-fMRI study. Neuroimage. 2020;223:117363.

  54. Ito M. Cerebellar circuitry as a neuronal machine. Prog Neurobiol. 2006;78(3–5):272–303.

    Article  PubMed  Google Scholar 

  55. D’Mello AM, Turkeltaub PE, Stoodley CJ. Cerebellar tdcs modulates neural circuits during semantic prediction: A combined tDCS-fMRI study. J Neurosci. 2017;37(6):1604–13.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Turkeltaub PE, Swears MK, D’Mello AM, Stoodley CJ. Cerebellar tDCS as a novel treatment for aphasia? Evidence from behavioral and resting-state functional connectivity data in healthy adults. Restor Neurol Neurosci. 2016;34(4):491–505.

    PubMed  PubMed Central  Google Scholar 

  57. Jalali R, Miall RC, Galea JM. No consistent effect of cerebellar transcranial direct current stimulation on visuomotor adaptation. J Neurophysiol. 2017;118(2):655–65.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Rezaee Z, Ruszala B, Dutta A. A computational pipeline to find lobule-specific electric field distribution during non-invasive cerebellar stimulation. In: IEEE International Conference on Rehabilitation Robotics. IEEE Computer Society; 2019. p. 1191–6.

  59. Gomez-Tames J, Asai A, Mikkonen M, Laakso I, Tanaka S, Uehara S, et al. Group-level and functional-region analysis of electric-field shape during cerebellar transcranial direct current stimulation with different electrode montages. J Neural Eng. 2019;16(3).

  60. Baillieux H, Vandervliet EJM, Manto M, Parizel PM, Deyn PPD, Mariën P. Developmental dyslexia and widespread activation across the cerebellar hemispheres. Brain Lang. 2009;108(2):122–32.

    Article  PubMed  Google Scholar 

  61. Walther S, Stegmayer K, Federspiel A, Bohlhalter S, Wiest R, Viher PV. Aberrant hyperconnectivity in the motor system at rest is linked to motor abnormalities in schizophrenia spectrum disorders. Schizophr Bull. 2017;43(5):982–92.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Grimaldi G, Taib NO Ben, 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(JAN).

  63. 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(MAR):71.

  64. Mitoma H, Buffo A, Gelfo F, Guell X, Fucà E, Kakei S, et al. Consensus Paper. Cerebellar Reserve: From Cerebellar Physiology to Cerebellar Disorders. Cerebellum. 2020;19(1):131–53.

  65. Miyaguchi S, Otsuru N, Kojima S, Saito K, Inukai Y, Masaki M, et al. Transcranial alternating current stimulation with gamma oscillations over the primary motor cortex and cerebellar hemisphere improved visuomotor performance. Front Behav Neurosci. 2018;5:12.

    Google Scholar 

  66. Miyaguchi S, Otsuru N, Kojima S, Yokota H, Saito K, Inukai Y, et al. The effect of gamma tACS over the M1 region and cerebellar hemisphere does not depend on current intensity. J Clin Neurosci. 2019;1(65):54–8.

    Article  Google Scholar 

  67. Singh A, Trapp NT, De Corte B, Cao S, Kingyon J, Boes AD, et al. Cerebellar Theta Frequency Transcranial Pulsed Stimulation Increases Frontal Theta Oscillations in Patients with Schizophrenia. Cerebellum. 2019;18(3):489–99.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Naro A, Russo M, Leo A, Cannavò A, Manuli A, Bramanti A, et al. Cortical connectivity modulation induced by cerebellar oscillatory transcranial direct current stimulation in patients with chronic disorders of consciousness: A marker of covert cognition? Clin Neurophysiol. 2016;127(3):1845–54.

    Article  PubMed  Google Scholar 

  69. Miterko LN, Baker KB, Beckinghausen J, Bradnam L V., Cheng MY, Cooperrider J, et al. Consensus Paper: Experimental Neurostimulation of the Cerebellum. Cerebellum 2019 186. 2019 Jun 4;18(6):1064–97.

  70. Di Nuzzo C, Ruggiero F, Cortese F, Cova I, Priori A, Ferrucci R. Non-invasive Cerebellar Stimulation in Cerebellar Disorders. CNS Neurol Disord - Drug Targets. 2018;17(3):193–8.

    Article  PubMed  Google Scholar 

  71. Mr D. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990;13(7):281–5.

    Article  Google Scholar 

  72. Bostan AC, Dum RP, Strick PL. Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci. 2013;17(5):241–54.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Asan AS, Sahin M. Modulation of Multiunit Spike Activity by Transcranial AC Stimulation (tACS) in the Rat Cerebellar Cortex. In: Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, EMBS. Institute of Electrical and Electronics Engineers Inc.; 2019. p. 5192–5.

  74. Chan CY, Nicholson C. Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol. 1986;371(1):89–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Morellini N, Grehl S, Tang A, Rodger J, Mariani J, Lohof AM, et al. What Does Low-Intensity rTMS Do to the Cerebellum? Vol. 14, Cerebellum. Springer New York LLC; 2015. p. 23–6.

  76. Taib NO Ben, Manto M. Trains of transcranial direct current stimulation antagonize motor cortex hypoexcitability induced by acute hemicerebellectomy: Laboratory investigation. J Neurosurg. 2009;111(4):796–806.

  77. Manto MU, Hampe CS, Rogemond V, Honnorat J. Respective implications of glutamate decarboxylase antibodies in stiff person syndrome and cerebellar ataxia. Orphanet J Rare Dis. 2011;6(1).

  78. Asan AS, Lang EJ, Sahin M. Entrainment of cerebellar purkinje cells with directional AC electric fields in anesthetized rats. Brain Stimul. 2020;13(6):1548–58.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Parker KL, Kim YC, Kelley RM, Nessler AJ, Chen K-H, Muller-Ewald VA, et al. Delta-frequency stimulation of cerebellar projections can compensate for schizophrenia-related medial frontal dysfunction. Mol Psychiatry 2017 225. 2017;22(5):647–55.

  80. Das S, Spoor M, Sibindi TM, Holland P, Schonewille M, De Zeeuw CI, et al. Impairment of long-term plasticity of cerebellar purkinje cells eliminates the effect of anodal direct current stimulation on vestibulo-ocular reflex habituation. Front Neurosci. 2017;11(AUG).

  81. de Solages C, Szapiro G, Brunel N, Hakim V, Isope P, Buisseret P, et al. High-Frequency Organization and Synchrony of Activity in the Purkinje Cell Layer of the Cerebellum. Neuron. 2008;58(5):775–88.

    Article  PubMed  Google Scholar 

  82. Ostojic S, Szapiro G, Schwartz E, Barbour B, Brunel N, Hakim V. Neuronal Morphology Generates High-Frequency Firing Resonance. J Neurosci. 2015;35(18):7056–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ferrucci R, Bocci T, Cortese F, Ruggiero F, Priori A. Noninvasive Cerebellar Stimulation as a Complement Tool to Pharmacotherapy. Curr Neuropharmacol. 2018;17(1):14–20.

    Article  Google Scholar 

  84. 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(12):E1090–101.

    Article  PubMed  Google Scholar 

  85. Spampinato D, Celnik P. Multiple Motor Learning Processes in Humans: Defining Their Neurophysiological Bases. Neurosci. 2020;25:107385842093955.

    Google Scholar 

  86. Smith MA, Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol. 2005;93(5):2809–21.

    Article  PubMed  Google Scholar 

  87. Streng ML, Popa LS, Ebner TJ. Modulation of sensory prediction error in Purkinje cells during visual feedback manipulations. Nat Commun. 2018;9(1):1–12.

    Article  CAS  Google Scholar 

  88. Medina JF, Lisberger SG. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci. 2008;11(10):1185–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Herzfeld DJ, Pastor D, Haith AM, Rossetti Y, Shadmehr R, O’Shea J. Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. Neuroimage. 2014;98:147–58.

    Article  PubMed  Google Scholar 

  90. Jayaram G, Tang B, Pallegadda R, Vasudevan EVL, Celnik P, Bastian A. Modulating locomotor adaptation with cerebellar stimulation. J Neurophysiol. 2012;107(11):2950–7.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Block H, Celnik P. Stimulating the cerebellum affects visuomotor adaptation but not intermanual transfer of learning. Cerebellum. 2013;12(6):781–93.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Bonnì S, Motta C, Pellicciari MC, Casula EP, Cinnera AM, Maiella M, et al. Intermittent Cerebellar Theta Burst Stimulation Improves Visuo-motor Learning in Stroke Patients: a Pilot Study. Cerebellum 2020 195. 2020;19(5):739–43.

  93. Cantarero G, Spampinato D, Reis J, Ajagbe L, Thompson T, Kulkarni K, et al. Cerebellar direct current stimulation enhances on-line motor skill acquisition through an effect on accuracy. J Neurosci. 2015;35(7):3285–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Torriero S, Oliveri M, Koch G, Caltagirone C, Petrosini L. Interference of left and right cerebellar rTMS with procedural learning. J Cogn Neurosci. 2004;16(9):1605–11.

    Article  PubMed  Google Scholar 

  95. Ehsani F, Bakhtiary AH, Jaberzadeh S, Talimkhani A, Hajihasani A. Differential effects of primary motor cortex and cerebellar transcranial direct current stimulation on motor learning in healthy individuals: A randomized double-blind sham-controlled study. Neurosci Res. 2016;1(112):10–9.

    Article  Google Scholar 

  96. 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(4):485–92.

    Article  CAS  PubMed  Google Scholar 

  97. Koch G, Bonnì S, Casula EP, Iosa M, Paolucci S, Pellicciari MC, et al. Effect of Cerebellar Stimulation on Gait and Balance Recovery in Patients with Hemiparetic Stroke: A Randomized Clinical Trial. JAMA Neurol. 2019;76(2):170–8.

    Article  PubMed  Google Scholar 

  98. Sebastian R, Saxena S, Tsapkini K, Faria AV, Long C, Wright A, et al. Cerebellar tDCS: A novel approach to augment language treatment post-stroke. Front Hum Neurosci. 2017;12(10):695.

    Google Scholar 

  99. 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):1701–5.

    Article  PubMed  Google Scholar 

  100. Feigin VL, Nichols E, Alam T, Bannick MS, Beghi E, Blake N, et al. Global, regional, and national burden of neurological disorders, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019;18(5):459–80.

    Article  Google Scholar 

  101. Baron JC, Bousser MG, Comar D, Castaigne P. “Crossed cerebellar diaschisis” in human supratentorial brain infarction. Trans Am Neurol Assoc. 1981;105:459–61.

    CAS  PubMed  Google Scholar 

  102. Kikuchi S, Mochizuki H, Moriya A, Nakatani-Enomoto S, Nakamura K, Hanajima R, et al. Ataxic hemiparesis: Neurophysiological analysis by cerebellar transcranial magnetic stimulation. Cerebellum. 2012;11(1):259–63.

    Article  PubMed  Google Scholar 

  103. Celnik P. Understanding and Modulating Motor Learning with Cerebellar Stimulation. Vol. 14, Cerebellum. Springer New York LLC; 2015. p. 171–4.

  104. Wessel MJ, Hummel FC. Non-invasive Cerebellar Stimulation: a Promising Approach for Stroke Recovery? Vol. 17, Cerebellum. Springer New York LLC; 2018. p. 359–71.

  105. Marangolo P, Fiori V, Caltagirone C, Pisano F, Priori A. Transcranial cerebellar direct current stimulation enhances verb generation but not verb naming in poststroke Aphasia. J Cogn Neurosci. 2018;30(2):188–99.

    Article  PubMed  Google Scholar 

  106. Zandvliet SB, Meskers CGM, Kwakkel G, van Wegen EEH. Short-Term Effects of Cerebellar tDCS on Standing Balance Performance in Patients with Chronic Stroke and Healthy Age-Matched Elderly. Cerebellum. 2018;17(5):575–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Picelli A, Chemello E, Castellazzi P, Filippetti M, Brugnera A, Gandolfi M, et al. Combined effects of cerebellar transcranial direct current stimulation and transcutaneous spinal direct current stimulation on robot-assisted gait training in patients with chronic brain stroke: A pilot, single blind, randomized controlled trial. Restor Neurol Neurosci. 2018;36(2):161–71.

    PubMed  Google Scholar 

  108. Picelli A, Brugnera A, Filippetti M, Mattiuz N, Chemello E, Modenese A, et al. Effects of two different protocols of cerebellar transcranial direct current stimulation combined with transcutaneous spinal direct current stimulation on robot-assisted gait training in patients with chronic supratentorial stroke: A single blind, randomized controlled trial. Restor Neurol Neurosci. 2019;37(2):97–107.

    PubMed  Google Scholar 

  109. Sebastian R, Kim JH, Brenowitz R, Tippett DC, Desmond JE, Celnik PA, et al. Cerebellar neuromodulation improves naming in post-stroke aphasia. Brain Commun. 2020.

  110. Bonnì S, Ponzo V, Caltagirone C, Koch G. Cerebellar theta burst stimulation in stroke patients with ataxia. Funct Neurol. 2014;29(1):41–5.

    PubMed  PubMed Central  Google Scholar 

  111. Kim WS, Jung SH, Oh MK, Min YS, Lim JY, Paik NJ. 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):418–23.

    Article  PubMed  Google Scholar 

  112. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: Validation of an instrument. In: Canadian Journal of Public Health. 1992. p. S7–11.

  113. Enright PL. The Six-Minute Walk Test. Respir Care. 2003;48(8).

  114. Wessel MJ, Zimerman M, Timmermann JE, Heise KF, Gerloff C, Hummel FC. Enhancing Consolidation of a New Temporal Motor Skill by Cerebellar Noninvasive Stimulation. Cereb Cortex. 2016;26(4):1660–7.

    Article  PubMed  Google Scholar 

  115. Leggio M, Olivito G, Lupo M, Clausi S. The Cerebellum: A Therapeutic Target in Treating Speech and Language Disorders. In: Translational Neuroscience of Speech and Language Disorders. Springer International Publishing; 2020. p. 141–75.

  116. Desmond JE, Chen SHA, Shieh PB. Cerebellar transcranial magnetic stimulation impairs verbal working memory. Ann Neurol. 2005;58(4):553–60.

    Article  PubMed  Google Scholar 

  117. Tomlinson SP, Davis NJ, Morgan HM, Bracewell RM. Cerebellar contributions to verbal working memory. Cerebellum. 2014;13(3):354–61.

    Article  PubMed  Google Scholar 

  118. 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(9):1687–97.

    Article  CAS  PubMed  Google Scholar 

  119. Boehringer A, Macher K, Dukart J, Villringer A, Pleger B. Cerebellar transcranial direct current stimulation modulates verbal working memory. Brain Stimul. 2013;6(4):649–53.

    Article  PubMed  Google Scholar 

  120. Macher K, Böhringer A, Villringer A, Pleger B. P 50. Anodal cerebellar tDCS impairs verbal working memory. Clin Neurophysiol. 2013;124(10):e87–8.

  121. Pope PA, Miall RC. Task-specific facilitation of cognition by cathodal transcranial direct current stimulation of the cerebellum. Brain Stimul. 2012;5(2):84–94.

    Article  PubMed  PubMed Central  Google Scholar 

  122. Gronwall DMA. Paced auditory serial addition task: A measure of recovery from concussion. Percept Mot Skills. 1977;44(2):367–73.

    Article  CAS  PubMed  Google Scholar 

  123. Arasanz CP, Staines WR, Roy EA, Schweizer TA. The cerebellum and its role in word generation: A cTBS study. Cortex. 2012;48(6):718–24.

    Article  PubMed  Google Scholar 

  124. Rami L, Gironell A, Kulisevsky J, García-Sánchez C, Berthier M, Estévez-González A. Effects of repetitive transcranial magnetic stimulation on memory subtypes: A controlled study. Neuropsychologia. 2003;41(14):1877–83.

    Article  CAS  PubMed  Google Scholar 

  125. Argyropoulos GPD. The cerebellum, internal models and prediction in ‘non-motor’ aspects of language: A critical review. Brain Lang. 2016;1(161):4–17.

    Article  Google Scholar 

  126. Argyropoulos GP. Cerebellar theta-burst stimulation selectively enhances lexical associative priming. Cerebellum. 2011;10(3):540–50.

    Article  PubMed  Google Scholar 

  127. Argyropoulos GP, Muggleton NG. Effects of cerebellar stimulation on processing semantic associations. Cerebellum. 2013;12(1):83–96.

    Article  PubMed  Google Scholar 

  128. Allen-Walker LST, Bracewell RM, Thierry G, Mari-Beffa P. Facilitation of Fast Backward Priming After Left Cerebellar Continuous Theta-Burst Stimulation. Cerebellum. 2018;17(2):132–42.

    Article  PubMed  Google Scholar 

  129. Lesage E, Morgan BE, Olson AC, Meyer AS, Miall RC. Cerebellar rTMS disrupts predictive language processing, vol. 22. Current Biology: Cell Press; 2012.

    Google Scholar 

  130. Miall RC, Antony J, Goldsmith-Sumner A, Harding SR, McGovern C, Winter JL. Modulation of linguistic prediction by TDCS of the right lateral cerebellum. Neuropsychologia. 2016;1(86):103–9.

    Article  Google Scholar 

  131. Gatti D, Van Vugt F, Vecchi T. A causal role for the cerebellum in semantic integration: a transcranial magnetic stimulation study. Sci Reports 2020 101. 2020;10(1):1–12.

  132. Dave S, VanHaerents S, Voss JL. Cerebellar Theta and Beta Noninvasive Stimulation Rhythms Differentially Influence Episodic Memory versus Semantic Prediction. J Neurosci. 2020;40(38):7300–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Oliveri M, Bonnì S, Turriziani P, Koch G, Lo Gerfo E, Torriero S, et al. Motor and linguistic linking of space and time in the cerebellum. PLoS One. 2009;4(11).

  134. Runnqvist E, Bonnard M, Gauvin HS, Attarian S, Trébuchon A, Hartsuiker RJ, et al. Internal modeling of upcoming speech: A causal role of the right posterior cerebellum in non-motor aspects of language production. Cortex. 2016;1(81):203–14.

    Article  Google Scholar 

  135. Cho SS, Yoon EJ, Bang SA, Park HS, Kim YK, Strafella AP, et al. Metabolic changes of cerebrum by repetitive transcranial magnetic stimulation over lateral cerebellum: A study with FDG PET. Cerebellum. 2012;11(3):739–48.

    Article  PubMed  Google Scholar 

  136. Macher K, Böhringer A, Villringer A, Pleger B. Cerebellar-parietal connections underpin phonological storage. J Neurosci. 2014;34(14):5029–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Farzan F, Wu Y, Manor B, Anastasio EM, Lough M, Novak V, et al. Cerebellar TMS in treatment of a patient with cerebellar ataxia: Evidence from clinical, biomechanics and neurophysiological assessments. Cerebellum. 2013;12(5):707–12.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Lin Q, Chang Y, Liu P, Jones JA, Chen X, Peng D, et al. Cerebellar Continuous Theta Burst Stimulation Facilitates Auditory–Vocal Integration in Spinocerebellar Ataxia. Cereb Cortex. 2021.

  139. Brusa L, Ponzo V, Mastropasqua C, Picazio S, Bonnì S, Di Lorenzo F, et al. Theta burst stimulation modulates Cerebellar-cortical connectivity in patients with progressive supranuclear palsy. Brain Stimul. 2014;7(1):29–35.

    Article  PubMed  Google Scholar 

  140. DeMarco AT, Dvorak E, Lacey E, Stoodley CJ, Turkeltaub PE. An Exploratory Study of Cerebellar Transcranial Direct Current Stimulation in Individuals With Chronic Stroke Aphasia. Cogn Behav Neurol. 2021;34(2):96–106.

    Article  PubMed  PubMed Central  Google Scholar 

  141. Phillips JR, Hewedi DH, Eissa AM, Moustafa AA. The Cerebellum and Psychiatric Disorders. Front Public Heal. 2015;5(3):66.

    Google Scholar 

  142. Ferrucci R, Bocci T, Priori A. Cerebellar and spinal tDCS. In: Transcranial Direct Current Stimulation in Neuropsychiatric Disorders: Clinical Principles and Management. Springer International Publishing; 2016. p. 223–9.

  143. O’Connell NE, Wand BM, Marston L, Spencer S, DeSouza LH. Non-invasive brain stimulation techniques for chronic pain. In: Cochrane Database of Systematic Reviews. John Wiley & Sons, Ltd; 2010.

  144. Tortella G. Transcranial direct current stimulation in psychiatric disorders. World J Psychiatry. 2015;5(1):88.

    Article  PubMed  PubMed Central  Google Scholar 

  145. Kuo MF, Nitsche MA. Exploring prefrontal cortex functions in healthy humans by transcranial electrical stimulation. Vol. 31, Neuroscience Bulletin. Science Press; 2015. p. 198–206.

  146. Ho KA, Bai S, Martin D, Alonzo A, Dokos S, Puras P, et al. A pilot study of alternative transcranial direct current stimulation electrode montages for the treatment of major depression. J Affect Disord. 2014;1(167):251–8.

    Article  Google Scholar 

  147. Minichino A, Bersani FS, Spagnoli F, Corrado A, De Michele F, Calò WK, et al. Prefronto-cerebellar transcranial direct current stimulation improves sleep quality in euthymic bipolar patients: A brief report. Behav Neurol. 2014;4:2014.

    Google Scholar 

  148. Curcio G, Tempesta D, Scarlata S, Marzano C, Moroni F, Rossini PM, et al. Validity of the Italian Version of the Pittsburgh Sleep Quality Index (PSQI). Neurol Sci. 2013;34(4):511–9.

    Article  PubMed  Google Scholar 

  149. Minichino A, Bersani FS, Bernabei L, Spagnoli F, Vergnani L, Corrado A, et al. Prefronto–cerebellar transcranial direct current stimulation improves visuospatial memory, executive functions, and neurological soft signs in patients with euthymic bipolar disorder. Neuropsychiatr Dis Treat. 2015;28(11):2265–70.

    Google Scholar 

  150. Shin MS, Park SY, Park SR, Seol SH, Kwon JS. Clinical and empirical applications of the Rey-Osterrieth Complex Figure Test. Nat Protoc. 2006;1(2):892–9.

    Article  PubMed  Google Scholar 

  151. Bation R, Poulet E, Haesebaert F, Saoud M, Brunelin J. Transcranial direct current stimulation in treatment-resistant obsessive-compulsive disorder: An open-label pilot study. Prog Neuro-Psychopharmacology Biol Psychiatry. 2016;4(65):153–7.

    Article  Google Scholar 

  152. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134(4):382–9.

    Article  CAS  PubMed  Google Scholar 

  153. Goodman WK, Price LH, Rasmussen SA, Mazure C, Delgado P, Heninger GR, et al. The Yale-Brown Obsessive Compulsive Scale: II. Validity Arch Gen Psychiatry. 1989;46(11):1012–6.

    Article  CAS  PubMed  Google Scholar 

  154. Jayadev S, Bird TD. Hereditary ataxias: Overview. Vol. 15, Genetics in Medicine. Genet Med; 2013. p. 673–83.

  155. Storey E. Genetic cerebellar ataxias. Semin Neurol. 2014;34(3):280–92.

    Article  PubMed  Google Scholar 

  156. Rüb U, Schöls L, Paulson H, Auburger G, Kermer P, Jen JC, et al. Clinical features, neurogenetics and neuropathology of the polyglutamine spinocerebellar ataxias type 1, 2, 3, 6 and 7. Vol. 104, Progress in Neurobiology. Prog Neurobiol; 2013. p. 38–66.

  157. Delatycki MB, Corben LA. Clinical features of Friedreich ataxia. In: Journal of Child Neurology. NIH Public Access; 2012. p. 1133–7.

  158. Pozzi NG, Minafra B, Zangaglia R, De Marzi R, Sandrini G, Priori A, et al. Transcranial direct current stimulation (tDCS) of the cortical motor areas in three cases of cerebellar ataxia. Cerebellum. 2014;13(1):109–12.

    Article  PubMed  Google Scholar 

  159. 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):2437–47.

    Article  PubMed  Google Scholar 

  160. Barretto TL, Bandeira ID, Jagersbacher JG, Barretto BL, de Oliveira e Torres ÂFS, Peña N, et al. Transcranial direct current stimulation in the treatment of cerebellar ataxia: A two-phase, double-blind, auto-matched, pilot study. Clin Neurol Neurosurg. 2019;182:123–9.

  161. Chen TX, Yang CY, Willson G, Lin CC, Kuo SH. The Efficacy and Safety of Transcranial Direct Current Stimulation for Cerebellar Ataxia: a Systematic Review and Meta-Analysis. Cerebellum. Springer; 2020. p. 1–10.

  162. Benussi A, Pascual-Leone A, Borroni B. Non-invasive cerebellar stimulation in neurodegenerative ataxia: A literature review. Vol. 21, International Journal of Molecular Sciences. MDPI AG; 2020.

  163. Orrù G, Cesari V, Conversano C, Gemignani A. The clinical application of transcranial direct current stimulation in patients with cerebellar ataxia: a systematic review. International Journal of Neuroscience. Taylor and Francis Ltd; 2020.

  164. Maas RPPWM, Helmich RCG, van de Warrenburg BPC. The role of the cerebellum in degenerative ataxias and essential tremor: Insights from noninvasive modulation of cerebellar activity. Vol. 35, Movement Disorders. John Wiley and Sons Inc.; 2020. p. 215–27.

  165. Mathiowetz V, Weber K, Kashman N, Volland G. Adult Norms for the Nine Hole Peg Test of Finger Dexterity. Occup Ther J Res. 1985;5(1):24–38.

    Article  Google Scholar 

  166. Hulst T, John L, Küper M, Van Der Geest JN, Göricke SL, Donchin O, et al. Cerebellar patients do not benefit from cerebellar or M1 transcranial direct current stimulation during force-field reaching adaptation. J Neurophysiol. 2017;118(2):732–48.

    Article  PubMed  PubMed Central  Google Scholar 

  167. John L, Küper M, Hulst T, Timmann D, Hermsdörfer J. Effects of transcranial direct current stimulation on grip force control in patients with cerebellar degeneration. Cerebellum and Ataxias. 2017;4(1).

  168. Lefaucheur JP, Antal A, Ayache SS, Benninger DH, Brunelin J, Cogiamanian F, et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS). Vol. 128, Clinical Neurophysiology. Elsevier Ireland Ltd; 2017. p. 56–92.

  169. Portaro S, Russo M, Bramanti A, Leo A, Billeri L, Manuli A, et al. The role of robotic gait training and tDCS in Friedrich ataxia rehabilitation: A case report. Medicine (Baltimore). 2019;98(8):e14447.

  170. Tada M, Nishizawa M, Onodera O. Redefining cerebellar ataxia in degenerative ataxias: Lessons from recent research on cerebellar systems. Vol. 86, Journal of Neurology, Neurosurgery and Psychiatry. BMJ Publishing Group; 2015. p. 922–8.

  171. Ferrucci R, Bocci T, Cortese F, Ruggiero F, Priori A. Cerebellar transcranial direct current stimulation in neurological disease. Vol. 3, Cerebellum and Ataxias. BioMed Central Ltd.; 2016.

  172. Pilloni G, Shaw M, Feinberg C, Clayton A, Palmeri M, Datta A, et al. Long term at-home treatment with transcranial direct current stimulation (tDCS) improves symptoms of cerebellar ataxia: a case report. J Neuroeng Rehabil. 2019;16(1):41.

    Article  PubMed  PubMed Central  Google Scholar 

  173. Marinela V, Gabriella P, Vasco M, Jimmy C, Jennifer P, Andrea M. Acta Scientific Neurology Combining Transcranial Direct Current Stimulation and Intensive Physiotherapy in Patients with Friedreich’s Ataxia: A Pilot Study.

  174. Albanese A, Bhatia K, Bressman SB, Delong MR, Fahn S, Fung VSC, et al. Phenomenology and classification of dystonia: A consensus update. Vol. 28, Movement Disorders. Mov Disord; 2013. p. 863–73.

  175. Jinnah HA, Neychev V, Hess EJ. The Anatomical Basis for Dystonia: The Motor Network Model. Vol. 7, Tremor and other hyperkinetic movements (New York, N.Y.). Ubiquity Press; 2017. p. 506.

  176. Odorfer TM, Homola GA, Reich MM, Volkmann J, Zeller D. Increased Finger-Tapping Related Cerebellar Activation in Cervical Dystonia, Enhanced by Transcranial Stimulation: An Indicator of Compensation? Front Neurol. 2019;15(10):231.

    Article  Google Scholar 

  177. Popa T, Hubsch C, James P, Richard A, Russo M, Pradeep S, et al. Abnormal cerebellar processing of the neck proprioceptive information drives dysfunctions in cervical dystonia. Sci Rep. 2018;8(1).

  178. Bradnam L V., McDonnell MN, Ridding MC. Cerebellar intermittent theta-burst stimulation and motor control training in individuals with cervical dystonia. Brain Sci. 2016;6(4).

  179. Bradnam L V., Frasca J, Kimberley TJ. Direct current stimulation of primary motor cortex and cerebellum and botulinum toxin a injections in a person with cervical dystonia. Vol. 7, Brain Stimulation. Elsevier Inc.; 2014. p. 909–11.

  180. Koch G, Porcacchia P, Ponzo V, Carrillo F, Cáceres-Redondo MT, Brusa L, et al. Effects of two weeks of cerebellar theta burst stimulation in cervical dystonia patients. Brain Stimul. 2014;7(4):564–72.

    Article  PubMed  Google Scholar 

  181. Hoffland BS, Kassavetis P, Bologna M, Teo JTH, Bhatia KP, Rothwell JC, et al. Cerebellum-dependent associative learning deficits in primary dystonia are normalized by rTMS and practice. Eur J Neurosci. 2013;38(1):2166–71.

    Article  CAS  PubMed  Google Scholar 

  182. Bradnam L V., 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;9(MAY).

  183. Linssen MW, Van Gaalen J, Munneke MAM, Hoffland BS, Hulstijn W, Van De Warrenburg BPC. A single session of cerebellar theta burst stimulation does not alter writing performance in writer’s cramp. Vol. 138, Brain. Oxford University Press; 2015. p. e355.

  184. Sadnicka A, Hamada M, Bhatia KP, Rothwell JC, Edwards MJ. Cerebellar stimulation fails to modulate motor cortex plasticity in writing dystonia. Mov Disord. 2014;29(10):1304–7.

    Article  PubMed  Google Scholar 

  185. Hubsch C, Roze E, Popa T, Russo M, Balachandran A, Pradeep S, et al. Defective cerebellar control of cortical plasticity in writer’s cramp. Brain. 2013;136(7):2050–62.

    Article  PubMed  PubMed Central  Google Scholar 

  186. Bologna M, Paparella G, Fabbrini A, Leodori G, Rocchi L, Hallett M, et al. Effects of cerebellar theta-burst stimulation on arm and neck movement kinematics in patients with focal dystonia. Clin Neurophysiol. 2016;127(11):3472–9.

    Article  PubMed  PubMed Central  Google Scholar 

  187. Shin HW, Youn YC, Hallett M. Focal Leg Dystonia Associated with Cerebellar Infarction and Application of Low-Frequency Cerebellar Transcranial Magnetic Stimulation: Evidence of Topographically Specific Cerebellar Contribution to Dystonia Development. Cerebellum. 2019;18(6):1147–50.

    Article  CAS  PubMed  Google Scholar 

  188. Sadnicka A, Rosset-Llobet J. A motor control model of task-specific dystonia and its rehabilitation. In: Progress in Brain Research. Elsevier B.V.; 2019. p. 269–83.

  189. Furuya S, Nitsche MA, Paulus W, Altenmüller E. Surmounting retraining limits in Musicians’ dystonia by transcranial stimulation. Ann Neurol. 2014;75(5):700–7.

    Article  PubMed  Google Scholar 

  190. Ferrucci R, Priori A. Noninvasive stimulation. In: Handbook of Clinical Neurology. Elsevier B.V.; 2018. p. 393–405.

  191. Sadnicka A, Hamada M. Plasticity and dystonia: a hypothesis shrouded in variability. Exp Brain Res. 2020;238(7–8):1611–7.

    Article  PubMed  PubMed Central  Google Scholar 

  192. Brighina F, Romano M, Giglia G, Saia V, Puma A, Giglia F, et al. Effects of cerebellar TMS on motor cortex of patients with focal dystonia: A preliminary report. Exp Brain Res. 2009;192(4):651–6.

    Article  CAS  PubMed  Google Scholar 

  193. Giompres P, Delis F. Dopamine transporters in the cerebellum of mutant mice. Cerebellum. 2005;4(2):105–11.

    Article  CAS  PubMed  Google Scholar 

  194. Kishore A, Popa T. Cerebellum in levodopa-induced dyskinesias: The unusual suspect in the motor network. Vol. 5 AUG, Frontiers in Neurology. Frontiers Research Foundation; 2014.

  195. Panagopoulos NT, Papadopoulos GC, Matsokis NA. Dopaminergic innervation and binding in the rat cerebellum. Neurosci Lett. 1991;130(2):208–12.

    Article  CAS  PubMed  Google Scholar 

  196. Melchitzky DS, Lewis DA. Tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in the primate cerebellum: Evidence for a lobular- and laminar-specific dopamine innervation. Neuropsychopharmacology. 2000;22(5):466–72.

    Article  CAS  PubMed  Google Scholar 

  197. Tremblay S, Austin D, Hannah R, Rothwell JC. Non-invasive brain stimulation as a tool to study cerebellar-M1 interactions in humans. Vol. 3, Cerebellum and Ataxias. BioMed Central Ltd.; 2016.

  198. Hallett M. Tremor: Pathophysiology. Park Relat Disord. 2014;20(SUPPL.1).

  199. Málly J, Stone TW, Sinkó G, Geisz N, Dinya E. Long term follow-up study of non-invasive brain stimulation (NBS) (rTMS and tDCS) in Parkinson’s disease (PD). Strong age-dependency in the effect of NBS. Brain Res Bull. 2018;142:78–87.

  200. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov Disord. 2008;23(15):2129–70.

    Article  PubMed  Google Scholar 

  201. Ferrucci R, Cortese F, Bianchi M, Pittera D, Turrone R, Bocci T, et al. Cerebellar and Motor Cortical Transcranial Stimulation Decrease Levodopa-Induced Dyskinesias in Parkinson’s Disease. Cerebellum. 2016;15(1):43–7.

    Article  CAS  PubMed  Google Scholar 

  202. Workman CD, Fietsam AC, Uc EY, Rudroff T. Cerebellar transcranial direct current stimulation in people with parkinson’s disease: A pilot study. Brain Sci. 2020;10(2).

  203. Bologna M, Di Biasio F, Conte A, Iezzi E, Modugno N, Berardelli A. Effects of cerebellar continuous theta burst stimulation on resting tremor in Parkinson’s disease. Park Relat Disord. 2015;21(9):1061–6.

    Article  Google Scholar 

  204. Di Biasio F, Conte A, Bologna M, Iezzi E, Rocchi L, Modugno N, et al. Does the cerebellum intervene in the abnormal somatosensory temporal discrimination in Parkinson’s disease? Park Relat Disord. 2015;21(7):789–92.

    Article  Google Scholar 

  205. Sanna A, Follesa P, Puligheddu M, Cannas A, Serra M, Pisu MG, et al. Cerebellar continuous theta burst stimulation reduces levodopa-induced dyskinesias and decreases serum BDNF levels. Neurosci Lett. 2020;716:134653.

  206. Janssen AM, Munneke MAM, Nonnekes J, van der Kraan T, Nieuwboer A, Toni I, et al. Cerebellar theta burst stimulation does not improve freezing of gait in patients with Parkinson’s disease. J Neurol. 2017;264(5):963–72.

    Article  PubMed  PubMed Central  Google Scholar 

  207. Brusa L, Ceravolo R, Kiferle L, Monteleone F, Iani C, Schillaci O, et al. Metabolic changes induced by theta burst stimulation of the cerebellum in dyskinetic Parkinson’s disease patients. Park Relat Disord. 2012;18(1):59–62.

    Article  Google Scholar 

  208. Kishore A, Popa T, Balachandran A, Chandran S, Pradeep S, Backer F, et al. Cerebellar sensory processing alterations impact motor cortical plasticity in Parkinson’s disease: Clues from dyskinetic patients. Cereb Cortex. 2014;24(8):2055–67.

    Article  PubMed  Google Scholar 

  209. Popa T, Russo M, Meunier S. Long-lasting inhibition of cerebellar output. Brain Stimul. 2010;3(3):161–9.

    Article  CAS  PubMed  Google Scholar 

  210. Aizenman CD, Manis PB, Linden DJ. Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron. 1998;21(4):827–35.

    Article  CAS  PubMed  Google Scholar 

  211. Minks E, Mareček R, Pavlík T, Ovesná P, Bareš M. Is the cerebellum a potential target for stimulation in parkinson’s disease? Results of 1-Hz rTMS on upper limb motor tasks. Cerebellum. 2011;10(4):804–11.

    Article  PubMed  Google Scholar 

  212. Lefaivre SC, Brown MJN, Almeida QJ. Cerebellar involvement in Parkinson’s disease resting tremor. Cerebellum & Ataxias. 2016;3(1):13.

    Article  Google Scholar 

  213. Farina M, Novelli E, Pagani R. Cross-sectional area variations of internal jugular veins during supine head rotation in multiple sclerosis patients with chronic cerebrospinal venous insufficiency: A prospective diagnostic controlled study with duplex ultrasound investigation. BMC Neurol. 2013;5:13.

    Google Scholar 

  214. Bagepally BS, Bhatt MD, Chandran V, Saini J, Bharath RD, Vasudev MK, et al. Decrease in cerebral and cerebellar gray matter in essential tremor: A voxel-based morphometric analysis under 3T MRI. J Neuroimaging. 2012;22(3):275–8.

    Article  PubMed  Google Scholar 

  215. Gironell A, Martínez-Horta S, Aguilar S, Torres V, Pagonabarraga J, Pascual-Sedano B, et al. Transcranial direct current stimulation of the cerebellum in essential tremor: A controlled study. Vol. 7, Brain Stimulation. Elsevier Inc.; 2014. p. 491–2.

  216. Yilmaz NH, Polat B, Hanoglu L. Transcranial direct current stimulation in the treatment of essential tremor: An open-label study. Neurologist. 2016;21(2):28–9.

    Article  Google Scholar 

  217. Elble RJ. The Essential Tremor Rating Assessment Scale. Vol. 1, J Neurol Neuromedicine. 2016.

  218. Schreglmann S, Wang D, Peach R, Li J, Zhang X, Latorre A, et al. Non-invasive Amelioration of Essential Tremor via Phase-Locked Disruption of its Temporal Coherence. bioRxiv. 2020;2020.06.23.165498.

  219. Rees EM, Farmer R, Cole JH, Haider S, Durr A, Landwehrmeyer B, et al. Cerebellar abnormalities in Huntington’s disease: A role in motor and psychiatric impairment? Mov Disord. 2014;29(13):1648–54.

    Article  PubMed  Google Scholar 

  220. Wolf RC, Thomann PA, Sambataro F, Wolf ND, Vasic N, Landwehrmeyer GB, et al. Abnormal cerebellar volume and corticocerebellar dysfunction in early manifest Huntington’s disease. J Neurol. 2015;262(4):859–69.

    Article  CAS  PubMed  Google Scholar 

  221. Bocci T, Baloscio D, Ferrucci R, Sartucci F, Priori A. Cerebellar Direct Current Stimulation (ctDCS) in the Treatment of Huntington’s Disease: A Pilot Study and a Short Review of the Literature. Front Neurol. 2020;3:11.

    Google Scholar 

  222. Tramontano M, Grasso MG, Soldi S, Casula EP, Bonnì S, Mastrogiacomo S, et al. Cerebellar Intermittent Theta-Burst Stimulation Combined with Vestibular Rehabilitation Improves Gait and Balance in Patients with Multiple Sclerosis: a Preliminary Double-Blind Randomized Controlled Trial. Cerebellum 2020 196. 2020;19(6):897–901.

  223. Rampersad S, Roig-Solvas B, Yarossi M, Kulkarni PP, Santarnecchi E, Dorval AD, et al. Prospects for transcranial temporal interference stimulation in humans: A computational study. Neuroimage. 2019;202:116124.

  224. Grossman N, Bono D, Dedic N, Kodandaramaiah SB, Rudenko A, Suk HJ, et al. Noninvasive Deep Brain Stimulation via Temporally Interfering Electric Fields. Cell. 2017;169(6):1029-1041.e16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Chhatbar PY, Kautz SA, Takacs I, Rowland NC, Revuelta GJ, George MS, et al. Evidence of transcranial direct current stimulation-generated electric fields at subthalamic level in human brain in vivo. Brain Stimul. 2018;11(4):727–33.

    Article  PubMed  PubMed Central  Google Scholar 

  226. Michelle Welman FHS, Smit AE, Jongen JLM, Tibboel D, van der Geest JN, Holstege JC. Pain Experience is Somatotopically Organized and Overlaps with Pain Anticipation in the Human Cerebellum. Cerebellum. 2018;17(4):447–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Baarbé JK, Yielder P, Haavik H, Holmes MWR, Murphy BA. Subclinical recurrent neck pain and its treatment impacts motor training-induced plasticity of the cerebellum and motor cortex. PLoS One. 2018;13(2).

  228. Mehnert J, May A. Functional and structural alterations in the migraine cerebellum. J Cereb Blood Flow Metab. 2019;39(4):730–9.

    Article  PubMed  Google Scholar 

  229. Mehnert J, Schulte L, Timmann D, May A. Activity and connectivity of the cerebellum in trigeminal nociception. Neuroimage. 2017;15(150):112–8.

    Article  Google Scholar 

  230. Claassen J, Koenen LR, Ernst TM, Labrenz F, Theysohn N, Forsting M, et al. Cerebellum is more concerned about visceral than somatic pain. Vol. 91, Journal of Neurology, Neurosurgery and Psychiatry. BMJ Publishing Group; 2020. p. 218–9.

  231. Liu HY, Lee PL, Chou KH, Lai KL, Wang YF, Chen SP, et al. The cerebellum is associated with 2-year prognosis in patients with high-frequency migraine. J Headache Pain. 2020;21(1):29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Qin Z, He XW, Zhang J, Xu S, Li GF, Su J, et al. Structural changes of cerebellum and brainstem in migraine without aura. J Headache Pain. 2019;20(1):93.

    Article  PubMed  PubMed Central  Google Scholar 

  233. Coombes SA, Misra G. Pain and motor processing in the human cerebellum. Pain. 2016;157(1):117–27.

    Article  PubMed  Google Scholar 

  234. Fernandez L, Albein-Urios N, Kirkovski M, McGinley JL, Murphy AT, Hyde C, et al. Cathodal Transcranial Direct Current Stimulation (tDCS) to the Right Cerebellar Hemisphere Affects Motor Adaptation During Gait. Cerebellum. 2017;16(1):168–77.

    Article  PubMed  Google Scholar 

  235. Henderson LA, Peck CC, Petersen ET, Rae CD, Youssef AM, Reeves JM, et al. Chronic pain: Lost inhibition? J Neurosci. 2013;33(17):1754–82.

    Article  Google Scholar 

  236. Ruscheweyh R, Kühnel M, Filippopulos F, Blum B, Eggert T, Straube A. Altered experimental pain perception after cerebellar infarction. Pain. 2014;155(7):1303–12.

    Article  PubMed  Google Scholar 

  237. Rueger MA, Keuters MH, Walberer M, Braun R, Klein R, Sparing R, et al. Multi-session transcranial direct current stimulation (tDCS) Elicits inflammatory and regenerative processes in the rat brain. PLoS One. 2012;7(8).

  238. Leffa DT, Bellaver B, Salvi AA, de Oliveira C, Caumo W, Grevet EH, et al. Transcranial direct current stimulation improves long-term memory deficits in an animal model of attention-deficit/hyperactivity disorder and modulates oxidative and inflammatory parameters. Brain Stimul. 2018;11(4):743–51.

    Article  PubMed  Google Scholar 

  239. Bocci T, De Carolis G, Ferrucci R, Paroli M, Mansani F, Priori A, et al. Cerebellar Transcranial Direct Current Stimulation (ctDCS) Ameliorates Phantom Limb Pain and Non-painful Phantom Limb Sensations. Cerebellum. 2019;18(3):527–35.

    Article  PubMed  Google Scholar 

  240. Bocci T, Santarcangelo E, Vannini B, Torzini A, Carli G, Ferrucci R, et al. Cerebellar direct current stimulation modulates pain perception in humans. Restor Neurol Neurosci. 2015;33(5):597–609.

    PubMed  Google Scholar 

  241. Bocci T, Barloscio D, Parenti L, Sartucci F, Carli G, Santarcangelo EL. High Hypnotizability Impairs the Cerebellar Control of Pain. Cerebellum. 2017;16(1):55–61.

    Article  PubMed  Google Scholar 

  242. Valeriani M, Le Pera D, Restuccia D, de Armas L, Miliucci R, Betti V, et al. Parallel spinal pathways generate the middle-latency N1 and the late P2 components of the laser evoked potentials. Clin Neurophysiol. 2007;118(5):1097–104.

    Article  PubMed  Google Scholar 

  243. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for Pain Involves the Affective but not Sensory Components of Pain. Science (80- ). 2004;303(5661):1157–62.

  244. Moriguchi Y, Decety J, Ohnishi T, Maeda M, Mori T, Nemoto K, et al. Empathy and judging other’s pain: An fMRI study of alexithymia. Cereb Cortex. 2007;17(9):2223–34.

    Article  PubMed  Google Scholar 

  245. Pereira M, Rafiq B, Chowdhury E, Babayev J, Boo HJ, Metwaly R, et al. Anodal cerebellar tDCS modulates lower extremity pain perception. NeuroRehabilitation. 2017;40(2):195–200.

    Article  PubMed  Google Scholar 

  246. Zunhammer M, Busch V, Griesbach F, Landgrebe M, Hajak G, Langguth B. RTMS over the cerebellum modulates temperature detection and pain thresholds through peripheral mechanisms. Brain Stimul. 2011;4(4):210-217.e1.

    Article  PubMed  Google Scholar 

  247. Bolognini N, Spandri V, Olgiati E, Fregni F, Ferraro F, Maravita A. Long-term analgesic effects of transcranial direct current stimulation of the motor cortex on phantom limb and stump pain: A case report. Vol. 46, Journal of Pain and Symptom Management. J Pain Symptom Manage; 2013.

  248. Bolognini N, Olgiati E, Maravita A, Ferraro F, Fregni F. Motor and parietal cortex stimulation for phantom limb pain and sensations. Pain. 2013;154(8):1274–80.

    Article  PubMed  Google Scholar 

  249. Bolognini N, Spandri V, Ferraro F, Salmaggi A, Molinari ACL, Fregni F, et al. Immediate and Sustained Effects of 5-Day Transcranial Direct Current Stimulation of the Motor Cortex in Phantom Limb Pain. J Pain. 2015;16(7):657–65.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Service de Neurologie, CHU-Charleroi, 6000, Charleroi, Belgium

    Mario Manto

  2. Service Des Neurosciences, UMons, 7000, Mons, Belgium

    Mario Manto

  3. Division of Psychology, Faculty of Natural Sciences, Faculty of Natural Sciences, University of Stirling, Stirling, FK9 4LA, UK

    Georgios P. D. Argyropoulos

  4. Aldo Ravelli Research Center for Neurotechnology and Experimental Neurotherapeutics, Department of Health Sciences, University of Milan, 20142, Milan, Italy

    Tommaso Bocci, Matteo Guidetti, Alberto Priori & Roberta Ferrucci

  5. ASST Santi Paolo E Carlo, Via di Rudinì, 8, 20142, Milan, Italy

    Tommaso Bocci, Alberto Priori & Roberta Ferrucci

  6. Department of Physical Medicine and Rehabilitation, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Pablo A. Celnik

  7. Bruce Lefroy Centre for Genetic Health Research, Murdoch Children’s Research Institute, Department of Paediatrics, University of Melbourne, Parkville. Victoria, Australia

    Louise A. Corben

  8. Department of Electronics, Information and Bioengineering, Politecnico Di Milano, 20133, Milan, Italy

    Matteo Guidetti

  9. Fondazione Santa Lucia IRCCS, via Ardeatina 306, 00179, Rome, Italy

    Giacomo Koch & Danny Spampinato

  10. Department of Clinical and Movement Neuroscience, UCL Queen Square Institute of Neurology, London, UK

    John C. Rothwell

  11. Motor Control and Movement Disorders Group, St George’s University of London, London, UK

    Anna Sadnicka

  12. Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, London, UK

    Anna Sadnicka

  13. Department of Human Neurophysiology, Fukushima Medical University, Fukushima, Japan

    Yoshikazu Ugawa

  14. Defitech Chair of Clinical Neuroengineering, Center for Neuroprosthetics (CNP) and Brain Mind Institute (BMI), Swiss Federal Institute of Technology (EPFL), Geneva, Switzerland

    Maximilian J. Wessel

  15. Defitech Chair of Clinical Neuroengineering, Center for Neuroprosthetics (CNP) and Brain Mind Institute (BMI), Swiss Federal Institute of Technology (EPFL Valais), Clinique Romande de Réadaptation, Sion, Switzerland

    Maximilian J. Wessel

Authors
  1. Mario Manto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Georgios P. D. Argyropoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tommaso Bocci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo A. Celnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Louise A. Corben
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matteo Guidetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giacomo Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alberto Priori
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. John C. Rothwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Anna Sadnicka
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Danny Spampinato
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yoshikazu Ugawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Maximilian J. Wessel
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Roberta Ferrucci
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Writing: All authors have read and agreed to the publication.

Corresponding author

Correspondence to Roberta Ferrucci.

Ethics declarations

Ethics Approval

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manto, M., Argyropoulos, G.P.D., Bocci, T. et al. Consensus Paper: Novel Directions and Next Steps of Non-invasive Brain Stimulation of the Cerebellum in Health and Disease. Cerebellum 21, 1092–1122 (2022). https://doi.org/10.1007/s12311-021-01344-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-021-01344-6

Keywords

Search

Navigation