Skip to main content
Log in

Efficacy of Cerebellar Transcranial Magnetic Stimulation for Post-stroke Balance and Limb Motor Function Impairments: Meta-analyses of Random Controlled Trials and Resting-State fMRI Studies

  • REVIEW
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

This study aimed to investigate the potential therapeutic effects of cerebellar transcranial magnetic stimulation (TMS) on balance and limb motor impairments in stroke patients. A meta-analysis of randomized controlled trials was conducted to assess the effects of cerebellar TMS on balance and motor impairments in stroke patients. Additionally, an activation likelihood estimation (ALE) meta-analysis was performed on resting-state functional magnetic resonance imaging (fMRI) studies to compare spontaneous neural activity differences between stroke patients and healthy controls using measures including the amplitude of low frequency fluctuation (ALFF), fractional ALFF (fALFF), and regional homogeneity (ReHo). The analysis included 10 cerebellar TMS studies and 18 fMRI studies. Cerebellar TMS treatment demonstrated significant improvements in the Berg Balance Scale score (p < 0.0001) and the Fugl-Meyer Assessment lower extremity score (p < 0.0001) compared to the control group in stroke patients. Additionally, spontaneous neural activity alterations were identified in motor-related regions after stroke, including the precentral gyrus, putamen, thalamus, and paracentral lobule. Cerebellar TMS shows promise as a therapeutic intervention to enhance balance and lower limb motor function in stroke patients. It is easy for clinical application and addresses the limitations of insufficient direct stimulation depth on the leg area of the cortex. However, further research combining neuroimaging outcomes with clinical measurements is necessary to validate these findings.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The data generated in this study are available from the corresponding author via email.

References

  1. Murphy SJ, Werring DJ. Stroke: causes and clinical features. Medicine (Abingdon). 2020;48:561–6. https://doi.org/10.1016/j.mpmed.2020.06.002.

    Article  PubMed  Google Scholar 

  2. Feigin VL, Brainin M, Norrving B, Martins S, Sacco RL, Hacke W, Fisher M, Pandian J, Lindsay P. World Stroke Organization (WSO): global stroke fact sheet 2022. Int J Stroke. 2022;17:18–29. https://doi.org/10.1177/17474930211065917.

    Article  PubMed  Google Scholar 

  3. Mehndiratta MM, Khan M, Mehndiratta P, Wasay M. Stroke in Asia: geographical variations and temporal trends. J Neurol Neurosurg Psychiatry. 2014;85:1308–12. https://doi.org/10.1136/jnnp-2013-306992.

    Article  PubMed  Google Scholar 

  4. Ovadia-Caro S, Khalil AA, Sehm B, Villringer A, Nikulin VV, Nazarova M. Predicting the response to non-invasive brain stimulation in stroke. Front Neurol. 2019;10:302. https://doi.org/10.3389/fneur.2019.00302.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Wang J, Meng H-J, Ji G-J, Jing Y, Wang H-X, Deng X-P, Feng Z-J, Zhao N, Zang Y-F, Zhang J. Finger tapping task activation vs. TMS hotspot: different locations and networks. Brain Topogr. 2020;33:123–34. https://doi.org/10.1007/s10548-019-00741-9.

    Article  PubMed  Google Scholar 

  6. Xu AH, Sun YX. Research hotspots and effectiveness of repetitive transcranial magnetic stimulation in stroke rehabilitation. Neural Regen Res. 2020;15:2089–97. https://doi.org/10.4103/1673-5374.282269.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cash RFH, Cocchi L, Lv J, Fitzgerald PB, Zalesky A. Functional magnetic resonance imaging-guided personalization of transcranial magnetic stimulation treatment for depression. JAMA Psychiatry. 2021;78:337–9. https://doi.org/10.1001/jamapsychiatry.2020.3794.

    Article  PubMed  Google Scholar 

  8. Wessel MJ, Hummel FC. Non-invasive cerebellar stimulation: a promising approach for stroke recovery? Cerebellum. 2018;17:359–71. https://doi.org/10.1007/s12311-017-0906-1.

    Article  PubMed  Google Scholar 

  9. Manto M, Argyropoulos GPD, Bocci T, Celnik PA, Corben LA, Guidetti M, Koch G, Priori A, Rothwell JC, Sadnicka A, Spampinato D, Ugawa Y, Wessel MJ, Ferrucci R. Consensus paper: novel directions and next steps of non-invasive brain stimulation of the cerebellum in health and disease. Cerebellum. 2022;21:1092–122. https://doi.org/10.1007/s12311-021-01344-6.

    Article  PubMed  Google Scholar 

  10. Lee MH, Smyser CD, Shimony JS. Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol. 2013;34:1866–72. https://doi.org/10.3174/ajnr.A3263.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage. 2004;22:394–400. https://doi.org/10.1016/j.neuroimage.2003.12.030.

    Article  PubMed  Google Scholar 

  12. Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, Wang YF, Zang YF. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008;172:137–41. https://doi.org/10.1016/j.jneumeth.2008.04.012.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wang J, Deng XP, Wu YY, Li XL, Feng ZJ, Wang HX, Jing Y, Zhao N, Zang YF, Zhang J. High-frequency rTMS of the motor cortex modulates cerebellar and widespread activity as revealed by SVM. Front Neurosci. 2020;14:186. https://doi.org/10.3389/fnins.2020.00186.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Cao X, Wang Z, Chen X, Liu Y, Abdoulaye IA, Ju S, Zhang S, Wu S, Wang Y, Guo Y. Changes in resting-state neural activity and nerve fibres in ischaemic stroke patients with Hemiplegia. Brain Topogr. 2023;36:255–68. https://doi.org/10.1007/s10548-022-00937-6.

    Article  PubMed  Google Scholar 

  15. Zhu J, Jin Y, Wang K, Zhou Y, Feng Y, Yu M, Jin X. Frequency-dependent changes in the regional amplitude and synchronization of resting-state functional MRI in stroke. PLoS ONE. 2015;10:e0123850. https://doi.org/10.1371/journal.pone.0123850.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT. Activation likelihood estimation meta-analysis revisited. Neuroimage. 2012;59:2349–61. https://doi.org/10.1016/j.neuroimage.2011.09.017.

    Article  PubMed  Google Scholar 

  17. Wang J, Zhang JR, Zang YF, Wu T. Consistent decreased activity in the putamen in Parkinson's disease: a meta-analysis and an independent validation of resting-state fMRI. Gigascience. 2018;7. https://doi.org/10.1093/gigascience/giy071.

  18. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. https://doi.org/10.1371/journal.pmed.1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Higgins JP, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JA. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928. https://doi.org/10.1136/bmj.d5928.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Wolters AF, van de Weijer SCF, Leentjens AFG, Duits AA, Jacobs HIL, Kuijf ML. Resting-state fMRI in Parkinson’s disease patients with cognitive impairment: a meta-analysis. Parkinsonism Relat Disord. 2019;62:16–27. https://doi.org/10.1016/j.parkreldis.2018.12.016.

    Article  PubMed  Google Scholar 

  21. Oberman L, Edwards D, Eldaief M, Pascual-Leone A. Safety of theta burst transcranial magnetic stimulation: a systematic review of the literature. J Clin Neurophysiol. 2011;28:67–74. https://doi.org/10.1097/WNP.0b013e318205135f.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 2009;30:2907–26. https://doi.org/10.1002/hbm.20718.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P. Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp. 2012;33:1–13. https://doi.org/10.1002/hbm.21186.

    Article  PubMed  Google Scholar 

  24. McCarthy P. FSLeyes (1.6.0). Zenodo. 2023. https://doi.org/10.5281/zenodo.7657800

  25. Bernhardt J, Hayward KS, Kwakkel G, Ward NS, Wolf SL, Borschmann K, Krakauer JW, Boyd LA, Carmichael ST, Corbett D, Cramer SC. Agreed definitions and a shared vision for new standards in stroke recovery research: the Stroke Recovery and Rehabilitation Roundtable taskforce. Int J Stroke. 2017;12:444–50. https://doi.org/10.1177/1747493017711816.

    Article  PubMed  Google Scholar 

  26. Cromheeke S, Mueller SC. Probing emotional influences on cognitive control: an ALE meta-analysis of cognition emotion interactions. Brain Struct Funct. 2014;219:995–1008. https://doi.org/10.1007/s00429-013-0549-z.

    Article  PubMed  Google Scholar 

  27. Polyanska L, Critchley HD, Rae CL. Centrality of prefrontal and motor preparation cortices to Tourette syndrome revealed by meta-analysis of task-based neuroimaging studies. Neuroimage Clin. 2017;16:257–67. https://doi.org/10.1016/j.nicl.2017.08.004.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Chen W, Li H, Hou X, Jia X. Gray matter alteration in medication overuse headache: a coordinates-based activation likelihood estimation meta-analysis. Brain Imaging Behav. 2022;16:2307–19. https://doi.org/10.1007/s11682-022-00634-9.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kang N, Lee RD, Lee JH, Hwang MH. Functional balance and postural control improvements in patients with stroke after noninvasive brain stimulation: a meta-analysis. Arch Phys Med Rehabil. 2020;101:141–53. https://doi.org/10.1016/j.apmr.2019.09.003.

    Article  PubMed  Google Scholar 

  30. Gera G, Fling BW, Horak FB. Cerebellar white matter damage is associated with postural sway deficits in people with multiple sclerosis. Arch Phys Med Rehabil. 2020;101:258–64. https://doi.org/10.1016/j.apmr.2019.07.011.

    Article  PubMed  Google Scholar 

  31. Surgent OJ, Dadalko OI, Pickett KA, Travers BG. Balance and the brain: a review of structural brain correlates of postural balance and balance training in humans. Gait Posture. 2019;71:245–52. https://doi.org/10.1016/j.gaitpost.2019.05.011.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Xia Y, Tang X, Hu R, Liu J, Zhang Q, Tian S, Wang W, Li C, Zhu Y. Cerebellum-cerebrum paired target magnetic stimulation on balance function and brain network of patients with stroke: a functional near-infrared spectroscopy pilot study. Front Neurol. 2022;13:1071328. https://doi.org/10.3389/fneur.2022.1071328.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Popa T, Russo M, Vidailhet M, Roze E, Lehéricy S, Bonnet C, Apartis E, Legrand AP, Marais L, Meunier S, Gallea C. Cerebellar rTMS stimulation may induce prolonged clinical benefits in essential tremor, and subjacent changes in functional connectivity: an open label trial. Brain Stimul. 2013;6:175–9. https://doi.org/10.1016/j.brs.2012.04.009.

    Article  PubMed  CAS  Google Scholar 

  34. Chou T-Y, Wang J-C, Lin M-Y, Tsai P-Y. Low-frequency vs. theta burst transcranial magnetic stimulation for the treatment of chronic non-fluent aphasia in stroke: a proof-of-concept study. Front Aging Neurosci. 2022;13:800377. https://doi.org/10.3389/fnagi.2021.800377.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Roshan L, Chen R. The mechanisms of interhemispheric inhibition in the human motor cortex. J Physiol. 2002;543:317–26. https://doi.org/10.1113/jphysiol.2002.017673.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Qi S, Tian M, Rao Y, Sun C, Li X, Qiao J, Huang Z-G. Applying transcranial magnetic stimulation to rehabilitation of poststroke lower extremity function and an improvement: individual-target TMS. Wiley Interdiscip Rev Cogn Sci. 2023;14:e1636. https://doi.org/10.1002/wcs.1636.

    Article  PubMed  Google Scholar 

  37. Xie YJ, Wei QC, Chen Y, Liao LY, Li BJ, Tan HX, Jiang HH, Guo QF, Gao Q. Cerebellar theta burst stimulation on walking function in stroke patients: a randomized clinical trial. Front Neurosci. 2021;15:688569. https://doi.org/10.3389/fnins.2021.688569.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Koch G, Bonnì S, Casula EP, Iosa M, Paolucci S, Pellicciari MC, Cinnera AM, Ponzo V, Maiella M, Picazio S, Sallustio F, Caltagirone C. Effect of cerebellar stimulation on gait and balance recovery in patients with hemiparetic stroke: a randomized clinical trial. JAMA Neurol. 2019;76:170–8. https://doi.org/10.1001/jamaneurol.2018.3639.

    Article  PubMed  Google Scholar 

  39. Duan Q, Sun L, Wei C, Lu M, Yu F, Huang J, Huang X. Effect of cerebellar low frequency rTMS on lower limb motor function and cortical excitability in patients with posterior circulation stroke. Chin J Brain Dis Rehabil (Electronic Edition). 2020;10:352–6. https://doi.org/10.3877/cma.j.issn.2095-123X.2020.06.008.

    Article  Google Scholar 

  40. Bestmann S, Krakauer JW. The uses and interpretations of the motor-evoked potential for understanding behaviour. Exp Brain Res. 2015;233:679–89. https://doi.org/10.1007/s00221-014-4183-7.

    Article  PubMed  Google Scholar 

  41. Celnik P. Understanding and modulating motor learning with cerebellar stimulation. Cerebellum. 2015;14:171–4. https://doi.org/10.1007/s12311-014-0607-y.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hardwick RM, Therrien AS, Lesage E. Non-invasive stimulation of the motor cerebellum has potential cognitive confounds. Brain Stimul. 2021;14:922–3. https://doi.org/10.1016/j.brs.2021.05.011.

    Article  PubMed  Google Scholar 

  43. Rehme AK, Eickhoff SB, Rottschy C, Fink GR, Grefkes C. Activation likelihood estimation meta-analysis of motor-related neural activity after stroke. Neuroimage. 2012;59:2771–82. https://doi.org/10.1016/j.neuroimage.2011.10.023.

    Article  PubMed  Google Scholar 

  44. Favre I, Zeffiro TA, Detante O, Krainik A, Hommel M, Jaillard A. Upper limb recovery after stroke is associated with ipsilesional primary motor cortical activity: a meta-analysis. Stroke. 2014;45:1077–83. https://doi.org/10.1161/strokeaha.113.003168.

    Article  PubMed  Google Scholar 

  45. White LE, Andrews TJ, Hulette C, Richards A, Groelle M, Paydarfar J, Purves D. Structure of the human sensorimotor system I: morphology and cytoarchitecture of the central sulcus. Cereb Cortex. 1997;7:18–30. https://doi.org/10.1093/cercor/7.1.18.

    Article  PubMed  CAS  Google Scholar 

  46. Jin Y, Bai X, Jiang B, Guo Z, Mu Q. Repetitive transcranial magnetic stimulation induces quantified functional and structural changes in subcortical stroke: a combined arterial spin labeling perfusion and diffusion tensor imaging study. Front Hum Neurosci. 2022;16:829688. https://doi.org/10.3389/fnhum.2022.829688.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Puig J, Blasco G, Schlaug G, Stinear CM, Daunis IEP, Biarnes C, Figueras J, Serena J, Hernández-Pérez M, Alberich-Bayarri A, Castellanos M, Liebeskind DS, Demchuk AM, Menon BK, Thomalla G, Nael K, Wintermark M, Pedraza S. Diffusion tensor imaging as a prognostic biomarker for motor recovery and rehabilitation after stroke. Neuroradiology. 2017;59:343–51. https://doi.org/10.1007/s00234-017-1816-0.

    Article  PubMed  Google Scholar 

  48. Tlamsa AP, Brumberg JC. Organization and morphology of thalamocortical neurons of mouse ventral lateral thalamus. Somatosens Mot Res. 2010;27:34–43. https://doi.org/10.3109/08990221003646736.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Edwards LL, King EM, Buetefisch CM, Borich MR. Putting the “sensory” into sensorimotor control: the role of sensorimotor integration in goal-directed hand movements after stroke. Front Integr Neurosci. 2019;13:16. https://doi.org/10.3389/fnint.2019.00016.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Yoo JS, Choi BY, Chang CH, Jung YJ, Kim SH, Jang SH. Characteristics of injury of the corticospinal tract and corticoreticular pathway in hemiparetic patients with putaminal hemorrhage. BMC Neurol. 2014;14:121. https://doi.org/10.1186/1471-2377-14-121.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Frenkel-Toledo S, Levin MF, Berman S, Liebermann DG, Baniña MC, Solomon JM, Ofir-Geva S, Soroker N. Shared and distinct voxel-based lesion-symptom mappings for spasticity and impaired movement in the hemiparetic upper limb. Sci Rep. 2022;12:10169. https://doi.org/10.1038/s41598-022-14359-8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Utevsky AV, Smith DV, Huettel SA. Precuneus is a functional core of the default-mode network. Front Neurosci. 2014;34:932–40. https://doi.org/10.1523/jneurosci.4227-13.2014.

    Article  CAS  Google Scholar 

  53. Lv H, Wang Z, Tong E, Williams LM, Zaharchuk G, Zeineh M, Goldstein-Piekarski AN, Ball TM, Liao C, Wintermark M. Resting-state functional MRI: everything that nonexperts have always wanted to know. AJNR Am J Neuroradiol. 2018;39:1390–9. https://doi.org/10.3174/ajnr.A5527.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. An L, Cao Q, Sui M, Sun L, Zou Q, Zang Y, Wang Y. Local synchronization and amplitude of the fluctuation of spontaneous brain activity in attention-deficit/hyperactivity disorder: a resting-state fMRI study. Neurosci Bull. 2013;29:603–13. https://doi.org/10.1007/s12264-013-1353-8.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Bu X, Hu X, Zhang L, Li B, Zhou M, Lu L, Hu X, Li H, Yang Y, Tang W, Gong Q, Huang X. Investigating the predictive value of different resting-state functional MRI parameters in obsessive-compulsive disorder. Transl Psychiatry. 2019;9:17. https://doi.org/10.1038/s41398-018-0362-9.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Liu C-H, Kung Y-Y, Yeh T-C, Hsu P-S, Yang C-J, Cheng C-M, Lin H-C, Yang J-L, Wu T-P, Chang C-M, Hsieh J-C, Chen F-P. Differing spontaneous brain activity in healthy adults with two different body constitutions: a resting-state functional magnetic resonance imaging study. J Clin Med. 2019;8:951. https://doi.org/10.3390/jcm8070951.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Liao LY, Xie YJ, Chen Y, Gao Q. Cerebellar theta-burst stimulation combined with physiotherapy in subacute and chronic stroke patients: a pilot randomized controlled trial. Neurorehabil Neural Repair. 2021;35:23–32. https://doi.org/10.1177/1545968320971735.

    Article  PubMed  Google Scholar 

  58. 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;46:418–23. https://doi.org/10.2340/16501977-1802.

    Article  PubMed  Google Scholar 

  59. Ding X, Yuan J, Chen J, Guo H. Effects of repetitive transcranial magnetic stimulation of the cerebellum on walking disorder, balance function, and magnetic resonance spectroscopy indexes in patients with ischemic stroke. Hainan Med J. 2022;33:688–91. https://doi.org/10.3969/j.issn.1003-6350.2022.06.003.

    Article  Google Scholar 

  60. Zhang J, Shi Y. The effect of cerebellar repetitive transcranial magnetic stimulation on balance function in stroke patients. Med J Commun. 2019;33:605–6. https://doi.org/10.19767/j.cnki.32-1412.2019.06.021.

    Article  Google Scholar 

  61. Mao J, Cui L, Chang L, Wang J, Wang Y, Zhang Q, Zhang M. Analysis of the effect of repetitive transcranial magnetic stimulation of the cerebellum on the balance function of stroke patients. Reflexology Rehabil Med. 2021;2:146–9.

    Google Scholar 

  62. Wang S, Li L. Effects of cerebellar theta-burst stimulation on lower extremity motor function in stroke patients. Chin J Rehabil Theory Pract. 2022;28:1205–10. https://doi.org/10.3969/j.issn.1006-9771.2022.10.011.

    Article  Google Scholar 

  63. Im NG, Oh KR, Kim MG, Lee Y, Lim NN, Cho TH, Ryu SR, Yoon SR. Effect of low frequency cerebellar repetitive transcranial magnetic stimulation on balance impairment in patients with cerebral infarction. Ann Rehabil Med. 2022;46:275–83. https://doi.org/10.5535/arm.22058.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Zhu D, Liu Y, Zhao Y, Yan L, Zhu L, Qian F, Wu M. Dynamic changes of resting state functional network following acute ischemic stroke. J Chem Neuroanat. 2023;130:102272. https://doi.org/10.1016/j.jchemneu.2023.102272.

    Article  PubMed  Google Scholar 

  65. Quan X, Hu S, Meng C, Cheng L, Lu Y, Xia Y, Li W, Liang H, Li M, Liang Z. Frequency-specific changes of amplitude of low-frequency fluctuations in patients with acute basal ganglia ischemic stroke. Neural Plast. 2022;2022:4106131. https://doi.org/10.1155/2022/4106131.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Gao J, Yang C, Li Q, Chen L, Jiang Y, Liu S, Zhang J, Liu G, Chen J. Hemispheric difference of regional brain function exists in patients with acute stroke in different cerebral hemispheres: a resting-state fMRI study. Front Aging Neurosci. 2021;13:691518. https://doi.org/10.3389/fnagi.2021.691518.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Liang L, Hu R, Luo X, Feng B, Long W, Song R. Reduced complexity in stroke with motor deficits: a resting-state fMRI study. Neuroscience. 2020;434:35–43. https://doi.org/10.1016/j.neuroscience.2020.03.020.

    Article  PubMed  CAS  Google Scholar 

  68. Jiang C, Yi L, Cai S, Zhang L. Ischemic stroke in pontine and corona radiata: location specific impairment of neural network investigated with resting state fMRI. Front Neurol. 2019;10:575. https://doi.org/10.3389/fneur.2019.00575.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Fan L, Hu J, Ma W, Wang D, Yao Q, Shi J. Altered baseline activity and connectivity associated with cognitive impairment following acute cerebellar infarction: a resting-state fMRI study. Neurosci Lett. 2019;692:199–203. https://doi.org/10.1016/j.neulet.2018.11.007.

    Article  PubMed  CAS  Google Scholar 

  70. Chen J, Sun D, Shi Y, Jin W, Wang Y, Xi Q, Ren C. Dynamic alterations in spontaneous neural activity in multiple brain networks in subacute stroke patients: a resting-state fMRI study. Front Neurosci. 2019;12:994. https://doi.org/10.3389/fnins.2018.00994.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Chen L, Li C, Zhai J, Wang A, Song Q, Liu Y, Ma R, Han L, Ndasauka Y, Li X, Li H, Zhang X. Altered resting-state signals in patients with acute stroke in or under the thalamus. Neurosci Bull. 2016;32:585–90. https://doi.org/10.1007/s12264-016-0064-3.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Wu P, Zeng F, Li YX, Yu BL, Qiu LH, Qin W, Li J, Zhou YM, Liang FR. Changes of resting cerebral activities in subacute ischemic stroke patients. Neural Regen Res. 2015;10:760–5. https://doi.org/10.4103/1673-5374.156977.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Yin D, Luo Y, Song F, Xu D, Peterson BS, Sun L, Men W, Yan X, Fan M. Functional reorganization associated with outcome in hand function after stroke revealed by regional homogeneity. Neuroradiology. 2013;55:761–70. https://doi.org/10.1007/s00234-013-1146-9.

    Article  PubMed  Google Scholar 

  74. Cheng X, Qiao P, Sun R. Amplitude of low-frequency fluctuation in patients with unilateral limb weakness acute isolated pontine infarction:a resting-state functional MRI study. J Clin Exp Med. 2021;20:2109–13. https://doi.org/10.3969/j.issn.1671-4695.2021.19.026.

    Article  Google Scholar 

  75. Ruan X, Che C, Lin H, Chen H, Pan X. Using resting-state functional magnetic resonance to explore the changes of different frequency bands of amplitude of low-frequency fluctuantions in the basal ganglia after cerebral infarction. J Fujian Med Univ. 2020;54:411–6. https://doi.org/CNKI:SUN:FJYD.0.2020-06-011.

    Google Scholar 

  76. Yang H, Yu Q, Wei Y. Brain regional homogeneity alterations at resting state in the patients with motor deficits after stroke. Chin J Rehabil Med. 2020;35:10–6. https://doi.org/10.3969/j.issn.1001-1242.2020.01.003.

    Article  Google Scholar 

  77. Long Y, Li W, Huang Y, Huang F. Relationship between functional magnetic resonance imaging and swallowing function in patients with dysphagia after cerebral infarction. Chin Gen Pract. 2019;22:726–30. https://doi.org/10.12114/j.issn.1007-9572.2018.00.337.

    Article  Google Scholar 

  78. Wang X, Zhao Z, Yin D, Sun L, Zheng X, Jia J, Fan M. A fractional amplitude of low frequency fluctuation study of resting-state fMRI in stroke. Chin J Magn Reson Imaging. 2016;7:401–6. https://doi.org/10.12015/issn.1674-8034.2016.06.001.

    Article  Google Scholar 

  79. Hu M, Cheng HJ, Ji F, Chong JSX, Lu Z, Huang W, Ang KK, Phua KS, Chuang KH, Jiang X, Chew E, Guan C, Zhou JH. Brain functional changes in stroke following rehabilitation using brain-computer interface-assisted motor imagery with and without tDCS: a pilot study. Front Hum Neurosci. 2021;15:692304. https://doi.org/10.3389/fnhum.2021.692304.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work is supported by the Department of Science and Technology of Sichuan Province (No. 2022NSFSC0808).

Author information

Authors and Affiliations

Authors

Contributions

Yuheng Zeng and Jue Wang designed the study. Yuheng Zeng and Wanxin Zheng conducted the literature search and extracted the information. Yuheng Zeng and Zujuan Ye analyzed the data. Yuheng Zeng drafted the manuscript. All the authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Yuheng Zeng.

Ethics declarations

Ethical Approval

Not applicable.

Competing Interests

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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 59 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeng, Y., Ye, Z., Zheng, W. et al. Efficacy of Cerebellar Transcranial Magnetic Stimulation for Post-stroke Balance and Limb Motor Function Impairments: Meta-analyses of Random Controlled Trials and Resting-State fMRI Studies. Cerebellum (2024). https://doi.org/10.1007/s12311-024-01660-7

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12311-024-01660-7

Keywords

Navigation