Effects of Repetitive Transcranial Magnetic Stimulation at Different Targets on Brain Function in Stroke Patients: a Randomized Controlled Trial

Overview

Journal Front Neurol

Specialty Neurology

Date 2024 Oct 15

PMID 39403265

Authors

Li Zhao

Li Chen

Chunyan Wang

Sha Li

Chunxiao Wan

Affiliations

Soon will be listed here.

Abstract

Introduction: Repetitive transcranial magnetic stimulation (rTMS) can improve post stroke motor function. However, there is little research on targets. The purpose of this study is to investigate the effects of rTMS therapy with different targets on post stroke motor function and neural plasticity.

Methods: Fifty-four subjects were randomly divided into M1 (Primary motor area) group, SMA (supplementary motor area) group and Sham group, and were given 10 Hz on the affected M1 area, SMA area and sham stimulation rTMS. The primary outcomes included Fugl-Meyer Assessment Upper Extremity Scale (FMA-UE), Fugl-Meyer Assessment Lower Extremity Scale (FMA-LE) and Berg balance scale (BBS). Secondary outcomes: amplitude of low frequency fluctuation (ALFF), regional homogeneity (ReHo) and functional connectivity (FC) were analyzed by functional magnetic resonance imaging (fMRI) to evaluate brain functional activation and functional connectivity changes.

Results: The 2-way repeated-measures ANOVA revealed a significant group × time interaction ( = 23.494, < 0.001; = 10.801, < 0.001; = 17.812, < 0.001) in the FMA-UE, FMA-LE and BBS scores. analysis indicated that 4 weeks of SMA rTMS resulted in an increase in FMA-UE, FMA-LE and BBS scores compared with Sham group ( = 0.006; = 0.033; = 0.012), SMA group was significantly increased in BBS compared with M1 group ( = 0.034). Moreover, there were significant effects of time in all 3 groups in the FMA-UE, FMA-LE and BBS scores ( < 0.001). In addition, the increase of ALFF in the supramarginal gyrus on the affected side was correlated with better FMA-UE recovery, the increase of ALFF in the middle temporal gyrus and the middle frontal gyrus on the affected side was positively correlated with the improvement of BBS, and the ALFF in the cerebellum on the healthy side was negatively correlated with the improvement of BBS. There was a positive correlation between FC (SMA - ipsilateral cerebellum) changes and BBS changes in SMA group.

Discussion: In conclusion, SMA-rTMS intervention has a better recovery effect on motor dysfunction after stroke than Sham-rTMS. SMA-rTMS led to similar improvement on motor function but significantly greater improvement on balance compared to M1-rTMS, and this may pave a new way for stroke rehabilitation.

Clinical Trial Registration: Registration number: ChiCTR2200060955, https://www.chictr.org.cn/.

References

Saini V, Guada L, Yavagal D . Global Epidemiology of Stroke and Access to Acute Ischemic Stroke Interventions. Neurology. 2021; 97(20 Suppl 2):S6-S16. DOI: 10.1212/WNL.0000000000012781. View

Hordacre B, Moezzi B, Ridding M . Neuroplasticity and network connectivity of the motor cortex following stroke: A transcranial direct current stimulation study. Hum Brain Mapp. 2018; 39(8):3326-3339. PMC: 6866552. DOI: 10.1002/hbm.24079. View

Fernandez L, Rogasch N, Do M, Clark G, Major B, Teo W . Cerebral Cortical Activity Following Non-invasive Cerebellar Stimulation-a Systematic Review of Combined TMS and EEG Studies. Cerebellum. 2020; 19(2):309-335. DOI: 10.1007/s12311-019-01093-7. View

Bozkurt B, Yagmurlu K, Middlebrooks E, Karadag A, Ovalioglu T, Jagadeesan B . Microsurgical and Tractographic Anatomy of the Supplementary Motor Area Complex in Humans. World Neurosurg. 2016; 95:99-107. DOI: 10.1016/j.wneu.2016.07.072. View

Palmer J, Wheaton L, Gray W, Saltao da Silva M, Wolf S, Borich M . Role of Interhemispheric Cortical Interactions in Poststroke Motor Function. Neurorehabil Neural Repair. 2019; 33(9):762-774. PMC: 6713273. DOI: 10.1177/1545968319862552. View

Xia Y, Tang X, Hu R, Liu J, Zhang Q, Tian S . 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. 2023; 13:1071328. PMC: 9813387. DOI: 10.3389/fneur.2022.1071328. View

Krakauer J, Carmichael S, Corbett D, Wittenberg G . Getting neurorehabilitation right: what can be learned from animal models?. Neurorehabil Neural Repair. 2012; 26(8):923-31. PMC: 4554531. DOI: 10.1177/1545968312440745. View

Manji A, Amimoto K, Matsuda T, Wada Y, Inaba A, Ko S . Effects of transcranial direct current stimulation over the supplementary motor area body weight-supported treadmill gait training in hemiparetic patients after stroke. Neurosci Lett. 2017; 662:302-305. DOI: 10.1016/j.neulet.2017.10.049. View

Guggisberg A, Koch P, Hummel F, Buetefisch C . Brain networks and their relevance for stroke rehabilitation. Clin Neurophysiol. 2019; 130(7):1098-1124. PMC: 6603430. DOI: 10.1016/j.clinph.2019.04.004. View

10.

Kim J, Lee J, Jo H, Kim S, Lee J, Kim S . Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: functional connectivity-based parcellation method. Neuroimage. 2009; 49(3):2375-86. PMC: 2819173. DOI: 10.1016/j.neuroimage.2009.10.016. View

11.

Cramer S . Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Ann Neurol. 2008; 63(3):272-87. DOI: 10.1002/ana.21393. View

12.

Mosayebi-Samani M, Agboada D, Mutanen T, Haueisen J, Kuo M, Nitsche M . Transferability of cathodal tDCS effects from the primary motor to the prefrontal cortex: A multimodal TMS-EEG study. Brain Stimul. 2023; 16(2):515-539. DOI: 10.1016/j.brs.2023.02.010. View

13.

Liao L, Zhu Y, Peng Q, Gao Q, Liu L, Wang Q . Intermittent Theta-Burst Stimulation for Stroke: Primary Motor Cortex Versus Cerebellar Stimulation: A Randomized Sham-Controlled Trial. Stroke. 2023; 55(1):156-165. DOI: 10.1161/STROKEAHA.123.044892. View

14.

Koch G, Bonni S, Casula E, Iosa M, Paolucci S, Pellicciari M . Effect of Cerebellar Stimulation on Gait and Balance Recovery in Patients With Hemiparetic Stroke: A Randomized Clinical Trial. JAMA Neurol. 2018; 76(2):170-178. PMC: 6439971. DOI: 10.1001/jamaneurol.2018.3639. View

15.

Grefkes C, Nowak D, Wang L, Dafotakis M, Eickhoff S, Fink G . Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage. 2009; 50(1):233-42. PMC: 8020334. DOI: 10.1016/j.neuroimage.2009.12.029. View

16.

Simonetta-Moreau M . Non-invasive brain stimulation (NIBS) and motor recovery after stroke. Ann Phys Rehabil Med. 2014; 57(8):530-542. DOI: 10.1016/j.rehab.2014.08.003. View

17.

Hosomi K, Morris S, Sakamoto T, Taguchi J, Maruo T, Kageyama Y . Daily Repetitive Transcranial Magnetic Stimulation for Poststroke Upper Limb Paresis in the Subacute Period. J Stroke Cerebrovasc Dis. 2016; 25(7):1655-1664. DOI: 10.1016/j.jstrokecerebrovasdis.2016.02.024. View

18.

Luk K, Ouyang H, Pang M . Low-Frequency rTMS over Contralesional M1 Increases Ipsilesional Cortical Excitability and Motor Function with Decreased Interhemispheric Asymmetry in Subacute Stroke: A Randomized Controlled Study. Neural Plast. 2022; 2022:3815357. PMC: 8756161. DOI: 10.1155/2022/3815357. View

19.

Silasi G, Murphy T . Stroke and the connectome: how connectivity guides therapeutic intervention. Neuron. 2014; 83(6):1354-68. DOI: 10.1016/j.neuron.2014.08.052. View

20.

Ni J, Jiang W, Gong X, Fan Y, Qiu H, Dou J . Effect of rTMS intervention on upper limb motor function after stroke: A study based on fNIRS. Front Aging Neurosci. 2023; 14:1077218. PMC: 9880218. DOI: 10.3389/fnagi.2022.1077218. View