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Effect of tDCS on corticomuscular coupling and the brain functional network of stroke patients

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Abstract

Transcranial direct current stimulation (tDCS) is an emerging brain intervention technique that has gained growing attention in recent years in the rehabilitation area. In this paper, we investigated the efficacy of tDCS in the rehabilitation process of stroke patients, utilizing corticomuscular coupling (CMC) and brain functional network analysis. Specifically, we examined changes in CMC relationships between the treatment and control groups before and after rehabilitation by transfer entropy (TE), and constructed brain functional networks by TE. We further calculated features of the functional networks, including node degree, global efficiency, clustering coefficient, characteristic path length, and small world index. Our results demonstrate that CMC in patients increased significantly after treatment, with greater improvements in the tDCS group, particularly within the beta and gamma bands. In addition, the functional brain network analysis revealed enhanced connectivity between brain regions, improved information processing capacity, and increased transmission efficiency in patients as their condition improved. Notably, treatment with tDCS resulted in more significant improvements than the sham group, with a statistically significant difference observed after rehabilitation treatment (p < 0.05). These findings provide compelling evidence regarding the role of tDCS in the treatment of stroke and highlight the potential of this approach in stroke rehabilitation.

Graphical Abstract

The use of tDCS for therapeutic interventions in stroke rehabilitation can significantly improve the coupling of patients' functional brain networks. Also, using Transfer Entropy (TE) as a characteristic of CMC, tDCS was found to significantly enhance patients' TE, i.e. enhanced CMC.

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References

  1. Sacco RL, Kasner SE, Broderick JP, Caplan LR, Connors J, Culebras A, Elkind MS, George MG, Hamdan AD, Higashida RT (2013) An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 44(7):2064–2089

    Article  PubMed  Google Scholar 

  2. Hachinski V, Donnan GA, Gorelick PB, Hacke W, Cramer SC, Kaste M, Fisher M, Brainin M, Buchan AM, Lo EH (2010) Stroke: working toward a prioritized world agenda. Stroke 41(6):1084–1099

    Article  PubMed  PubMed Central  Google Scholar 

  3. Singam A, Ytterberg C, Tham K, von Koch L (2015) Participation in complex and social everyday activities six years after stroke: predictors for return to pre-stroke level. PLoS One 10(12):e0144344

    Article  PubMed  PubMed Central  Google Scholar 

  4. Li S (2017) Spasticity, motor recovery, and neural plasticity after stroke. Front Neurol 8:120

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hummel F, Celnik P, Giraux P, Floel A, Wu W-H, Gerloff C, Cohen LG (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128(3):490–499

    Article  PubMed  Google Scholar 

  6. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553(1):293–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kim DY, Ohn SH, Yang EJ, Park C-I, Jung KJ (2009) Enhancing motor performance by anodal transcranial direct current stimulation in subacute stroke patients. Am J Phys Med Rehabil 88(10):829–836

    Article  PubMed  Google Scholar 

  8. Bornheim S, Croisier J-L, Maquet P, Kaux J-F (2020) Transcranial direct current stimulation associated with physical-therapy in acute stroke patients-a randomized, triple blind, sham-controlled study. Brain Stimul 13(2):329–336

    Article  PubMed  Google Scholar 

  9. Rossi C, Sallustio F, Di Legge S, Stanzione P, Koch G (2013) Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur J Neurol 20(1):202–204

    Article  CAS  PubMed  Google Scholar 

  10. Triccas LT, Burridge J, Hughes A, Pickering R, Desikan M, Rothwell J, Verheyden G (2016) Multiple sessions of transcranial direct current stimulation and upper extremity rehabilitation in stroke: a review and meta-analysis. Clin Neurophysiol 127(1):946–955

    Article  Google Scholar 

  11. Mima T, Toma K, Koshy B, Hallett M (2001) Coherence between cortical and muscular activities after subcortical stroke. Stroke 32(11):2597–2601

    Article  CAS  PubMed  Google Scholar 

  12. Krause V, Wach C, Südmeyer M, Ferrea S, Schnitzler A, Pollok B (2014) Cortico-muscular coupling and motor performance are modulated by 20 Hz transcranial alternating current stimulation (tACS) in Parkinson’s disease. Front Hum Neurosci 7:928

    Article  PubMed  PubMed Central  Google Scholar 

  13. von Carlowitz-Ghori K, Bayraktaroglu Z, Hohlefeld FU, Losch F, Curio G, Nikulin VV (2014) Corticomuscular coherence in acute and chronic stroke. Clin Neurophysiol 125(6):1182–1191

    Article  Google Scholar 

  14. Rossiter HE, Eaves C, Davis E, Boudrias M-H, Park C-h, Farmer S, Barnes G, Litvak V, Ward NS (2013) Changes in the location of cortico-muscular coherence following stroke. NeuroImage: Clin 2:50–55

    Article  Google Scholar 

  15. Grosse P, Guerrini R, Parmeggiani L, Bonanni P, Pogosyan A, Brown P (2003) Abnormal corticomuscular and intermuscular coupling in high-frequency rhythmic myoclonus. Brain 126(2):326–342

    Article  CAS  PubMed  Google Scholar 

  16. Meng F, Tong K-Y, Chan S-T, Wong W-W, Lui K-H, Tang K-W, Gao X, Gao S (2008) Cerebral plasticity after subcortical stroke as revealed by cortico-muscular coherence. IEEE Trans Neural Syst Rehabil Eng 17(3):234–243

    Article  PubMed  Google Scholar 

  17. Brown P, Salenius S, Rothwell JC, Hari R (1998) Cortical correlate of the Piper rhythm in humans. J Neurophysiol 80(6):2911–2917

    Article  CAS  PubMed  Google Scholar 

  18. Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85(2):461

    Article  CAS  PubMed  Google Scholar 

  19. Baravalle R, Guisande N, Granado M, Rosso OA, Montani F (2019) Characterization of visuomotor/imaginary movements in EEG: an information theory and complex network approach. Front Phys 7:115

    Article  Google Scholar 

  20. Urbin M, Hong X, Lang CE, Carter AR (2014) Resting-state functional connectivity and its association with multiple domains of upper-extremity function in chronic stroke. Neurorehabil Neural Repair 28(8):761–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, Pope DL, Shulman GL, Corbetta M (2010) Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol 67(3):365–375

    Article  PubMed  PubMed Central  Google Scholar 

  22. Nicolo P, Rizk S, Magnin C, Pietro MD, Schnider A, Guggisberg AG (2015) Coherent neural oscillations predict future motor and language improvement after stroke. Brain 138(10):3048–3060

    Article  PubMed  Google Scholar 

  23. Fallani FDV, Pichiorri F, Morone G, Molinari M, Babiloni F, Cincotti F, Mattia D (2013) Multiscale topological properties of functional brain networks during motor imagery after stroke. Neuroimage 83:438–449

    Article  Google Scholar 

  24. Koessler L, Maillard L, Benhadid A, Vignal JP, Felblinger J, Vespignani H, Braun M (2009) Automated cortical projection of EEG sensors: anatomical correlation via the international 10–10 system. Neuroimage 46(1):64–72

    Article  CAS  PubMed  Google Scholar 

  25. Roy A, Baxter B, He B (2014) High-definition transcranial direct current stimulation induces both acute and persistent changes in broadband cortical synchronization: a simultaneous tDCS–EEG study. IEEE Trans Biomed Eng 61(7):1967–1978

    Article  PubMed  PubMed Central  Google Scholar 

  26. Omlor W, Patino L, Hepp-Reymond M-C, Kristeva R (2007) Gamma-range corticomuscular coherence during dynamic force output. Neuroimage 34(3):1191–1198

    Article  PubMed  Google Scholar 

  27. Kristeva R, Patino L, Omlor W (2007) Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output. Neuroimage 36(3):785–792

    Article  PubMed  Google Scholar 

  28. Dai C, Suresh NL, Suresh AK, Rymer WZ, Hu X (2017) Altered motor unit discharge coherence in paretic muscles of stroke survivors. Front Neurol 8:202

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wheaton LA, Bohlhalter S, Nolte G, Shibasaki H, Hattori N, Fridman E, Vorbach S, Grafman J, Hallett M (2008) Cortico-cortical networks in patients with ideomotor apraxia as revealed by EEG coherence analysis. Neurosci Lett 433(2):87–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Slewa-Younan S, Green AM, Baguley IJ, Felmingham KL, Haig AR, Gordon E (2002) Is ‘gamma’(40 Hz) synchronous activity disturbed in patients with traumatic brain injury? Clin Neurophysiol 113(10):1640–1646

    Article  PubMed  Google Scholar 

  31. Desowska A, Turner DL (2019) Dynamics of brain connectivity after stroke. Rev Neurosci 30(6):605–623

    Article  PubMed  Google Scholar 

  32. Salenius S, Hari R (2003) Synchronous cortical oscillatory activity during motor action. Curr Opin Neurobiol 13(6):678–684

    Article  CAS  PubMed  Google Scholar 

  33. Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701

    Article  CAS  PubMed  Google Scholar 

  34. Guggisberg AG, Koch PJ, Hummel FC, Buetefisch CM (2019) Brain networks and their relevance for stroke rehabilitation. Clin Neurophysiol 130(7):1098–1124

    Article  PubMed  PubMed Central  Google Scholar 

  35. Power JD, Fair DA, Schlaggar BL, Petersen SE (2010) The development of human functional brain networks. Neuron 67(5):735–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Zihao Zhuo for assisting us with the experiments and checking the manuscript.

Funding

This work was supported by the National Key R&D Program of China (No.2021ZD0113204), the National Natural Science Foundation of China (Nos. 61971169, 61971168), and the Zhejiang Provincial Key Research and Development Program of China (No.2021C03031).

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Zhuyao Fan and Xugang Xi wrote the main manuscript text; Zhong Lü, Ting Wang, and Lihua Li reviewed the manuscript; Hangcheng Li and Maofeng Wang conducted an ethical review.

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Correspondence to Xugang Xi.

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All the experimental procedures were approved by the ethics committee of Hangzhou Mingzhou Brain Rehabilitation Hospital.

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The authors declare no competing interests.

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Fan, Z., Xi, X., Wang, T. et al. Effect of tDCS on corticomuscular coupling and the brain functional network of stroke patients. Med Biol Eng Comput 61, 3303–3317 (2023). https://doi.org/10.1007/s11517-023-02905-z

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  • DOI: https://doi.org/10.1007/s11517-023-02905-z

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