The Impact of Transcranial Direct Current Stimulation Combined with Task-Oriented Training on EEG-Based Measures of Motor Recovery in Chronic Stroke: A Randomized Clinical Trial Study
-
Maryam Zolghadr
,
Shohreh Noorizadeh Dehkordi
,
Javad Sarrafzadeh
,
Saeed Talebian
,
Hassan Haddadzade niri
,
Marzieh Yassin
Abstract
Introduction: Upper limb motor disability, with a prevalence of approximately 77%, is the most common complication after stroke. Despite advancements in rehabilitation, many patients face persistent upper limb deficits. Adopting an approach combining top-down and bottom-up interventions may enhance neuroplasticity and improve upper limb function. This study aims to determine the effect of motor cortical trans-Cranial Direct Current stimulation (tDCs) as a top-down approach combined with Task-Oriented Training (TOT) as a down-to-top intervention on changes in Electroencephalography (EEG) spectral power in chronic stroke patients.
Materials and Methods: Thirty chronic hemiparetic stroke survivors were randomly assigned to receive real or sham stimulation targeting the primary motor cortex (C3/C4) at 2 mA for 20 minutes and TOT daily over 15 sessions. Electroencephalography was conducted pre- and post-intervention, with a 3-month follow-up, and the relative powers of delta to gamma frequency bands were recorded during the movement task with each hand (healthy and involved).
Results: Significant differences in theta (P=.000), alpha (P=0.004), beta (P=0.000), and gamma (P=0.003) relative powers were observed between groups at follow-up. Additionally, Friedman tests revealed a significant decrease in alpha and beta bands’ relative powers in the healthy hand of the control group at follow-up (P=0.001). The experimental group displayed increased alpha and beta powers and decreased theta, without statistical significance.
Conclusion: The increase in the relative power of low frequencies and the decrease in high frequencies in the sham group, which were more prominent than the increases in alpha and beta bands’ relative power and the decrease in theta in the experimental group, can indicate that the presence of real-tDCs has been able to prevent the recovery drop of relative powers. Due to the inconsistent effects of tDCs on the EEG power spectrum in stroke patients, conventional tDCs administration may require adjustments for optimal application to brain target points.
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2. Donkor ES. Stroke in the century: a snapshot of the burden, epidemiology, and quality of life. Stroke research and treatment. 2018;2018
3. Yao X, Cui L, Wang J, Feng W, Bao Y, Xie Q. Effects of transcranial direct current stimulation with virtual reality on upper limb function in patients with ischemic stroke: a randomized controlled trial. Journal of NeuroEngineering and Rehabilitation. 2020;17(1):73.[10.1186/s12984-020-00699-x]
4. Van Hoornweder S, Debeuf R, Verstraelen S, Meesen R, Cuypers K. Unravelling ipsilateral interactions between left dorsal premotor and primary motor cortex: a proof of concept study. Neuroscience. 2021;466:36-46
5. Tu-Chan AP, Natraj N, Godlove J, Abrams G, Ganguly K. Effects of somatosensory electrical stimulation on motor function and cortical oscillations. Journal of neuroengineering and rehabilitation. 2017;14:1-9
6. Dimyan MA, Cohen LG. Contribution of transcranial magnetic stimulation to the understanding of functional recovery mechanisms after stroke. Neurorehabilitation and neural repair. 2010;24(2):125-35
7. Liew S-L, Santarnecchi E, Buch ER, Cohen LG. Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery. Frontiers in human neuroscience. 2014;8:378
8. López ND, Monge Pereira E, Centeno EJ, Miangolarra Page JC. Motor imagery as a complementary technique for functional recovery after stroke: a systematic review. Topics in stroke rehabilitation. 2019;26(8):576-87
9. Daly JJ, Wolpaw JR. Brain–computer interfaces in neurological rehabilitation. The Lancet Neurology. 2008;7(11):1032-43
10. Bhagat NA, Yozbatiran N, Sullivan JL, Paranjape R, Losey C, Hernandez Z, et al. Neural activity modulations and motor recovery following brain-exoskeleton interface mediated stroke rehabilitation. NeuroImage: Clinical. 2020;28:102502
11. Remsik AB, Williams Jr L, Gjini K, Dodd K, Thoma J, Jacobson T, et al. Ipsilesional Mu rhythm desynchronization and changes in motor behavior following post stroke BCI intervention for motor rehabilitation. Frontiers in Neuroscience. 2019;13:53
12. Yassin M, Takamjani IE, Talebian S, Maroufi N, Sarrafzadeh J, Ahmadi A, et al. Preparatory Brain Activity and Anticipatory Postural Control in cervical myofascial trigger point. Journal of Modern Rehabilitation. 2022
13. Swart T, Chisholm K, Brown P. Neuroscience for leadership: Harnessing the brain gain advantage: Springer; 2015.
14. Pellegrino G, Maran M, Turco C, Weis L, Di Pino G, Piccione F, et al. Bilateral transcranial direct current stimulation reshapes resting-state brain networks: a magnetoencephalography assessment. Neural Plasticity. 2018;2018
15. Mondini V, Mangia AL, Cappello A. Single-session tDCS over the dominant hemisphere affects contralateral spectral EEG power, but does not enhance neurofeedback-guided event-related desynchronization of the non-dominant hemisphere's sensorimotor rhythm. PloS one. 2018;13(3):e0193004
16. Baharlouei H, Goosheh M, Moore M, Ramezani Ahmadi AH, Yassin M, Jaberzadeh S. The effect of transcranial direct current stimulation on rating of perceived exertion: A systematic review of the literature. Psychophysiology. 2024:e14520.[10.1111/psyp.14520]
17. Group MoSRW. VA/DOD Clinical practice guideline for the management of stroke rehabilitation. Journal of rehabilitation research and development. 2010;47(9):1-43
18. Rossiter HE, Boudrias M-H, Ward NS. Do movement-related beta oscillations change after stroke? Journal of neurophysiology. 2014;112(9):2053-8
19. Cha T-H, Hwang H-S. Rehabilitation interventions combined with noninvasive brain stimulation on upper limb motor function in stroke patients. Brain Sciences. 2022;12(8):994
20. Ho K-A, Taylor JL, Chew T, Gálvez V, Alonzo A, Bai S, et al. The effect of transcranial direct current stimulation (tDCS) electrode size and current intensity on motor cortical excitability: evidence from single and repeated sessions. Brain stimulation. 2016;9(1):1-7
21. Afsharipor M, Hejazi-Shirmard M, Irani A, Kalantari M, Baghban AA. Combined Transcranial Direct Current Stimulation with Occupational Therapy Improves Activities of Daily Living in Traumatic Brain Injuries: A Pilot Randomized Clinical Trial. Journal of Modern Rehabilitation. 2024;18(1):114-20
22. da Silva ESM, Ocamoto GN, Santos-Maia GLd, de Fatima Carreira Moreira Padovez R, Trevisan C, de Noronha MA, et al. The effect of priming on outcomes of task-oriented training for the upper extremity in chronic stroke: a systematic review and meta-analysis. Neurorehabilitation and Neural Repair. 2020;34(6):479-504
23. Snyder DB, Schmit BD, Hyngstrom AS, Beardsley SA. Electroencephalography resting‐state networks in people with Stroke. Brain and Behavior. 2021;11(5):e02097
24. Boonstra TW, Nikolin S, Meisener A-C, Martin DM, Loo CK. Change in mean frequency of resting-state electroencephalography after transcranial direct current stimulation. Frontiers in human neuroscience. 2016;10:270
25. Hu J, Li C, Hua Y, Zhang B, Gao B-Y, Liu P-L, et al. Constrained-induced movement therapy promotes motor function recovery by enhancing the remodeling of ipsilesional corticospinal tract in rats after stroke. Brain research. 2019;1708:27-35
26. Hu M, Ji F, Lu Z, Huang W, Khosrowabadi R, Zhao L, et al., editors. Differential amplitude of low-frequency fluctuations in brain networks after BCI training with and without tDCS in stroke. 2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC); 2018: IEEE.
27. Cunningham DA, Machado A, Janini D, Varnerin N, Bonnett C, Yue G, et al. Assessment of inter-hemispheric imbalance using imaging and noninvasive brain stimulation in patients with chronic stroke. Archives of physical medicine and rehabilitation. 2015;96(4):S94-S103
28. Van Wijngaarden JB, Zucca R, Finnigan S, Verschure PF. The impact of cortical lesions on thalamo-cortical network dynamics after acute ischaemic stroke: a combined experimental and theoretical study. PLoS computational biology. 2016;12(8):e1005048
29. Bao S-C, Wong W-W, Leung TWH, Tong K-Y. Cortico-muscular coherence modulated by high-definition transcranial direct current stimulation in people with chronic stroke. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2018;27(2):304-13
30. Jomhouri S, Talebian S, Vaez-Mousavi M, Sadjadi-Hazaveh SH. Training Interventions Change Relative Power Spectrum of Alpha After Anterior Cruciate Ligament Deficiency in Athletes. Journal of Modern Rehabilitation. 2023
31. Naghdi S, Ansari NN, Mansouri K, Hasson S. A neurophysiological and clinical study of Brunnstrom recovery stages in the upper limb following stroke. Brain Inj. 2010;24(11):1372-8.[10.3109/02699052.2010.506860]
32. Kim W-S, Kwon BS, Seo HG, Park J, Paik N-J. Low-frequency repetitive transcranial magnetic stimulation over contralesional motor cortex for motor recovery in subacute ischemic stroke: a randomized sham-controlled trial. Neurorehabilitation and neural repair. 2020;34(9):856-67
33. Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, et al. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47(6):e98-e169
34. Yuvaraj R, Murugappan M, Mohamed Ibrahim N, Iqbal Omar M, Sundaraj K, Mohamad K, et al. On the analysis of EEG power, frequency and asymmetry in Parkinson’s disease during emotion processing. Behavioral and Brain Functions. 2014;10(1):12.[10.1186/1744-9081-10-12]
35. Ulam F, Shelton C, Richards L, Davis L, Hunter B, Fregni F, et al. Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury. Clinical Neurophysiology. 2015;126(3):486-96
36. Dodd KC, Nair VA, Prabhakaran V. Role of the contralesional vs. ipsilesional hemisphere in stroke recovery. Frontiers in human neuroscience. 2017;11:469
37. Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? The Lancet Neurology. 2006;5(8):708-12
38. van der Cruijsen J, Dooren RF, Schouten AC, Oostendorp TF, Frens MA, Ribbers GM, et al. Addressing the inconsistent electric fields of tDCS by using patient-tailored configurations in chronic stroke: Implications for treatment. NeuroImage: Clinical. 2022;36:103178
39. Salazar CA, Feng W, Bonilha L, Kautz S, Jensen JH, George MS, et al. Transcranial Direct Current Stimulation for Chronic Stroke: Is Neuroimaging the Answer to the Next Leap Forward? Journal of Clinical Medicine. 2023;12(7):2601
40. Wiesman AI, Mills MS, McDermott TJ, Spooner RK, Coolidge NM, Wilson TW. Polarity-dependent modulation of multi-spectral neuronal activity by transcranial direct current stimulation. Cortex. 2018;108:222-33
41. McDermott TJ, Wiesman AI, Mills MS, Spooner RK, Coolidge NM, Proskovec AL, et al. tDCS modulates behavioral performance and the neural oscillatory dynamics serving visual selective attention. Human brain mapping. 2019;40(3):729-40.[10.1002/hbm.24405]
42. Dutta A. Simultaneous functional near-infrared spectroscopy (fNIRS) and electroencephalogram (EEG) to elucidate neurovascular modulation by transcranial electrical stimulation (tES). Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation. 2021;14(5):1093-4
43. Seibt O, Brunoni AR, Huang Y, Bikson M. The pursuit of DLPFC: non-neuronavigated methods to target the left dorsolateral pre-frontal cortex with symmetric bicephalic transcranial direct current stimulation (tDCS). Brain stimulation. 2015;8(3):590-602
44. Zakaria H, Valentine O, Mayza A. Analysis of quantitative EEG (QEEG) parameters on the effect of transcranial direct current stimulation (TDCS) on post-stroke patients. AIP Conference Proceedings. 2021;2344(1):050001.[10.1063/5.0047216]
2. Donkor ES. Stroke in the century: a snapshot of the burden, epidemiology, and quality of life. Stroke research and treatment. 2018;2018
3. Yao X, Cui L, Wang J, Feng W, Bao Y, Xie Q. Effects of transcranial direct current stimulation with virtual reality on upper limb function in patients with ischemic stroke: a randomized controlled trial. Journal of NeuroEngineering and Rehabilitation. 2020;17(1):73.[10.1186/s12984-020-00699-x]
4. Van Hoornweder S, Debeuf R, Verstraelen S, Meesen R, Cuypers K. Unravelling ipsilateral interactions between left dorsal premotor and primary motor cortex: a proof of concept study. Neuroscience. 2021;466:36-46
5. Tu-Chan AP, Natraj N, Godlove J, Abrams G, Ganguly K. Effects of somatosensory electrical stimulation on motor function and cortical oscillations. Journal of neuroengineering and rehabilitation. 2017;14:1-9
6. Dimyan MA, Cohen LG. Contribution of transcranial magnetic stimulation to the understanding of functional recovery mechanisms after stroke. Neurorehabilitation and neural repair. 2010;24(2):125-35
7. Liew S-L, Santarnecchi E, Buch ER, Cohen LG. Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery. Frontiers in human neuroscience. 2014;8:378
8. López ND, Monge Pereira E, Centeno EJ, Miangolarra Page JC. Motor imagery as a complementary technique for functional recovery after stroke: a systematic review. Topics in stroke rehabilitation. 2019;26(8):576-87
9. Daly JJ, Wolpaw JR. Brain–computer interfaces in neurological rehabilitation. The Lancet Neurology. 2008;7(11):1032-43
10. Bhagat NA, Yozbatiran N, Sullivan JL, Paranjape R, Losey C, Hernandez Z, et al. Neural activity modulations and motor recovery following brain-exoskeleton interface mediated stroke rehabilitation. NeuroImage: Clinical. 2020;28:102502
11. Remsik AB, Williams Jr L, Gjini K, Dodd K, Thoma J, Jacobson T, et al. Ipsilesional Mu rhythm desynchronization and changes in motor behavior following post stroke BCI intervention for motor rehabilitation. Frontiers in Neuroscience. 2019;13:53
12. Yassin M, Takamjani IE, Talebian S, Maroufi N, Sarrafzadeh J, Ahmadi A, et al. Preparatory Brain Activity and Anticipatory Postural Control in cervical myofascial trigger point. Journal of Modern Rehabilitation. 2022
13. Swart T, Chisholm K, Brown P. Neuroscience for leadership: Harnessing the brain gain advantage: Springer; 2015.
14. Pellegrino G, Maran M, Turco C, Weis L, Di Pino G, Piccione F, et al. Bilateral transcranial direct current stimulation reshapes resting-state brain networks: a magnetoencephalography assessment. Neural Plasticity. 2018;2018
15. Mondini V, Mangia AL, Cappello A. Single-session tDCS over the dominant hemisphere affects contralateral spectral EEG power, but does not enhance neurofeedback-guided event-related desynchronization of the non-dominant hemisphere's sensorimotor rhythm. PloS one. 2018;13(3):e0193004
16. Baharlouei H, Goosheh M, Moore M, Ramezani Ahmadi AH, Yassin M, Jaberzadeh S. The effect of transcranial direct current stimulation on rating of perceived exertion: A systematic review of the literature. Psychophysiology. 2024:e14520.[10.1111/psyp.14520]
17. Group MoSRW. VA/DOD Clinical practice guideline for the management of stroke rehabilitation. Journal of rehabilitation research and development. 2010;47(9):1-43
18. Rossiter HE, Boudrias M-H, Ward NS. Do movement-related beta oscillations change after stroke? Journal of neurophysiology. 2014;112(9):2053-8
19. Cha T-H, Hwang H-S. Rehabilitation interventions combined with noninvasive brain stimulation on upper limb motor function in stroke patients. Brain Sciences. 2022;12(8):994
20. Ho K-A, Taylor JL, Chew T, Gálvez V, Alonzo A, Bai S, et al. The effect of transcranial direct current stimulation (tDCS) electrode size and current intensity on motor cortical excitability: evidence from single and repeated sessions. Brain stimulation. 2016;9(1):1-7
21. Afsharipor M, Hejazi-Shirmard M, Irani A, Kalantari M, Baghban AA. Combined Transcranial Direct Current Stimulation with Occupational Therapy Improves Activities of Daily Living in Traumatic Brain Injuries: A Pilot Randomized Clinical Trial. Journal of Modern Rehabilitation. 2024;18(1):114-20
22. da Silva ESM, Ocamoto GN, Santos-Maia GLd, de Fatima Carreira Moreira Padovez R, Trevisan C, de Noronha MA, et al. The effect of priming on outcomes of task-oriented training for the upper extremity in chronic stroke: a systematic review and meta-analysis. Neurorehabilitation and Neural Repair. 2020;34(6):479-504
23. Snyder DB, Schmit BD, Hyngstrom AS, Beardsley SA. Electroencephalography resting‐state networks in people with Stroke. Brain and Behavior. 2021;11(5):e02097
24. Boonstra TW, Nikolin S, Meisener A-C, Martin DM, Loo CK. Change in mean frequency of resting-state electroencephalography after transcranial direct current stimulation. Frontiers in human neuroscience. 2016;10:270
25. Hu J, Li C, Hua Y, Zhang B, Gao B-Y, Liu P-L, et al. Constrained-induced movement therapy promotes motor function recovery by enhancing the remodeling of ipsilesional corticospinal tract in rats after stroke. Brain research. 2019;1708:27-35
26. Hu M, Ji F, Lu Z, Huang W, Khosrowabadi R, Zhao L, et al., editors. Differential amplitude of low-frequency fluctuations in brain networks after BCI training with and without tDCS in stroke. 2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC); 2018: IEEE.
27. Cunningham DA, Machado A, Janini D, Varnerin N, Bonnett C, Yue G, et al. Assessment of inter-hemispheric imbalance using imaging and noninvasive brain stimulation in patients with chronic stroke. Archives of physical medicine and rehabilitation. 2015;96(4):S94-S103
28. Van Wijngaarden JB, Zucca R, Finnigan S, Verschure PF. The impact of cortical lesions on thalamo-cortical network dynamics after acute ischaemic stroke: a combined experimental and theoretical study. PLoS computational biology. 2016;12(8):e1005048
29. Bao S-C, Wong W-W, Leung TWH, Tong K-Y. Cortico-muscular coherence modulated by high-definition transcranial direct current stimulation in people with chronic stroke. IEEE Transactions on Neural Systems and Rehabilitation Engineering. 2018;27(2):304-13
30. Jomhouri S, Talebian S, Vaez-Mousavi M, Sadjadi-Hazaveh SH. Training Interventions Change Relative Power Spectrum of Alpha After Anterior Cruciate Ligament Deficiency in Athletes. Journal of Modern Rehabilitation. 2023
31. Naghdi S, Ansari NN, Mansouri K, Hasson S. A neurophysiological and clinical study of Brunnstrom recovery stages in the upper limb following stroke. Brain Inj. 2010;24(11):1372-8.[10.3109/02699052.2010.506860]
32. Kim W-S, Kwon BS, Seo HG, Park J, Paik N-J. Low-frequency repetitive transcranial magnetic stimulation over contralesional motor cortex for motor recovery in subacute ischemic stroke: a randomized sham-controlled trial. Neurorehabilitation and neural repair. 2020;34(9):856-67
33. Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, et al. Guidelines for adult stroke rehabilitation and recovery: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47(6):e98-e169
34. Yuvaraj R, Murugappan M, Mohamed Ibrahim N, Iqbal Omar M, Sundaraj K, Mohamad K, et al. On the analysis of EEG power, frequency and asymmetry in Parkinson’s disease during emotion processing. Behavioral and Brain Functions. 2014;10(1):12.[10.1186/1744-9081-10-12]
35. Ulam F, Shelton C, Richards L, Davis L, Hunter B, Fregni F, et al. Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury. Clinical Neurophysiology. 2015;126(3):486-96
36. Dodd KC, Nair VA, Prabhakaran V. Role of the contralesional vs. ipsilesional hemisphere in stroke recovery. Frontiers in human neuroscience. 2017;11:469
37. Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? The Lancet Neurology. 2006;5(8):708-12
38. van der Cruijsen J, Dooren RF, Schouten AC, Oostendorp TF, Frens MA, Ribbers GM, et al. Addressing the inconsistent electric fields of tDCS by using patient-tailored configurations in chronic stroke: Implications for treatment. NeuroImage: Clinical. 2022;36:103178
39. Salazar CA, Feng W, Bonilha L, Kautz S, Jensen JH, George MS, et al. Transcranial Direct Current Stimulation for Chronic Stroke: Is Neuroimaging the Answer to the Next Leap Forward? Journal of Clinical Medicine. 2023;12(7):2601
40. Wiesman AI, Mills MS, McDermott TJ, Spooner RK, Coolidge NM, Wilson TW. Polarity-dependent modulation of multi-spectral neuronal activity by transcranial direct current stimulation. Cortex. 2018;108:222-33
41. McDermott TJ, Wiesman AI, Mills MS, Spooner RK, Coolidge NM, Proskovec AL, et al. tDCS modulates behavioral performance and the neural oscillatory dynamics serving visual selective attention. Human brain mapping. 2019;40(3):729-40.[10.1002/hbm.24405]
42. Dutta A. Simultaneous functional near-infrared spectroscopy (fNIRS) and electroencephalogram (EEG) to elucidate neurovascular modulation by transcranial electrical stimulation (tES). Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation. 2021;14(5):1093-4
43. Seibt O, Brunoni AR, Huang Y, Bikson M. The pursuit of DLPFC: non-neuronavigated methods to target the left dorsolateral pre-frontal cortex with symmetric bicephalic transcranial direct current stimulation (tDCS). Brain stimulation. 2015;8(3):590-602
44. Zakaria H, Valentine O, Mayza A. Analysis of quantitative EEG (QEEG) parameters on the effect of transcranial direct current stimulation (TDCS) on post-stroke patients. AIP Conference Proceedings. 2021;2344(1):050001.[10.1063/5.0047216]
| Issue | Articles in Press | |
| Section | Research Article(s) | |
| Keywords | ||
| Electroencephalography, stroke, Task, transcranial direct current stimulation, Upper Extremity | ||
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How to Cite
1.
Zolghadr M, Dehkordi S, Sarrafzadeh J, Talebian S, Haddadzade niri H, Yassin M. The Impact of Transcranial Direct Current Stimulation Combined with Task-Oriented Training on EEG-Based Measures of Motor Recovery in Chronic Stroke: A Randomized Clinical Trial Study. jmr. 2024;(-).
