Effects of motor imagery-based neurofeedback training after bilateral repetitive transcranial magnetic stimulation on post-stroke upper limb motor function: an exploratory crossover clinical trial

Authors

  • Francisco José Sánchez Cuesta Faculty of Experimental Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Injury and Movement Disorders Neurorehabilitation Group (GINDAT), Institute of Life Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain https://orcid.org/0000-0001-6202-7071
  • Yeray González-Zamorano Brain Injury and Movement Disorders Neurorehabilitation Group (GINDAT), Institute of Life Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Department of Physiotherapy, Occupational Therapy, Rehabilitation and Physical Medicine, King Juan Carlos University, Alcorcón, Spain; Cognitive Neuroscience, Pain, and Rehabilitation Research Group (NECODOR), Faculty of Health Sciences, Rey Juan Carlos University, Madrid, Spain https://orcid.org/0000-0003-3819-3090
  • Marcos Moreno-Verdú Faculty of Experimental Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Injury and Movement Disorders Neurorehabilitation Group (GINDAT), Institute of Life Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain https://orcid.org/0000-0002-9726-8518
  • Athanasios Vourvopoulos Institute for Systems and Robotics-Lisboa, Department of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, Portugal https://orcid.org/0000-0001-9676-8599
  • Ignacio J. Serrano Neural and Cognitive Engineering group, Centre for Automation and Robotics (CAR) CSIC-UPM, Arganda del Rey, Madrid, Spain https://orcid.org/0000-0002-9333-1305
  • Maria Dolores Del Castillo-Sobrino Neural and Cognitive Engineering group, Centre for Automation and Robotics (CAR) CSIC-UPM, Arganda del Rey, Madrid, Spain https://orcid.org/0000-0002-9366-4484
  • Patrícia Figueiredo Institute for Systems and Robotics-Lisboa, Department of Bioengineering, Instituto Superior Técnico, Universidade de Lisboa, Lisbon, Portugal https://orcid.org/0000-0002-0743-0869
  • Juan Pablo Romero Faculty of Experimental Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Injury and Movement Disorders Neurorehabilitation Group (GINDAT), Institute of Life Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Damage Unit, Beata María Ana Hospital, Madrid, Spain https://orcid.org/0000-0002-3190-1296

DOI:

https://doi.org/10.2340/jrm.v56.18253

Keywords:

repetitive transcranial magnetic stimulation, rTMS, motor imagery, neurofeedback, stroke, motor cortex, upper limb

Abstract

Objective: To examine the clinical effects of combining motor imagery-based neurofeedback training with bilateral repetitive transcranial magnetic stimulation for upper limb motor function in subacute and chronic stroke.

Design: Clinical trial following an AB/BA crossover design with counterbalanced assignment.

Subjects: Twenty individuals with subacute (n = 4) or chronic stroke (n = 16).

Methods: Ten consecutive sessions of bilateral repetitive transcranial magnetic stimulation alone (therapy A) were compared vs a combination of10 consecutive sessions of bilateral repetitive transcranial magnetic stimulation with 12 non-consecutive sessions of motor imagery-based neurofeedback training (therapy B). Patients received both therapies (1-month washout period), in sequence AB or BA. Participants were assessed before and after each therapy and at 15-days follow-up, using the Fugl-Meyer Assessment-upper limb, hand-grip strength, and the Nottingham Sensory Assessment as primary outcome measures.

Results: Both therapies resulted in improved functionality and sensory function. Therapy B consistently exhibited superior effects compared with therapy A, according to Fugl-Meyer Assessment and tactile and kinaesthetic sensory function across multiple time-points, irrespective of treatment sequence. No statistically significant differences between therapies were found for hand-grip strength.

Conclusion: Following subacute and chronic stroke, integrating bilateral repetitive transcranial magnetic stimulation and motor imagery-based neurofeedback training has the potential to enhance functional performance compared with using bilateral repetitive transcranial magnetic stimulation alone in upper limb recovery.

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Author Biography

Juan Pablo Romero, Faculty of Experimental Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Injury and Movement Disorders Neurorehabilitation Group (GINDAT), Institute of Life Sciences, Francisco de Vitoria University, Pozuelo de Alarcón, Spain; Brain Damage Unit, Beata María Ana Hospital, Madrid, Spain

Principal Investigator of GINDAT research group

References

Vena AB, Cabré X, Piñol R, Molina J, Purroy F. Evaluation of the incidence and trend of cerebrovascular disease in the health region of Lleida (Spain) in the period 2010-2014. Neurología 2022; 37: 631-638. DOI: https://doi.org/10.1016/j.nrleng.2019.10.010

https://doi.org/10.1016/j.nrl.2019.10.012 DOI: https://doi.org/10.1016/j.nrl.2019.10.012

Park S, Park JY. Grip strength in post-stroke hemiplegia. J Phys Ther Sci 2016; 28: 677-679.

https://doi.org/10.1589/jpts.28.677 DOI: https://doi.org/10.1589/jpts.28.677

Virani SS, Alonso A, Benjamin EJ, Bittencourt MS, Callaway CW, Carson AP, et al. Heart Disease and Stroke Statistics- 2020 update: a report from the American Heart Association. Circulation 2020; 141: 139-596. DOI: https://doi.org/10.1161/CIR.0000000000000746

https://doi.org/10.1161/CIR.0000000000000757 DOI: https://doi.org/10.1161/CIR.0000000000000757

Buma F, Kwakkel G, Ramsey N. Understanding upper limb recovery after stroke. Restor Neurol Neurosci 2013; 31: 707-722.

https://doi.org/10.3233/RNN-130332 DOI: https://doi.org/10.3233/RNN-130332

Kwakkel G, Kollen BJ, van der Grond J, Prevo AJH. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke 2003; 34: 2181-2186.

https://doi.org/10.1161/01.STR.0000087172.16305.CD DOI: https://doi.org/10.1161/01.STR.0000087172.16305.CD

Alia C, Spalletti C, Lai S, Panarese A, Lamola G, Bertolucci F, et al. Neuroplastic changes following brain ischemia and their contribution to stroke recovery: novel approaches in neurorehabilitation. Front Cell Neurosci 2017; 11: 76

https://doi.org/10.3389/fncel.2017.00076 DOI: https://doi.org/10.3389/fncel.2017.00076

Starosta M, Cichon N, Saluk-Bijak J, Miller E. Benefits from repetitive transcranial magnetic stimulation in post-stroke rehabilitation. J Clin Med 2022; 11: 2149.

https://doi.org/10.3390/jcm11082149 DOI: https://doi.org/10.3390/jcm11082149

Pichiorri F, Morone G, Petti M, Toppi J, Pisotta I, Molinari M, et al. Brain-computer interface boosts motor imagery practice during stroke recovery. Ann Neurol 2015; 77: 851-865.

https://doi.org/10.1002/ana.24390 DOI: https://doi.org/10.1002/ana.24390

Ramos-Murguialday A, Curado MR, Broetz D, Yilmaz O, Brasil FL, Liberati G, et al. Brain-machine interface in chronic stroke: randomized trial long-term follow-up. Neurorehabil Neural Repair 2019; 33: 188-198.

https://doi.org/10.1177/1545968319827573 DOI: https://doi.org/10.1177/1545968319827573

Mihara M, Hattori N, Hatakenaka M, Yagura H, Kawano T, Hino T, et al. Near-infrared spectroscopy-mediated neurofeedback enhances efficacy of motor imagery-based training in poststroke victims: a pilot study. Stroke 2013; 44: 1091-1098.

https://doi.org/10.1161/STROKEAHA.111.674507 DOI: https://doi.org/10.1161/STROKEAHA.111.674507

Saikaley M, Pauli G, Sun H, Serra JR, Iruthayarajah J, Teasell R. Network meta-analysis of non-conventional therapies for improving upper limb motor impairment poststroke. Stroke 2022; 53: 3717-3727.

https://doi.org/10.1161/STROKEAHA.122.040687 DOI: https://doi.org/10.1161/STROKEAHA.122.040687

Hsu WY, Cheng CH, Liao KK, Lee IH, Lin YY. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke 2012; 43: 1849-1857.

https://doi.org/10.1161/STROKEAHA.111.649756 DOI: https://doi.org/10.1161/STROKEAHA.111.649756

Sharma N, Pomeroy VM, Baron JC. Motor imagery - a backdoor to the motor system after stroke? Stroke 2006; 37: 1941-1952.

https://doi.org/10.1161/01.STR.0000226902.43357.fc DOI: https://doi.org/10.1161/01.STR.0000226902.43357.fc

Sitaram R, Ros T, Stoeckel L, Haller S, Scharnowski F, Lewis-Peacock J, et al. Closed-loop brain training: the science of neurofeedback. Nat Rev Neurosci 2017; 18: 86-100.

https://doi.org/10.1038/nrn.2016.164 DOI: https://doi.org/10.1038/nrn.2016.164

Sanders ZB, Fleming MK, Smejka T, Marzolla MC, Zich C, Rieger SW, et al. Self-modulation of motor cortex activity after stroke: a randomized controlled trial. Brain 2022; 145: 3391-3404.

https://doi.org/10.1093/brain/awac239 DOI: https://doi.org/10.1093/brain/awac239

Dwan K, Li T, Altman DG, Elbourne D. CONSORT 2010 statement: extension to randomized crossover trials. BMJ 2019; 366: 4378.

https://doi.org/10.1136/bmj.l4378 DOI: https://doi.org/10.1136/bmj.l4378

Hirakawa Y, Takeda K, Tanabe S, Koyama S, Motoya I, Sakurai H, et al. Effect of intensive motor training with repetitive transcranial magnetic stimulation on upper limb motor function in chronic post-stroke patients with severe upper limb motor impairment. Top Stroke Rehabil 2018; 25: 321-325.

https://doi.org/10.1080/10749357.2018.1466971 DOI: https://doi.org/10.1080/10749357.2018.1466971

Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 2013; 4: 863.

https://doi.org/10.3389/fpsyg.2013.00863 DOI: https://doi.org/10.3389/fpsyg.2013.00863

Aranciva F, Casals-Coll M, Sánchez-Benavides G, Quintana M, Manero RM, Rognoni T, et al. Spanish normative studies in young adult population: norms for the Boston Naming Test and the Token Test. Neurología 2012; 27: 394-399. DOI: https://doi.org/10.1016/j.nrleng.2011.12.010

https://doi.org/10.1016/j.nrl.2011.12.016 DOI: https://doi.org/10.1016/j.nrl.2011.12.016

Zhang Z, Fang Q, Gu X. Fuzzy inference system based automatic Brunnstrom stage classification for upper-extremity rehabilitation. Expert Syst Appl 2014; 41: 1973-1980.

https://doi.org/10.1016/j.eswa.2013.08.094 DOI: https://doi.org/10.1016/j.eswa.2013.08.094

Takeuchi N, Tada T, Toshima M, Matsuo Y, Ikoma K. Repetitive transcranial magnetic stimulation over bilateral hemispheres enhances motor function and training effect of paretic hand in patients after stroke. J Rehabil Med 2009; 41: 1049-1054.

https://doi.org/10.2340/16501977-0454 DOI: https://doi.org/10.2340/16501977-0454

Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015; 126: 1071-1107.

https://doi.org/10.1016/j.clinph.2015.02.001 DOI: https://doi.org/10.1016/j.clinph.2015.02.001

Rossi S, Antal A, Bestmann S, Bikson M, Brewer C, Brockmöller J, et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: expert guidelines. Clin Neurophysiol 2021; 132: 269-306.

https://doi.org/10.1016/j.clinph.2020.10.003 DOI: https://doi.org/10.1016/j.clinph.2020.10.003

Renard Y, Lotte F, Gibert G, Congedo M, Maby E, Delannoy V, et al. OpenViBE: An open-source software platform to design, test and use brain-computer interfaces in real and virtual environments. Presence Teleoperators Virtual 2010; 19: 35-53.

https://doi.org/10.1162/pres.19.1.35 DOI: https://doi.org/10.1162/pres.19.1.35

Vourvopoulos A, Ferreira A, Bermúdez i Badia S. NeuRow: an immersive VR environment for motor-imagery training with the use of brain-computer interfaces and vibrotactile feedback. PhyCS 2016; 43-53.

https://doi.org/10.5220/0005939400430053 DOI: https://doi.org/10.5220/0005939400430053

Vourvopoulos A, Jorge C, Abreu R, Figueiredo P, Fernandes JC, Bermúdez i Badia S. Efficacy and brain imaging correlates of an immersive motor imagery BCI-driven VR system for upper limb motor rehabilitation: a clinical case report. Front Hum Neurosci 2019; 13: 244.

https://doi.org/10.3389/fnhum.2019.00244 DOI: https://doi.org/10.3389/fnhum.2019.00244

Hsieh YW, Wu CY, Lin KC, Chang YF, Chen CL, Liu JS. Responsiveness and validity of three outcome measures of motor function after stroke rehabilitation. Stroke 2009; 40: 1386-1391.

https://doi.org/10.1161/STROKEAHA.108.530584 DOI: https://doi.org/10.1161/STROKEAHA.108.530584

Page SJ, Fulk GD, Boyne P. Clinically important differences for the upper-extremity Fugl-Meyer Scale in people with minimal to moderate impairment due to chronic stroke. Phys Ther 2012; 92: 791-798.

https://doi.org/10.2522/ptj.20110009 DOI: https://doi.org/10.2522/ptj.20110009

Ademoyegun AB, Mbada CE, Sonuga OA, Malomo OE, Fatai WA, Aghedo IA. Does grip strength of the less-affected side of ischemic stroke survivors influences performance of self-care activities? Bull Fac Phys Ther 2022; 27: 28.

https://doi.org/10.1186/s43161-022-00090-y DOI: https://doi.org/10.1186/s43161-022-00090-y

Rayegani SM, Raeissadat SA, Sedighipour L, Rezazadeh IM, Bahrami MH, Eliaspour D, et al. Effect of neurofeedback and electromyographic-biofeedback therapy on improving hand function in stroke patients. Top Stroke Rehabil 2014; 21: 137-151.

https://doi.org/10.1310/tsr2102-137 DOI: https://doi.org/10.1310/tsr2102-137

Liepert J, Greiner J, Nedelko V, Dettmers C. Reduced upper limb sensation impairs mental chronometry for motor imagery after stroke: clinical and electrophysiological findings. Neurorehabil Neural Repair 2012; 26: 470-478.

https://doi.org/10.1177/1545968311425924 DOI: https://doi.org/10.1177/1545968311425924

Johansson BB. Current trends in stroke rehabilitation. A review with focus on brain plasticity. Acta Neurol Scand 2011; 123: 147-159.

https://doi.org/10.1111/j.1600-0404.2010.01417.x DOI: https://doi.org/10.1111/j.1600-0404.2010.01417.x

Lin KC, Chuang LL, Wu CY, Hsieh YW, Chang WY. Responsiveness and validity of three dexterous function measures in stroke rehabilitation. J Rehabil Res Dev 2010; 47: 563-571.

https://doi.org/10.1682/JRRD.2009.09.0155 DOI: https://doi.org/10.1682/JRRD.2009.09.0155

Austin D, Jimison H, Hayes T, Mattek N, Kaye J, Pavel M. Measuring motor speed through typing: a surrogate for the finger tapping test. Behav Res Methods 2011; 43: 903-909.

https://doi.org/10.3758/s13428-011-0100-1 DOI: https://doi.org/10.3758/s13428-011-0100-1

Villafañe JH, Taveggia G, Galeri S, Bissolotti L, Mullè C, Imperio G, et al. Efficacy of short-term robot-assisted rehabilitation in patients with hand paralysis after stroke: a randomized clinical trial. Hand (N Y) 2018; 13: 95-102.

https://doi.org/10.1177/1558944717692096 DOI: https://doi.org/10.1177/1558944717692096

Bohannon R. Motricity Index Scores are valid indicators of paretic upper extremity strength following stroke. J Phys Ther Sci 1999; 11: 59-61.

https://doi.org/10.1589/jpts.11.59 DOI: https://doi.org/10.1589/jpts.11.59

Johnson NN, Carey J, Edelman BJ, Doud A, Grande A, Lakshminarayan K, et al. Combined rTMS and virtual reality brain-computer interface training for motor recovery after stroke. J Neural Eng 2018; 15: 016009.

https://doi.org/10.1088/1741-2552/aa8ce3 DOI: https://doi.org/10.1088/1741-2552/aa8ce3

Chen YH, Chen CL, Huang YZ, Chen HC, Chen CY, Wu CY, et al. Augmented efficacy of intermittent theta burst stimulation on the virtual reality-based cycling training for upper limb function in patients with stroke: a double-blinded, randomized controlled trial. J NeuroEngineering Rehabil 2021; 18: 91.

https://doi.org/10.1186/s12984-021-00885-5 DOI: https://doi.org/10.1186/s12984-021-00885-5

Hung CT, Croft EA, Van der Loos HFM. A wearable vibrotactile device for upper-limb bilateral motion training in stroke rehabilitation: a case study. Annu Int Conf IEEE Eng Med Biol Soc 2015; 2015: 3480-3483.

Perez-Marcos D, Chevalley O, Schmidlin T, Garipelli G, Serino A, Vuadens P, et al. Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study. J Neuroengineering Rehabil 2017; 14: 119.

https://doi.org/10.1186/s12984-017-0328-9 DOI: https://doi.org/10.1186/s12984-017-0328-9

Pundik S, McCabe JP, Hrovat K, Fredrickson AE, Tatsuoka C, Feng IJ, et al. Recovery of post-stroke proximal arm function, driven by complex neuroplastic bilateral brain activation patterns and predicted by baseline motor dysfunction severity. Front Hum Neurosci 2015; 9: 394.

https://doi.org/10.3389/fnhum.2015.00394 DOI: https://doi.org/10.3389/fnhum.2015.00394

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Published

2024-03-07

How to Cite

Sánchez Cuesta, F. J. ., González-Zamorano, Y. ., Moreno-Verdú, M., Vourvopoulos, A., Serrano, I. J., Del Castillo-Sobrino, M. D. ., Figueiredo, P., & Romero, J. P. . (2024). Effects of motor imagery-based neurofeedback training after bilateral repetitive transcranial magnetic stimulation on post-stroke upper limb motor function: an exploratory crossover clinical trial. Journal of Rehabilitation Medicine, 56, jrm18253. https://doi.org/10.2340/jrm.v56.18253

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Vol. 56 (2024)

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Copyright (c) 2024 Francisco José Sánchez Cuesta, Yeray González-Zamorano, Marcos Moreno-Verdú, Athanasios Vourvopoulos, Ignacio J. Serrano; Maria Dolores Del Castillo-Sobrino; Patrícia Figueiredo, Juan Pablo Romero

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