Combined Transcranial Direct Current Stimulation and Virtual Reality-Based Paradigm for Upper Limb Rehabilitation in Individuals with Restricted Movements. A Feasibility Study with a Chronic Stroke Survivor with Severe Hemiparesis

  • María Antonia Fuentes
  • Adrián Borrego
  • Jorge Latorre
  • Carolina Colomer
  • Mariano Alcañiz
  • María José Sánchez-LedesmaEmail author
  • Enrique Noé
  • Roberto Llorens
Patient Facing Systems
Part of the following topical collections:
  1. Emergent Visualization Systems in Biomedical Sciences (TEEM 2017)


Impairments of the upper limb function are a major cause of disability and rehabilitation. Most of the available therapeutic options are based on active exercises and on motor and attentional inclusion of the affected arm in task oriented movements. However, active movements may not be possible after severe impairment of the upper limbs. Different techniques, such as mirror therapy, motor imagery, and non-invasive brain stimulation have been shown to elicit cortical activity in absence of movements, which could be used to preserve the available neural circuits and promote motor learning. We present a virtual reality-based paradigm for upper limb rehabilitation that allows for interaction of individuals with restricted movements from active responses triggered when they attempt to perform a movement. The experimental system also provides multisensory stimulation in the visual, auditory, and tactile channels, and transcranial direct current stimulation coherent to the observed movements. A feasibility study with a chronic stroke survivor with severe hemiparesis who seemed to reach a rehabilitation plateau after two years of its inclusion in a physical therapy program showed clinically meaningful improvement of the upper limb function after the experimental intervention and maintenance of gains in both the body function and activity. The experimental intervention also was reported to be usable and motivating. Although very preliminary, these results could highlight the potential of this intervention to promote functional recovery in severe impairments of the upper limb.


Virtual reality tDCS Eye-tracking Surface electromyography Upper limb paresis Monoparesis, stroke 



This study was funded in part by Ministerio de Economía y Competitividad of Spain (Project TIN2014–61975-EXP and Grant BES-2014-068218) and by Universitat Politècnica de València (Grant PAID-10-14 and Grant PAID-10-16).

Compliance with Ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.


  1. 1.
    Invernizzi, M., Negrini, S., Da, S. C., Lanzotti, L., Cisari, C., and Baricich, A., The value of adding mirror therapy for upper limb motor recovery of subacute stroke patients: A randomized controlled trial. Eur. J. Phys. Rehabil. Med. 49:311–317, 2013.PubMedGoogle Scholar
  2. 2.
    Park, Y., Chang, M., Kim, K.-M., and An, D.-H., The effects of mirror therapy with tasks on upper extremity function and self-care in stroke patients. J. Phys. Ther. Sci. 27:1499–1501, 2015. Scholar
  3. 3.
    Pollock, A., Farmer, S. E., Brady, M. C., Langhorne, P., Mead, G. E., Mehrholz, J., and van Wijck, F., Interventions for improving upper limb function after stroke. Cochrane Database Syst. Rev. 11, 2014.
  4. 4.
    Barker, R. N., Gill, T. J., and Brauer, S. G., Factors contributing to upper limb recovery after stroke: A survey of stroke survivors in Queensland Australia. Disabil. Rehabil. 29:981–989, 2007. Scholar
  5. 5.
    Bayona, N. A., Bitensky, J., Salter, K., and Teasell, R., The role of task-specific training in rehabilitation therapies. Top. Stroke Rehabil. 12:58–65, 2005. Scholar
  6. 6.
    Coupar, F., Pollock, A., Rowe, P., Weir, C., and Langhorne, P., Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin. Rehabil. 26:291–313, 2012. Scholar
  7. 7.
    Hunter, S. M., Crome, P., Sim, J., and Pomeroy, V. M., Effects of Mobilization and Tactile Stimulation on Recovery of the Hemiplegic Upper Limb: A Series of Replicated Single-System Studies. Arch. Phys. Med. Rehabil. 89:2003–2010, 2008. Scholar
  8. 8.
    Colomer, C., Noé, E., and Llorens, R., Mirror therapy in chronic stroke survivors with severely impaired upper limb function: A randomized controlled trial. Eur. J. Phys. Rehabil. Med. 52:271–278, 2016.PubMedGoogle Scholar
  9. 9.
    Lum, P. S., Mulroy, S., Amdur, R. L., Requejo, P., Prilutsky, B. I., and Dromerick, A. W., Gains in upper extremity function after stroke via recovery or compensation: Potential differential effects on amount of real-world limb use. Top. Stroke Rehabil. 16:237–253, 2009. Scholar
  10. 10.
    Taub, E., Uswatte, G., Mark, V. W., and Morris, D. M. M., The learned nonuse phenomenon: implications for rehabilitation. Eura. Medicophys. 42:241–256, 2006.PubMedGoogle Scholar
  11. 11.
    Deconinck, F. J. A., Smorenburg, A. R. P., Benham, A., Ledebt, A., Feltham, M. G., and Savelsbergh, G. J. P., Reflections on Mirror Therapy: A Systematic Review of the Effect of Mirror Visual Feedback on the Brain. Neurorehabil. Neural Repair. 29:349–361, 2014. Scholar
  12. 12.
    Lindberg, P. G., Schmitz, C., Engardt, M., Forssberg, H., and Borg, J., Use-dependent up- and down-regulation of sensorimotor brain circuits in stroke patients. Neurorehabil. Neural Repair. 21:315–326, 2007. Scholar
  13. 13.
    Thieme, H., Bayn, M., Wurg, M., Zange, C., Pohl, M., and Behrens, J., Mirror therapy for patients with severe arm paresis after stroke--a randomized controlled trial. Clin. Rehabil. 27:314–324, 2013. Scholar
  14. 14.
    Dettmers, C., Benz, M., Liepert, J., and Rockstroh, B., Motor imagery in stroke patients, or plegic patients with spinal cord or peripheral diseases. Acta Neurol. Scand. 126:238–247, 2012. Scholar
  15. 15.
    Kimberley, T. J., Khandekar, G., Skraba, L. L., Spencer, J. A., Van Gorp, E. A., and Walker, S. R., Neural substrates for motor imagery in severe hemiparesis. Neurorehabil. Neural Repair. 20:268–277, 2006. Scholar
  16. 16.
    Pascual-Leone, A., The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. J. Neurol. Neurosurg. Psychiatry. 82:393–398, 2011. Scholar
  17. 17.
    Gatti, R., Rocca, M. A., Fumagalli, S., Cattrysse, E., Kerckhofs, E., Falini, A., and Filippi, M., The effect of action observation/execution on mirror neuron system recruitment: an fMRI study in healthy individuals. Brain Imaging Behav. 11:565–576, 2017. Scholar
  18. 18.
    Bonato, C., Miniussi, C., and Rossini, P. M., Transcranial magnetic stimulation and cortical evoked potentials: A TMS/EEG co-registration study. Clin. Neurophysiol. 117:1699–1707, 2006. Scholar
  19. 19.
    Grundmann, L., Rolke, R., Nitsche, M. A., Pavlakovic, G., Happe, S., Treede, R. D., Paulus, W., and Bachmann, C. G., Effects of transcranial direct current stimulation of the primary sensory cortex on somatosensory perception. Brain Stimul. 4:253–260, 2011. Scholar
  20. 20.
    von Rein, E., Hoff, M., Kaminski, E., Sehm, B., Steele, C. J., Villringer, A., and Ragert, P., Improving motor performance without training: the effect of combining mirror visual feedback with transcranial direct current stimulation. J. Neurophysiol. 113:2383–2389, 2015. Scholar
  21. 21.
    Kim, Y. J., Ku, J., Cho, S., Kim, H. J., Cho, Y. K., Lim, T., and Kang, Y. J., Facilitation of corticospinal excitability by virtual reality exercise following anodal transcranial direct current stimulation in healthy volunteers and subacute stroke subjects. J. Neuroeng. Rehabil. 11:124, 2014. Scholar
  22. 22.
    S. Bermúdez i Badia, G.G. Fluet, R. Llorens, J.E. Deutsch, Virtual Reality for Sensorimotor Rehabilitation Post Stroke: Design Principles and Evidence. In: Neurorehabilitation Technol., Second edi, Springer, 2016: pp. 573–603.
  23. 23.
    Im, H., Ku, J., Kim, H. J., and Kang, Y. J., Virtual reality-guided motor imagery increases corticomotor excitability in healthy volunteers and stroke patients. Ann. Rehabil. Med. 40:420–431, 2016. Scholar
  24. 24.
    Colomer, C., Llorens, R., Noé, E., and Alcañiz, M., Effect of a mixed reality-based intervention on arm, hand, and finger function on chronic stroke. J. Neuroeng. Rehabil. 13, 2016.
  25. 25.
    Grimm, F., Naros, G., and Gharabaghi, A., Closed-Loop Task Difficulty Adaptation during Virtual Reality Reach-to-Grasp Training Assisted with an Exoskeleton for Stroke Rehabilitation. Front. Neurosci. 10:518, 2016. Scholar
  26. 26.
    Poole, A., and Ball, L. J., Eye Tracking in Human-Computer Interaction and Usability Research: Current Status and Future Prospects. Encycl. Human-Computer Interact.:211–219, 2005.
  27. 27.
    R. Merletti, A. Botter, A. Troiano, E. Merlo, M.A. Minetto, Technology and instrumentation for detection and conditioning of the surface electromyographic signal: State of the art, Clin. Biomech. 24 (2009) 122–134.
  28. 28.
    Trojano, L., Moretta, P., Loreto, V., Cozzolino, A., Santoro, L., and Estraneo, A., Quantitative assessment of visual behavior in disorders of consciousness. J. Neurol. 259:1888–1895, 2012. Scholar
  29. 29.
    Trojano, L., Moretta, P., Loreto, V., Santoro, L., and Estraneo, A., Affective saliency modifies visual tracking behavior in disorders of consciousness: A quantitative analysis. J. Neurol. 260:306–308, 2013. Scholar
  30. 30.
    Sanford, J., Moreland, J., Swanson, L. R., Stratford, P. W., and Gowland, C., Reliability of the Fugl-Meyer assessment for testing motor performance in patients following stroke. Phys. Ther. 73:447–454, 1993. Scholar
  31. 31.
    Lang, C. E., Edwards, D. F., Birkenmeier, R. L., and Dromerick, A. W., Estimating Minimal Clinically Important Differences of Upper-Extremity Measures Early After Stroke. Arch. Phys. Med. Rehabil. 89:1693–1700, 2008. Scholar
  32. 32.
    Brooke, J., SUS - A quick and dirty usability scale. Usability Eval. Ind. 189:4–7, 1996. Scholar
  33. 33.
    McAuley, E., Duncan, T., and Tammen, V. V., Psychometric Properties of the Intrinsic Motivation Inventory in a Competitive Sport Setting: A Confirmatory Factor Analysis. Res. Q. Exerc. Sport. 60:48–58, 1989. Scholar
  34. 34.
    Page, S. J., Fulk, G. D., and 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. 92:791–798, 2012. Scholar
  35. 35.
    R. Teasell, Evidence-Based Review of Stroke Rehabilitation - Background Concepts in Stroke Rehabilitation, 2016.
  36. 36.
    Cameirão, M. S., Badia, S. B. I., Duarte, E., Frisoli, A., and Verschure, P. F. M. J., The combined impact of virtual reality neurorehabilitation and its interfaces on upper extremity functional recovery in patients with chronic stroke. Stroke. 43:2720–2728, 2012. Scholar
  37. 37.
    K.E. Laver, S. George, S. Thomas, J.E. Deutsch, M. Crotty, Virtual reality for stroke rehabilitation. In: Cochrane Database Syst. Rev., 2015: pp. 1–107.
  38. 38.
    Lefebvre, S., Laloux, P., Peeters, A., Desfontaines, P., Jamart, J., and Vandermeeren, Y., Dual-tDCS Enhances Online Motor Skill Learning and Long-Term Retention in Chronic Stroke Patients. Front. Hum. Neurosci. 6:343, 2012. Scholar
  39. 39.
    Lindenberg, R., Renga, V., Zhu, L. L., Nair, D., and Schlaug, G., Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 75:2176–2184, 2010. Scholar
  40. 40.
    K. Figlewski, J.U. Blicher, J. Mortensen, K.E. Severinsen, J.F. Nielsen, H. Andersen, Transcranial Direct Current Stimulation Potentiates Improvements in Functional Ability in Patients With Chronic Stroke Receiving Constraint-Induced Movement Therapy, Stroke. (2016).
  41. 41.
    Lee, S. J., and Chun, M. H., Combination transcranial direct current stimulation and virtual reality therapy for upper extremity training in patients with subacute stroke. Arch. Phys. Med. Rehabil. 95:431–438, 2014. Scholar
  42. 42.
    Viana, R. T., Laurentino, G. E. C., Souza, R. J. P., Fonseca, J. B., Silva Filho, E. M., Dias, S. N., Teixeira-Salmela, L. F., and Monte-Silva, K. K., Effects of the addition of transcranial direct current stimulation to virtual reality therapy after stroke: A pilot randomized controlled trial. NeuroRehabilitation. 34:437–446, 2014. Scholar
  43. 43.
    Sigrist, R., Rauter, G., Riener, R., and Wolf, P., Augmented visual, auditory, haptic, and multimodal feedback in motor learning: A review. Psychon. Bull. Rev. 20:21–53, 2013. Scholar
  44. 44.
    Bowering, K. J., O’Connell, N. E., Tabor, A., Catley, M. J., Leake, H. B., Moseley, G. L., and Stanton, T. R., The Effects of Graded Motor Imagery and Its Components on Chronic Pain: A Systematic Review and Meta-Analysis. J. Pain. 14:3–13, 2013. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • María Antonia Fuentes
    • 1
  • Adrián Borrego
    • 2
  • Jorge Latorre
    • 2
  • Carolina Colomer
    • 1
  • Mariano Alcañiz
    • 2
  • María José Sánchez-Ledesma
    • 3
    Email author
  • Enrique Noé
    • 1
  • Roberto Llorens
    • 1
    • 2
  1. 1.Servicio de Neurorrehabilitación y Daño Cerebral de los Hospitales VITHAS-NISAFundación Hospitales NISAValenciaSpain
  2. 2.Neurorehabilitation and Brain Research Group, Instituto de Investigación e Innovación en BioingenieríaUniversitat Politècnica de ValènciaValenciaSpain
  3. 3.VisualMed Systems GroupUniversity of SalamancaSalamancaSpain

Personalised recommendations