Non-invasive electrical brain stimulation for vision restoration after stroke: An exploratory randomized trial (REVIS)
Silja Räty, Carolin Borrmann, Giuseppe Granata, Lizbeth Cárdenas-Morales, Ariel Schoenfeld, Michael Sailer, Katri Silvennoinen, Juha Holopainen, Francesca De Rossi, Andrea Antal, Paolo M Rossini, Turgut Tatlisumak, Bernhard A Sabel, Silja Räty, Carolin Borrmann, Giuseppe Granata, Lizbeth Cárdenas-Morales, Ariel Schoenfeld, Michael Sailer, Katri Silvennoinen, Juha Holopainen, Francesca De Rossi, Andrea Antal, Paolo M Rossini, Turgut Tatlisumak, Bernhard A Sabel
Abstract
Background: Occipital strokes often cause permanent homonymous hemianopia leading to significant disability. In previous studies, non-invasive electrical brain stimulation (NIBS) has improved vision after optic nerve damage and in combination with training after stroke.
Objective: We explored different NIBS modalities for rehabilitation of hemianopia after chronic stroke.
Methods: In a randomized, double-blinded, sham-controlled, three-armed trial, altogether 56 patients with homonymous hemianopia were recruited. The three experiments were: i) repetitive transorbital alternating current stimulation (rtACS, n = 8) vs. rtACS with prior cathodal transcranial direct current stimulation over the intact visual cortex (tDCS/rtACS, n = 8) vs. sham (n = 8); ii) rtACS (n = 9) vs. sham (n = 9); and iii) tDCS of the visual cortex (n = 7) vs. sham (n = 7). Visual functions were evaluated before and after the intervention, and after eight weeks follow-up. The primary outcome was change in visual field assessed by high-resolution and standard perimetries. The individual modalities were compared within each experimental arm.
Results: Primary outcomes in Experiments 1 and 2 were negative. Only significant between-group change was observed in Experiment 3, where tDCS increased visual field of the contralesional eye compared to sham. tDCS/rtACS improved dynamic vision, reading, and visual field of the contralesional eye, but was not superior to other groups. rtACS alone increased foveal sensitivity, but was otherwise ineffective. All trial-related procedures were tolerated well.
Conclusions: This exploratory trial showed safety but no main effect of NIBS on vision restoration after stroke. However, tDCS and combined tDCS/rtACS induced improvements in visually guided performance that need to be confirmed in larger-sample trials.NCT01418820 (clinicaltrials.gov).
Keywords: Electrical stimulation; homonymous hemianopia; occipital stroke; randomized controlled trial; rehabilitation; vision restoration.
Conflict of interest statement
BS is a shareholder of SAVIR-Center, a vision rehabilitation outpatient clinic, where NIBS methods are used. Other authors have no disclosures.
Figures
References
- Alber, R., Moser, H., Gall, C., & Sabel, B. A. (2017). Combined transcranial direct current stimulation and Vision Restoration training in subacute stroke rehabilitation: A Pilot study. PM & R, 9(8), 787–794.
- Ali, M., Hazelton, C., Lyden, P., Pollock, A., & Brady, M. (2013). Recovery from poststroke visual impairment: Evidence from a clinical trials resource. Neurorehabilitation and Neural Repair, 27(2), 133–141.
- Antal, A., Alekseichuk, I., Bikson, M., Brockmöller, J., Brunoni, A. R., Chen, R.,... Paulus, W. (2017). Low intensity transcranial electric stimulation: Safety, ethical, legal regulatory and application guidelines. Clinical Neurophysiology, 128(9), 1774–1809.
- Antal, A., Boros, K., Poreisz, C., Chaieb, L., Terney, D., & Paulus, W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimulation, 1(2), 97–105.
- Bola, M., Gall, C., Moewes, C., Fedorov, A., Hinrichs, H., & Sabel, B. A. (2014). Brain functional connectivity network breakdown and restoration in blindness. Neurology, 83(6), 542–551.
- Dougherty, B. E., Flom, R. E., & Bullimore, M. A. (2005). An evaluation of the MARS letter contrast sensitivity test. Optometry and Vision Science, 82(11), 970–975.
- Foik, A. T., Kublik, E., Sergeeva, E. G., Tatlisumak, T., Rossini, P. M., Sabel, B. A., & Waleszczyk, W. J. (2015). Retinal origin of electrically evoked potentials in response to transcorneal alternating current stimulation in the rat. Investigative Ophthalmology & Visual Science, 56(3), 1711–1718.
- Gall, C., Franke, G. H., & Sabel, B. A. (2010). Vision-related quality of life in first stroke patients with homonymous visual field defects. Health & Quality of Life Outcomes, 8, 33.
- Gall, C., Schmidt, S., Schittkowski, M. P., Antal, A., Ambrus, G. G., Paulus, W.,... Sabel, B. A. (2016). Alternating current stimulation for vision restoration after optic nerve damage: A randomized clinical trial. PloS One, 11(6), e0156134.
- Gall, C., Silvennoinen, K., Granata, G., de Rossi, F., Vecchio, F., Brosel, D.,... Sabel, B. A. (2015). Non-invasive electric current stimulation for restoration of vision after unilateral occipital stroke. Contemporary Clinical Trials, 43, 231–236.
- Gray, C. S., French, J. M., Bates, D., Cartlidge, N. E., Venables, G. S., & James, O. F. (1989). Recovery of visual fields in acute stroke: Homonymous hemianopia associated with adverse prognosis. Age & Ageing, 18(6), 419–421.
- Halko, M. A., Datta, A., Plow, E. B., Scaturro, J., Bikson, M., & Merabet, L. B. (2011). Neuroplastic changes following rehabilitative training correlate with regional electrical field induced with tDCS. Neuroimage, 57(3), 885–891.
- Herring, J. D., Esterer, S., Marshall, T. R., Jensen, O., & Bergmann, T. O. (2019). Low-frequency alternating current stimulation rhythmically suppresses gamma-band oscillations and impairs perceptual performance. Neuroimage, 184, 440–449.
- Huang, Y. Y., Colino, A., Selig, D. K., & Malenka, R. C. (1992). The influence of prior synaptic activity on the induction of long-term potentiation. Science, 255(5045), 730–733.
- Kanai, R., Chaieb, L., Antal, A., Walsh, V., & Paulus, W. (2008). Frequency-dependent electrical stimulation of the visual cortex. Current Biology, 18(23), 1839–1843.
- Kasten, E., Wust, S., Behrens-Baumann, W., & Sabel, B. A. (1998). Computer-based training for the treatment of partial blindness. Nature Medicine, 4(9), 1083–1087.
- Lang, N., Siebner, H. R., Ernst, D., Nitsche, M. A., Paulus, W., Lemon, R. N., & Rothwell, J. C. (2004). Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biological Psychiatry, 56(9), 634–639.
- Larcombe, S. J., Kulyomina, Y., Antonova, N., Ajina, S., Stagg, C. J., Clatworthy, P. L., & Bridge, H. (2018). Visual training in hemianopia alters neural activity in the absence of behavioural improvement: A pilot study. Ophthalmic & Physiological Optics, 38(5), 538–549.
- Matteo, B. M., Viganò, B., Cerri, C. G., Meroni, R., Cornaggia, C. M., & Perin, C. (2017). Transcranial direct current stimulation (tDCS) combined with blindsight rehabilitation for the treatment of homonymous hemianopia: A report of two-cases. Journal of Physical Therapy Science, 29(9), 1700–1705.
- Murphy, T. H., & Corbett, D. (2009). Plasticity during stroke recovery: From synapse to behaviour. Nature Reviews Neuroscience, 10(12), 861–872.
- Nitsche, M. A., Cohen, L. G., Wassermann, E. M., Priori, A., Lang, N., Antal, A.,... Pascual-Leone, A. (2008). Transcranial direct current stimulation: State of the art. Brain Stimulation, 1(3), 206–223.
- Ozen, S., Sirota, A., Belluscio, M. A., Anastassiou, C. A., Stark, E., Koch, C., & Buzsáki, G. (2010). Transcranial electric stimulation entrains cortical neuronal populations in rats. The Journal of Neuroscience, 30(34), 11476–11485.
- Plow, E. B., Obretenova, S. N., Fregni, F., Pascual-Leone, A., & Merabet, L. B. (2012). Comparison of visual field training for hemianopia with active versus sham transcranial direct cortical stimulation. Neurorehabilitation and Neural Repair, 26(6), 616–626.
- Plow, E. B., Obretenova, S. N., Halko, M. A., Kenkel, S., Jackson, M. L., Pascual-Leone, A., & Merabet, L. B. (2011). Combining visual rehabilitative training and noninvasive brain stimulation to enhance visual function in patients with hemianopia: A comparative case study. PM & R, 3(9), 825–835.
- Pollock, A., Hazelton, C., Rowe, F. J., Jonuscheit, S., Kernohan, A., Angilley, J.,... Campbell, P. (2019). Interventions for visual field defects in people with stroke. Cochrane Database of Systematic Reviews, (5).
- Poppel, E., Held, R., & Frost, D. (1973). Leter: Residual visual function after brain wounds involving the central visual pathways in man. Nature, 243(5405), 295–296.
- Raninen, A., Vanni, S., Hyvarinen, L., & Nasanen, R. (2007). Temporal sensitivity in a hemianopic visual field can be improved by long-term training using flicker stimulation. Journal of Neurology, Neurosurgery & Psychiatry, 78(1), 66–73.
- Rossini, P. M., Calautti, C., Pauri, F., & Baron, J. (2003). Post-stroke plastic reorganisation in the adult brain. Lancet Neurology, 2(8), 493–502.
- Rowe, F. J., Hepworth, L. R., Howard, C., Hanna, K. L., Cheyne, C. P., & Currie, J. (2019). High incidence and prevalence of visual problems after acute stroke: An epidemiology study with implications for service delivery. PloS One, 14(3), e0213035.
- Sabel, B. A., Henrich-Noack, P., Fedorov, A., & Gall, C. (2011). Vision restoration after brain and retina damage: The “residual vision activation theory”. Progress in Brain Research, 192, 199–262.
- Sabel, B. A., Thut, G., Haueisen, J., Henrich-Noack, P., Herrmann, C. S., Hunold, A.,... Antal, A. (2020). Vision modulation, plasticity and restoration using non-invasive brain stimulation - an IFCN-sponsored review. Clinical Neurophysiology, 131(4), 887–911.
- Sahraie, A., Trevethan, C. T., MacLeod, M. J., Murray, A. D., Olson, J. A., & Weiskrantz, L. (2006). Increased sensitivity after repeated stimulation of residual spatial channels in blindsight. Proceedings of the National Academy of Sciences of the United States of America, 103(40), 14971–14976.
- Strbian, D., Ahmed, N., Wahlgren, N., Kaste, M., Tatlisumak, T., SITS Investigators. (2012). Intravenous thrombolysis in ischemic stroke patients with isolated homonymous hemianopia: Analysis of Safe Implementation of Thrombolysis in Stroke-International Stroke Thrombolysis Register (SITS-ISTR. Stroke, 43(10), 2695–2698.
- Tiel, K., & Kolmel, H. W. (1991). Patterns of recovery from homonymous hemianopia subsequent to infarction in the distribution of the posterior cerebral-artery. Neuro-Ophthalmology, 11(1), 33–39.
- Trauzettel-Klosinski, S., & Dietz, K. (2012). Standardized assessment of reading performance: The new international reading speed texts IReST. Investigative Ophthalmology & Visual Science, 53(9), 5452–5461.
- Weiskrantz, L., Warrington, E. K., Sanders, M. D., & Marshall, J. (1974). Visual capacity in the hemianopic field following a restricted occipital ablation. Brain, 97(4), 709–728.
- Wist, E. R., Ehrenstein, W. H., Schrauf, M., & Schraus, M. (1998). A computer-assisted test for the electrophysiological and psychophysical measurement of dynamic visual function based on motion contrast. Journal of Neuroscience Methods, 80(1), 41–47.
- Zaehle, T., Rach, S., & Herrmann, C. S. (2010). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PloS One, 5(11), e13766.
- Zhang, X., Kedar, S., Lynn, M. J., Newman, N. J., & Biousse, V. (2006). Natural history of homonymous hemianopia. Neurology, 66(6), 901–905.
Source: PubMed