Transcranial direct current stimulation as a motor neurorehabilitation tool: an empirical review

Ana Sánchez-Kuhn, Cristian Pérez-Fernández, Rosa Cánovas, Pilar Flores, Fernando Sánchez-Santed, Ana Sánchez-Kuhn, Cristian Pérez-Fernández, Rosa Cánovas, Pilar Flores, Fernando Sánchez-Santed

Abstract

The present review collects the most relevant empirical evidence available in the literature until date regarding the effects of transcranial direct current stimulation (tDCS) on the human motor function. tDCS in a non-invasive neurostimulation technique that delivers a weak current through the brain scalp altering the cortical excitability on the target brain area. The electrical current modulates the resting membrane potential of a variety of neuronal population (as pyramidal and gabaergic neurons); raising or dropping the firing rate up or down, depending on the nature of the electrode and the applied intensity. These local changes additionally have shown long-lasting effects, evidenced by its promotion of the brain-derived neurotrophic factor. Due to its easy and safe application and its neuromodulatory effects, tDCS has attracted a big attention in the motor neurorehabilitation field among the last years. Therefore, the present manuscript updates the knowledge available about the main concept of tDCS, its practical use, safety considerations, and its underlying mechanisms of action. Moreover, we will focus on the empirical data obtained by studies regarding the application of tDCS on the motor function of healthy and clinical population, comprising motor deficiencies of a variety of pathologies as Parkinson's disease, stroke, multiple sclerosis and cerebral palsy, among others. Finally, we will discuss the main current issues and future directions of tDCS as a motor neurorehabilitation tool.

References

    1. Llinás RR. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science. 1988;242(4886):1654–1664. doi: 10.1126/science.3059497.
    1. Kellaway P. The part played by electric fish in the early history of bioelectricity and electrotherapy. Bull Hist Med. 1946;20(2):112–137. .
    1. Zago S, Ferrucci R, Fregni F, Priori A. Bartholow, Sciamanna, Alberti: pioneers in the electrical stimulation of the exposed human cerebral cortex. Neuroscientist. 2008;14(5):521–528. doi: 10.1177/1073858407311101.
    1. Miniussi C, Paulus W, Rossini P. Transcranial brain stimulation. Boca Raton: CRC Press, Taylor & Francis group; 2012. .
    1. Hershey T, Wu J, Weaver PM, et al. Unilateral vs. bilateral STN DBS effects on working memory and motor function in Parkinson disease. Exp Neurol. 2008;210(2):402–408. doi: 10.1016/j.expneurol.2007.11.011.
    1. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Cañete C, Catalá MD. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol. 1998;15:333–343. doi: 10.1097/00004691-199807000-00005.
    1. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003;2(3):145–156. doi: 10.1016/S1474-4422(03)00321-1.
    1. Espadaler J, Rogić M, Deletis V, Leon A, Quijada C, Conesa G. Representation of cricothyroid muscles at the primary motor cortex (M1) in healthy subjects, mapped by navigated transcranial magnetic stimulation (nTMS) Clin Neurophysiol. 2012;123(11):2205–2211. doi: 10.1016/j.clinph.2012.04.008.
    1. Vitikainen AM, Salli E, Lioumis P, Mäkelä JP, Metsähonkala L. Applicability of nTMS in locating the motor cortical representation areas in patients with epilepsy. Acta Neurochir (Wien) 2013;155(3):507–518. doi: 10.1007/s00701-012-1609-5.
    1. Priori A, Hallett M, Rothwell JC. Repetitive transcranial magnetic stimulation or transcranial direct current stimulation? Brain Stimul. 2009;2(4):241–245. doi: 10.1016/j.brs.2009.02.004.
    1. Zaghi S, Acar M, Hultgren B, Boggio PS, Fregni F. Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist. 2010;16(3):285–307. doi: 10.1177/1073858409336227.
    1. Nitsche MA, Cohen LG, Wassermann EM, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1(3):206–223. doi: 10.1016/j.brs.2008.06.004.
    1. Sriraman A, Oishi T, Madhavan S. Timing-dependent priming effects of tDCS on ankle motor skill learning. Brain Res. 2014;1581:23–29. doi: 10.1016/j.brainres.2014.07.021.
    1. Mendonca ME, Simis M, Grecco LC, Battistella LR, Baptista AF, Fregni F. Transcranial direct current stimulation combined with aerobic exercise to optimize analgesic responses in fibromyalgia: a randomized placebo-controlled clinical trial. Front Hum Neurosci. 2016;10(March):68.
    1. Tortella G, Casati R, Aparicio LVM, et al. Transcranial direct current stimulation in psychiatric disorders. World J Psychiatry. 2015;5(1):88. doi: 10.5498/wjp.v5.i1.88.
    1. Nitsche MA, Boggio PS, Fregni F, Pascual-Leone A. Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp Neurol. 2009;219(1):14–19. doi: 10.1016/j.expneurol.2009.03.038.
    1. Brunelin J, Mondino M, Gassab L, et al. Examining transcranial direct-current stimulation (tDCS) as a treatment for hallucinations in schizophrenia. Am J Psychiatry. 2012;169(7):719–724. doi: 10.1176/appi.ajp.2012.11071091.
    1. Volpato C, Piccione F, Cavinato M, et al. Modulation of affective symptoms and resting state activity by brain stimulation in a treatment-resistant case of obsessive–compulsive disorder. Neurocase. 2013;19(4):360–70. doi: 10.1080/13554794.2012.667131.
    1. Nakamura-Palacios EM, Lopes IBC, Souza RA, et al. Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction. J Neural Transm. 2016
    1. Schjetnan AGP, Faraji J, Metz GA, Tatsuno M, Luczak A. Transcranial direct current stimulation in stroke rehabilitation: a review of recent advancements. Stroke Res Treat. 2013;2013:1–14. doi: 10.1155/2013/170256.
    1. Benninger DH, Lomarev M, Lopez G, et al. Transcranial direct current stimulation for the treatment of Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2010;81(10):1105–1111. doi: 10.1136/jnnp.2009.202556.
    1. Fritsch B, Reis J, Martinowich K, et al. Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron. 2010;66(2):198–204. doi: 10.1016/j.neuron.2010.03.035.
    1. Kuo MF, Paulus W, Nitsche MA. Boosting focally-induced brain plasticity by dopamine. Cereb Cortex. 2008;18(3):648–651. doi: 10.1093/cercor/bhm098.
    1. Faria P, Hallett M, Miranda PC. A finite element analysis of the effect of electrode area and inter-electrode distance on the spatial distribution of the current density in tDCS. J Neural Eng. 2011;8(6):66017. doi: 10.1088/1741-2560/8/6/066017.
    1. Minhas P, Bikson M, Woods AJ, Alyssa R. Rosen A, Kessler SK. NIH Public Access. 2012. doi: 10.1109/EMBC.2012.6346067.Transcranial.
    1. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(Pt 3):633–639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x.
    1. Rroji O, Van Kuyck K, Nuttin B, Wenderoth N. Anodal tDCS over the primary motor cortex facilitates long-term memory formation reflecting use-dependent plasticity. PLoS ONE. 2015;10(5):e0127270. doi: 10.1371/journal.pone.0127270.
    1. Costa TL, Lapenta OM, Boggio PS, Ventura DF. Transcranial direct current stimulation as a tool in the study of sensory-perceptual processing. Atten Percept Psychophys. 2015;77(6):1813–1840. doi: 10.3758/s13414-015-0932-3.
    1. Bastani A, Jaberzadeh S. A-tDCS differential modulation of corticospinal excitability: the effects of electrode size. Brain Stimul. 2013;6(6):932–937. doi: 10.1016/j.brs.2013.04.005.
    1. DaSilva AF, Volz MS, Bikson M, Fregni F. Electrode positioning and montage in transcranial direct current stimulation. J Vis Exp. 2011;51:e2744.
    1. Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G. Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 2010;75(24):2176–2184. doi: 10.1212/WNL.0b013e318202013a.
    1. Kwon YH, Ko M-H, Ahn SH, et al. Primary motor cortex activation by transcranial direct current stimulation in the human brain. Neurosci Lett. 2008;435(1):56–59. doi: 10.1016/j.neulet.2008.02.012.
    1. Schneider HD, Hopp JP. The use of the Bilingual Aphasia Test for assessment and transcranial direct current stimulation to modulate language acquisition in minimally verbal children with autism. Clin Linguist Phon. 2011;25:640–654. doi: 10.3109/02699206.2011.570852.
    1. Ardolino G, Bossi B, Barbieri S, Priori A. Non-synaptic mechanisms underlie the after-effects of cathodal transcutaneous direct current stimulation of the human brain. J Physiol. 2005;568(Pt 2):653–663. doi: 10.1113/jphysiol.2005.088310.
    1. Lefaucheur JP. Principles of therapeutic use of transcranial and epidural cortical stimulation. Clin Neurophysiol. 2008;119(10):2179–2184. doi: 10.1016/j.clinph.2008.07.007.
    1. Boggio PS, Zaghi S, Lopes M, Fregni F. Modulatory effects of anodal transcranial direct current stimulation on perception and pain thresholds in healthy volunteers. Eur J Neurol. 2008;15(10):1124–1130. doi: 10.1111/j.1468-1331.2008.02270.x.
    1. Boggio PS, Zaghi S, Fregni F. Modulation of emotions associated with images of human pain using anodal transcranial direct current stimulation (tDCS) Neuropsychologia. 2009;47(1):212–217. doi: 10.1016/j.neuropsychologia.2008.07.022.
    1. Chiken S, Nambu A. Mechanism of deep brain stimulation: inhibition, excitation, or disruption? Neuroscientist. 2015
    1. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120(12):2008–2039. doi: 10.1016/j.clinph.2009.08.016.
    1. Tanaka S, Watanabe K. Transcranial direct current stimulation—a new tool for human cognitive neuroscience. Brain Nerve Shinkei kenkyu no shinpo. 2009;61(1):53–64.
    1. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006;117(4):845–850. doi: 10.1016/j.clinph.2005.12.003.
    1. Cabral ME, Baltar A, Borba R, et al. Transcranial direct current stimulation: before, during, or after motor training? NeuroReport. 2015;26(11):618–622. doi: 10.1097/WNR.0000000000000397.
    1. Salvador R, Wenger C, Miranda PC. Investigating the cortical regions involved in MEP modulation in tDCS. Front Cell Neurosci. 2015;9:405.
    1. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57(10):1899–1901. doi: 10.1212/WNL.57.10.1899.
    1. Rango M, Cogiamanian F, Marceglia S, et al. Myoinositol content in the human brain is modified by transcranial direct current stimulation in a matter of minutes: a 1H-MRS study. Magn Reson Med. 2008;60(4):782–789. doi: 10.1002/mrm.21709.
    1. Merzagora AC, Foffani G, Panyavin I, et al. Prefrontal hemodynamic changes produced by anodal direct current stimulation. Neuroimage. 2010;49(3):2304–2310. doi: 10.1016/j.neuroimage.2009.10.044.
    1. Takai H, Tsubaki A, Sugawara K, et al. Effect of transcranial direct current stimulation over the primary motor cortex on cerebral blood flow: a time course study using near-infrared spectroscopy. Adv Exp Med Biol. 2016;876:335–341. doi: 10.1007/978-1-4939-3023-4_42.
    1. Molaee-Ardekani B, Márquez-Ruiz J, Merlet I, et al. Effects of transcranial direct current stimulation (tDCS) on cortical activity: a computational modeling study. Brain Stimul. 2012;6(1):1–15.
    1. Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC stimulation induced after effects of human motor cortex excitability. Brain. 2002;125(10):2238–2247. doi: 10.1093/brain/awf238.
    1. Stagg CJ, Best JG, Stephenson MC, et al. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci. 2009;29(16):5202–5206. doi: 10.1523/JNEUROSCI.4432-08.2009.
    1. Nitsche MA, Kuo MF, Karrasch R, Wächter B, Liebetanz D, Paulus W. Serotonin affects transcranial direct current—induced neuroplasticity in humans. Biol Psychiatry. 2009;66(5):503–508. doi: 10.1016/j.biopsych.2009.03.022.
    1. Izumi Y, Zorumski CF. Direct cortical inputs erase long-term potentiation at Schaffer collateral synapses. J Neurosci. 2008;28(38):9557–9563. doi: 10.1523/JNEUROSCI.3346-08.2008.
    1. Márquez-Ruiz J, Leal-Campanario R, Sánchez-Campusano R, et al. Transcranial direct-current stimulation modulates synaptic mechanisms involved in associative learning in behaving rabbits. Proc Natl Acad Sci USA. 2012;109(17):6710–6715. doi: 10.1073/pnas.1121147109.
    1. Nitsche MA, Grundey J, Liebetanz D, Lang N, Tergau F, Paulus W. Catecholaminergic consolidation of motor cortical neuroplasticity in humans. Cereb Cortex. 2004;14(11):1240–1245. doi: 10.1093/cercor/bhh085.
    1. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature. 2010;468(7321):305–309. doi: 10.1038/nature09511.
    1. Filho PRM, Vercelino R, Cioato SG, et al. Transcranial direct current stimulation (tDCS) reverts behavioral alterations and brainstem BDNF level increase induced by neuropathic pain model: long-lasting effect. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;64:44–51. doi: 10.1016/j.pnpbp.2015.06.016.
    1. Iyer MB, Mattu U, Grafman J, Lomarev M, Sato S, Wassermann EM. Safety and cognitive effect of frontal DC brain polarization in healthy individuals. Neurology. 2005;64(5):872–875. doi: 10.1212/01.WNL.0000152986.07469.E9.
    1. Minhas P, Datta A, Bikson M. Cutaneous perception during tDCS: role of electrode shape and sponge salinity. Clin Neurophysiol. 2011;122(4):637–638. doi: 10.1016/j.clinph.2010.09.023.
    1. Vandermeeren Y, Jamart J, Ossemann M. Effect of tDCS with an extracephalic reference electrode on cardio-respiratory and autonomic functions. BMC Neurosci. 2010;11:38. doi: 10.1186/1471-2202-11-38.
    1. Poreisz C, Boros K, Antal A, Paulus W. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull. 2007;72(4–6):208–214. doi: 10.1016/j.brainresbull.2007.01.004.
    1. Palm U, Keeser D, Schiller C, et al. Skin lesions after treatment with transcranial direct current stimulation (tDCS) Brain Stimul. 2008;1(4):386–387. doi: 10.1016/j.brs.2008.04.003.
    1. Bikson M, Datta A, Elwassif M. Establishing safety limits for transcranial direct current stimulation. Clin Neurophysiol. 2009;120(6):1033–1034. doi: 10.1016/j.clinph.2009.03.018.
    1. Bikson M, Grossman P, Thomas C, et al. Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul. 2016
    1. van Asseldonk EHF, Boonstra TA. Transcranial direct current stimulation of the leg motor cortex enhances coordinated motor output during walking with a large inter-individual variability. Brain Stimul. 2016;9(2):182–190. doi: 10.1016/j.brs.2015.10.001.
    1. Galea JM, Jayaram G, Ajagbe L, Celnik P. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J Neurosci. 2009;29(28):9115–9122. doi: 10.1523/JNEUROSCI.2184-09.2009.
    1. Jayaram G, Tang B, Pallegadda R, Vasudevan EVL, Celnik P, Bastian A. Modulating locomotor adaptation with cerebellar stimulation. J Neurophysiol. 2012;107(11):2950–2957. doi: 10.1152/jn.00645.2011.
    1. Kim CR, Kim D-Y, Kim LS, Chun MH, Kim SJ, Park CH. Modulation of cortical activity after anodal transcranial direct current stimulation of the lower limb motor cortex: a functional MRI study. Brain Stimul. 2012;5(4):462–467. doi: 10.1016/j.brs.2011.08.002.
    1. Madhavan S, Stinear JW. Focal and bidirectional modulation of lower limb motor cortex using anodal transcranial direct current stimulation. Brain Stimul. 2010;3(1):42–50. doi: 10.1016/j.brs.2009.06.005.
    1. Jeffery DT, Norton JA, Roy FD, Gorassini MA. Effects of transcranial direct current stimulation on the excitability of the leg motor cortex. Exp Brain Res. 2007;182:281–287. doi: 10.1007/s00221-007-1093-y.
    1. Reis J, Fritsch B. Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr Opin Neurol. 2011;24(6):590–596. doi: 10.1097/WCO.0b013e32834c3db0.
    1. Hashemirad F, Zoghi M, Fitzgerald PB, Jaberzadeh S. The effect of anodal transcranial direct current stimulation on motor sequence learning in healthy individuals: a systematic review and meta-analysis. Brain Cogn. 2016;102:1–12. doi: 10.1016/j.bandc.2015.11.005.
    1. Kwon YH, Kwon JW. Response inhibition induced in the stop-signal task by transcranial direct current stimulation of the pre-supplementary motor area and primary sensoriomotor cortex. J Phys Ther Sci. 2013;25(9):1083–1086. doi: 10.1589/jpts.25.1083.
    1. Agata FD, Peila E, Cicerale A, et al. Cognitive and neurophysiological effects of non-invasive brain stimulation in stroke patients after motor rehabilitation. Front Behav Neurosci. 2016;10:1–11. doi: 10.3389/fnbeh.2016.00135.
    1. Schlaug G, Renga V, Nair D. Transcranial direct current stimulation in stroke recovery. Stroke. 2009;65(12):1571–1576.
    1. Nair DG, Renga V, Lindenberg R, et al. Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor Neurol Neurosci. 2015;29(6):411–420.
    1. O’Shea J, Boudrias M, Jane C, et al. NeuroImage predicting behavioural response to TDCS in chronic motor stroke. Neuroimage. 2014;85:924–933. doi: 10.1016/j.neuroimage.2013.05.096.
    1. Hummel F, Celnik P, Giraux P, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128(3):490–499. doi: 10.1093/brain/awh369.
    1. Rosso C, Perlbarg V, Valabregue R, et al. Broca’s area damage is necessary but not sufficient to induce after-effects of cathodal tDCS on the unaffected hemisphere in post-stroke aphasia. Brain Stimul. 2014;7(5):627–635. doi: 10.1016/j.brs.2014.06.004.
    1. Málly J. Non-invasive brain stimulation (rTMS and tDCS) in patients with aphasia: mode of action at the cellular level. Brain Res Bull. 2013;98:30–35. doi: 10.1016/j.brainresbull.2013.07.005.
    1. Gordon C, Hewer RL, Wade DT. Dysphagia in acute stroke. Br Med J (Clin Res Ed) 1987;295(6595):411–414. doi: 10.1136/bmj.295.6595.411.
    1. Barer DH. The natural history and functional consequences of dysphagia after hemispheric stroke. J Neurol Neurosurg Psychiatry. 1989;52(2):236–241. doi: 10.1136/jnnp.52.2.236.
    1. Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195–202. doi: 10.1007/BF01354538.
    1. Hamdy S, Rothwell JC, Aziz Q, Thompson DG. Organization and reorganization of human swallowing motor cortex: implications for recovery after stroke. Clin Sci. 2000;99(2):151–157. doi: 10.1042/cs0990151.
    1. Sandrini M, Cohen LG. Noninvasive brain stimulation in neurorehabilitation. Handb Clin Neurol. 2013;116:499–524. doi: 10.1016/B978-0-444-53497-2.00040-1.
    1. Kumar S, Wagner CW, Frayne C, et al. Noninvasive brain stimulation may improve stroke-related dysphagia: a pilot study. Stroke. 2011;42(4):1035–1040. doi: 10.1161/STROKEAHA.110.602128.
    1. Yang EJ, Baek S-R, Shin J, et al. Effects of transcranial direct current stimulation (tDCS) on post-stroke dysphagia. Restor Neurol Neurosci. 2012;30(4):303–311.
    1. Hickey P, Stacy M. Deep brain stimulation: a paradigm shifting approach to treat Parkinson’s disease. Front Neurosci. 2016;10:1–11. doi: 10.3389/fnins.2016.00173.
    1. Broeder S, Nackaerts E, Heremans E, et al. Transcranial direct current stimulation in Parkinson’s disease: neurophysiological mechanisms and behavioral effects. Neurosci Biobehav Rev. 2015;57:105–117. doi: 10.1016/j.neubiorev.2015.08.010.
    1. Fregni F, Boggio PS, Santos MC, et al. Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov Disord. 2006;21(10):1693–1702. doi: 10.1002/mds.21012.
    1. Valentino F, Cosentino G, Brighina F, et al. Transcranial direct current stimulation for treatment of freezing of gait: a cross-over study. Mov Disord. 2014;29(8):1064–1069. doi: 10.1002/mds.25897.
    1. Ferrucci R, Cortese F, Bianchi M, et al. Cerebellar and motor cortical transcranial stimulation decrease levodopa-induced dyskinesias in Parkinson’s disease. Cerebellum. 2016;15(1):43–47. doi: 10.1007/s12311-015-0737-x.
    1. Mehta S, McIntyre A, Guy S, Teasell RW, Loh E. Effectiveness of transcranial direct current stimulation for the management of neuropathic pain after spinal cord injury: a meta-analysis. Spinal Cord. 2015;53:1–6. doi: 10.1038/sc.2015.118.
    1. Pérez-Fernández C, Sánchez-Kuhn A, Cánovas R, Flores P, Sánchez-Santed F. The effect of transcranial direct current stimulation (tDCS) over human motor function. 2016;9656. doi:10.1007/978-3-319-31744-1_43.
    1. Cuypers K, Leenus DJF, Van Wijmeersch B, et al. Anodal tDCS increases corticospinal output and projection strength in multiple sclerosis. Neurosci Lett. 2013;554:151–155. doi: 10.1016/j.neulet.2013.09.004.
    1. Meesen RLJ, Thijs H, Leenus DJF, Cuypers K. A single session of 1 mA anodal tDCS-supported motor training does not improve motor performance in patients with multiple sclerosis. Restor Neurol Neurosci. 2013
    1. Mori F, Nicoletti CG, Kusayanagi H, et al. Transcranial direct current stimulation ameliorates tactile sensory deficit in multiple sclerosis. Brain Stimul. 2013;6(4):654–659. doi: 10.1016/j.brs.2012.10.003.
    1. Mori F, Codecà C, Kusayanagi H, et al. Effects of anodal transcranial direct current stimulation on chronic neuropathic pain in patients with multiple sclerosis. J Pain. 2010;11(5):436–442. doi: 10.1016/j.jpain.2009.08.011.
    1. Di Lazzaro V, Ranieri F, Capone F, Musumeci G, Dileone M. Direct current motor cortex stimulation for amyotrophic lateral sclerosis: a proof of principle study. Brain Stimul. 2013;6(6):969–970. doi: 10.1016/j.brs.2013.06.005.
    1. Munneke MAM, Stegeman DF, Hengeveld YA, Rongen JJ, Jurgen Schelhaas H, Zwarts MJ. Transcranial direct current stimulation does not modulate motor cortex excitability in patients with Amyotrophic lateral sclerosis. Muscle Nerve. 2011; 44(1):109–114. .
    1. Quartarone A, Lang N, Rizzo V, et al. Motor cortex abnormalities in amyotrophic lateral sclerosis with transcranial direct-current stimulation. Muscle Nerve. 2007;35(5):620–624. doi: 10.1002/mus.20737.
    1. Munneke MAM, Rongen JJ, Overeem S, Schelhaas HJ, Zwarts MJ, Stegeman DF. Cumulative effect of 5 daily sessions of θ burst stimulation on corticospinal excitability in amyotrophic lateral sclerosis. Muscle Nerve. 2013;48(5):733–738. doi: 10.1002/mus.23818.
    1. Silva FTG, Raulino JTP, Reynaud FR, et al. Transcranial direct current stimulation on the autonomic modulation and exercise time in individuals with spinal cord injury. A case report. Auton Neurosci Basic Clin. 2015; 193:152–5. .
    1. Murray LM, Edwards DJ, Ruffini G, et al. Intensity dependent effects of transcranial direct current stimulation on corticospinal excitability in chronic spinal cord injury. Arch Phys Med Rehabil. 2014;96(4 Suppl):S114–S121.
    1. Hubli M, Dietz V, Schrafl-Altermatt M, Bolliger M. Modulation of spinal neuronal excitability by spinal direct currents and locomotion after spinal cord injury. Clin Neurophysiol. 2013;124(6):1187–1195. doi: 10.1016/j.clinph.2012.11.021.
    1. Cogiamanian F, Vergari M, Pulecchi F, Marceglia S, Priori A. Effect of spinal transcutaneous direct current stimulation on somatosensory evoked potentials in humans. Clin Neurophysiol. 2008;119(11):2636–2640. doi: 10.1016/j.clinph.2008.07.249.
    1. Barrière G, Cazalets JR, Bioulac B, Tison F, Ghorayeb I. The restless legs syndrome. Prog Neurobiol. 2005;77(3):139–165. doi: 10.1016/j.pneurobio.2005.10.007.
    1. Heide AC, Winkler T, Helms HJ, et al. Effects of transcutaneous spinal direct current stimulation in idiopathic restless legs patients. Brain Stimul. 2014;7(5):636–642. doi: 10.1016/j.brs.2014.06.008.
    1. Koo Yong Seo, Kim SM, et al. Transcranial direct current stimulation on primary sensorimotor area has no effect in patients with drug-naive restless legs syndrome: a proof-of-concept clinical trial. Sleep Med. 2015;16(2):280–287. doi: 10.1016/j.sleep.2014.07.032.
    1. De Almeida JR, Guyatt GH, Sud S, et al. Management of Bell palsy: clinical practice guideline. CMAJ. 2014;186(12):917–922. doi: 10.1503/cmaj.131801.
    1. Minhas P, Bikson M, Woods AJ, Rosen AR, Kessler SK. Transcranial direct current stimulation in pediatric brain: a computational modeling study. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:859–862.
    1. Duarte NDAC, Grecco LAC, Galli M, Fregni F, Oliveira CS. Effect of transcranial direct-current stimulation combined with treadmill training on balance and functional performance in children with cerebral palsy: a double-blind randomized controlled trial. PLoS ONE. 2014;9(8):e105777. doi: 10.1371/journal.pone.0105777.
    1. Kheder A, Nair KPS. Spasticity: pathophysiology, evaluation and management. Pract Neurol. 2012;12(5):289–298. doi: 10.1136/practneurol-2011-000155.
    1. Aree-Uea B, Auvichayapat N, Janyacharoen T, et al. Reduction of spasticity in cerebral palsy by anodal transcranial direct current stimulation. J Med Assoc Thail. 2014;97(9):954–962.
    1. Delasta Lazzari R, Politti F, Almeida Santos C, et al. Effect of a single session of transcranial direct-current stimulation combined with virtual reality training on the balance of children with cerebral palsy: a randomized, controlled, double-blind trial. J Phys Ther Sci. 2015;27:763–768. doi: 10.1589/jpts.27.763.
    1. André L, Grecco C, De N, et al. Effects of anodal transcranial direct current stimulation combined with virtual reality for improving gait in children with spastic diparetic cerebral palsy: a pilot, randomized, controlled, double-blind, clinical trial. Clin Rehabil. 2015
    1. Teo W, Muthalib M, Yamin S, Hendy AM, Bramstedt K, Reilly RB. Does a combination of virtual reality, neuromodulation and neuroimaging provide a comprehensive platform for neurorehabilitation ?—A narrative review of the literature. Front Hum Neurosci. 2016;10:1–15. doi: 10.3389/fnhum.2016.00284.
    1. Parkin BL, Ekhtiari H, Walsh VF. Non-invasive human brain stimulation in cognitive neuroscience: a primer. Neuron. 2015;87(5):932–945. doi: 10.1016/j.neuron.2015.07.032.
    1. Woods AJ, Antal A, Bikson M, et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol. 2016;127(2):1031–1048. doi: 10.1016/j.clinph.2015.11.012.
    1. Wiethoff S, Hamada M, Rothwell JC. Variability in response to transcranial direct current stimulation of the motor cortex. Brain Stimul. 2014;7(3):468–475. doi: 10.1016/j.brs.2014.02.003.
    1. Schlaug G. Musicians and music making as a model for the study of brain plasticity. Prog Brain Res. 2015;217:37–55. doi: 10.1016/bs.pbr.2014.11.020.
    1. Saucedo Marquez CM, Zhang X, Swinnen SP, Meesen R, Wenderoth N. Task-specific effect of transcranial direct current stimulation on motor learning. Front Hum Neurosci. 2013;7(July):333.
    1. Furuya S, Klaus M, Nitsche MA, Paulus W, Altenmüller E. Ceiling effects prevent further improvement of transcranial stimulation in skilled musicians. J Neurosci. 2014
    1. Krings T, Töpper R, Foltys H, et al. Cortical activation patterns during complex motor tasks in piano players and control subjects. A functional magnetic resonance imaging study. Neurosci Lett. 2000;278(3):189–193. doi: 10.1016/S0304-3940(99)00930-1.
    1. Wright DJ, Holmes PS, Di Russo F, Loporto M, Smith D. Differences in cortical activity related to motor planning between experienced guitarists and non-musicians during guitar playing. Hum Mov Sci. 2012;31(3):567–577. doi: 10.1016/j.humov.2011.07.001.
    1. Koeneke S, Lutz K, Wüstenberg T, Jäncke L. Long-term training affects cerebellar processing in skilled keyboard players. NeuroReport. 2004;15(8):1279–1282. doi: 10.1097/01.wnr.0000127463.10147.e7.
    1. Hasan A, Misewitsch K, Nitsche MA, et al. Impaired motor cortex responses in non-psychotic first-degree relatives of schizophrenia patients: a cathodal tDCS pilot study. Brain Stimul. 2013;6(5):821–829. doi: 10.1016/j.brs.2013.03.001.
    1. Lang N, Siebner HR, Ward NS, et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci. 2005;22(2):495–504. doi: 10.1111/j.1460-9568.2005.04233.x.
    1. Kuo H, Bikson M, Datta A, et al. Brain stimulation comparing cortical plasticity induced by conventional and high-definition 4 Â 1 ring tDCS: a neurophysiological study. Brain Stimul. 2013;6(4):644–648. doi: 10.1016/j.brs.2012.09.010.
    1. Datta A, Elwassif M, Bikson M. Bio-heat transfer model of transcranial DC stimulation: Comparison of conventional pad versus ring electrode. In: Proceedings of the 31st annual international conference of the IEEE engineering in medicine and biology society: engineering the future of biomedicine, EMBC 2009. 2009; 670–3. doi: 10.1109/IEMBS.2009.5333673.
    1. Roy A, Baxter B, He B. 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. 2014;61(7):1967–1978. doi: 10.1109/TBME.2014.2311071.
    1. Garnett EO, den Ouden D-B. Validating a sham condition for use in high definition transcranial direct current stimulation. Brain Stimul. 2015;8(3):551–554. doi: 10.1016/j.brs.2015.01.399.
    1. Been G, Ngo TT, Miller SM, Fitzgerald PB. The use of tDCS and CVS as methods of non-invasive brain stimulation. Brain Res Rev. 2007;56(2):346–361. doi: 10.1016/j.brainresrev.2007.08.001.
    1. Brunoni AR, Nitsche MA, Bolognini N, et al. Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul. 2012;5(3):175–195. doi: 10.1016/j.brs.2011.03.002.
    1. Radman T, Ramos RL, Brumberg JC, Bikson M. Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain Stimul. 2009;2(4):215–228. doi: 10.1016/j.brs.2009.03.007.
    1. Brunoni AR, Ferrucci R, Bortolomasi M, et al. Interactions between transcranial direct current stimulation (tDCS) and pharmacological interventions in the Major Depressive Episode: findings from a naturalistic study. Eur Psychiatry. 2013;28(6):356–361. doi: 10.1016/j.eurpsy.2012.09.001.
    1. Kouzani AZ, Jaberzadeh S, Zoghi M, Usma C, Parastarfeizabadi M. Development and validation of a miniature programmable tDCS device. IEEE Trans Neural Syst Rehabil Eng. 2016;24(1):192–198. doi: 10.1109/TNSRE.2015.2468579.

Source: PubMed

3
Abonneren