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. 2012 Sep 5;3(4):474–481. doi: 10.1016/j.nurx.2006.07.008

Noninvasive brain stimulation in stroke rehabilitation

Brian R Webster 1, Pablo A Celnik 1, Leonardo G Cohen 1,
PMCID: PMC3593409  PMID: 17012061

Summary

Stroke is a common disorder that produces a major burden to society, largely through long-lasting motor disability in survivors. Recent studies have broadened our understanding of the processes underlying recovery of motor function after stroke. Bilateral motor regions of the brain experience substantial reorganization after stroke, including changes in the strength of interhemispheric inhibitory interactions. Our understanding of the extent to which different forms of reorganization contribute to behavioral gains in the rehabilitative process, although still limited, has led to the formulation of novel interventional strategies to regain motor function. Transcranial magnetic (TMS) and DC (tDCS) electrical stimulation are noninvasive brain stimulation techniques that modulate cortical excitability in both healthy individuals and stroke patients. These techniques can enhance the effect of training on performance of various motor tasks, including those that mimic activities of daily living. This review looks at the effects of TMS and tDCS on motor cortical function and motor performance in healthy volunteers and in patients with stroke. Both techniques can either enhance or suppress cortical excitability, and may move to the clinical arena as strategies to enhance the beneficial effects of customarily used neurorehabilitative treatments after stroke.

Key Words: Stroke, motor cortex, rehabilitation, cortical stimulation, transcranial magnetic stimulation (TMS), transcranial direct current stimulation (tDCS), plasticity

References

  • 1.Heart disease and stroke statistics: 2005 update. Dallas, Texas: AHA; 2005. [Google Scholar]
  • 2.Centers for Disease Control and Prevention Prevalence of disabilities and associated health conditions among adults: United States, 1999. MMWR Morb Mortal Wkly Rep. 2001;50:120–5. [PubMed] [Google Scholar]
  • 3.Kavanagh S, Knapp M, Patel A. Costs and disability among stroke patients. J Public Health Med. 1999;21:385–394. doi: 10.1093/pubmed/21.4.385. [DOI] [PubMed] [Google Scholar]
  • 4.Wade DT, Langton-Hewer R, Wood VA, Skilbeck CE, Ismail HM. The hemiplegic arm after stroke: measurement and recovery. J Neurol Neurosurg Psychiatry. 1983;46:521–524. doi: 10.1136/jnnp.46.6.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Sunderland A, Tinson D, Bradley L, Hewer RL. Arm function after stroke: an evaluation of grip strength as a measure of recovery and a prognostic indicator. J Neurol Neurosurg Psychiatry. 1989;52:1267–1272. doi: 10.1136/jnnp.52.11.1267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Demaerschalk BM, Yip TR. Economic benefit of increasing utilization of intravenous tissue plasminogen activator for acute ischemic stroke in the United States. Stroke. 2005;36:2500–2503. doi: 10.1161/01.STR.0000185699.37843.14. [DOI] [PubMed] [Google Scholar]
  • 7.Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J. Measurement of motor recovery after stroke: outcome assessment and sample size requirements. Stroke. 1992;23:1084–1089. doi: 10.1161/01.str.23.8.1084. [DOI] [PubMed] [Google Scholar]
  • 8.Barreca S, Wolf SL, Fasoli S, Bohannon R. Treatment interventions for the paretic upper limb of stroke survivors: a critical review. Neurorehabil Neural Repair. 2003;17:220–226. doi: 10.1177/0888439003259415. [DOI] [PubMed] [Google Scholar]
  • 9.Krakauer JW. Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol. 2006;19:84–90. doi: 10.1097/01.wco.0000200544.29915.cc. [DOI] [PubMed] [Google Scholar]
  • 10.Taub E, Miller NE, Novack TA, et al. Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil. 1993;74:347–354. [PubMed] [Google Scholar]
  • 11.Taub E, Uswatte G, Pidikiti R. Constraint-induced movement therapy: a new family of techniques with broad application to physical rehabilitation—a clinical review. J Rehabil Res Dev. 1999;36:237–251. [PubMed] [Google Scholar]
  • 12.Taub E, Uswatte G, Elbert T. New treatments in neurorehabilitation founded on basic research. Nat Rev Neurosci. 2002;3:228–236. doi: 10.1038/nrn754. [DOI] [PubMed] [Google Scholar]
  • 13.Luft AR, McCombe-Waller S, Whitall J, et al. Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. JAMA. 2004;292:1853–1861. doi: 10.1001/jama.292.15.1853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Whitall J, McCombe Waller S, Silver KH, Macko RF. Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke. 2000;31:2390–2395. doi: 10.1161/01.str.31.10.2390. [DOI] [PubMed] [Google Scholar]
  • 15.Dobkin B, Apple D, Barbeau H, et al. Weight-supported treadmill vs. over-ground training for walking after acute incomplete SCI. Neurology. 2006;66:484–493. doi: 10.1212/01.wnl.0000202600.72018.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Dobkin B, Apple D, Barbeau H, et al. Methods for a randomized trial of weight-supported treadmill training versus conventional training for walking during inpatient rehabilitation after incomplete traumatic spinal cord injury. Neurorehabil Neural Repair. 2003;17:153–167. doi: 10.1177/0888439003255508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Sullivan KJ, Knowlton BJ, Dobkin BH. Step training with body weight support: effect of treadmill speed and practice paradigms on poststroke locomotor recovery. Arch Phys Med Rehabil. 2002;83:683–691. doi: 10.1053/apmr.2002.32488. [DOI] [PubMed] [Google Scholar]
  • 18.Hesse S, Schmidt H, Werner C, Bardeleben A. Upper and lower extremity robotic devices for rehabilitation and for studying motor control. Curr Opin Neurol. 2003;16:705–710. doi: 10.1097/01.wco.0000102630.16692.38. [DOI] [PubMed] [Google Scholar]
  • 19.Hesse S, Schulte-Tigges G, Konrad M, Bardeleben A, Werne C. Robot-assisted arm trainer for the passive and active practice of bilateral forearm and wrist movements in hemiparetic subjects. Arch Phys Med Rehabil. 2003;84:915–920. doi: 10.1016/s0003-9993(02)04954-7. [DOI] [PubMed] [Google Scholar]
  • 20.Lum PS, Burgar CG, Shor PC, Majmundar M, van der Loos M. Robot-assisted movement training compared with conventional therapy techniques for the rehabilitation of upper-limb motor function after stroke. Arch Phys Med Rehabil. 2002;83:952–959. doi: 10.1053/apmr.2001.33101. [DOI] [PubMed] [Google Scholar]
  • 21.Patton JL, Stoykov ME, Kovic M, Mussa-Ivaldi FA. Evaluation of robotic training forces that either enhance or reduce error in chronic hemiparetic stroke survivors. Exp Brain Res. 2006;168:368–383. doi: 10.1007/s00221-005-0097-8. [DOI] [PubMed] [Google Scholar]
  • 22.Stein J, Krebs HI, Frontera WR, Fasoli SE, Hughes R, Hogan N. Comparison of two techniques of robot-aided upper limb exercise training after stroke. Am J Phys Med Rehabil. 2004;83:720–728. doi: 10.1097/01.phm.0000137313.14480.ce. [DOI] [PubMed] [Google Scholar]
  • 23.Volpe BT, Ferraro M, Lynch D, et al. Robotics and other devices in the treatment of patients recovering from stroke. Curr Neurol Neurosci Rep. 2005;5:465–470. doi: 10.1007/s11910-005-0035-y. [DOI] [PubMed] [Google Scholar]
  • 24.Volpe BT, Krebs HI, Hogan N. Is robot-aided sensorimotor training in stroke rehabilitation a realistic option? Curr Opin Neurol. 2001;14:745–752. doi: 10.1097/00019052-200112000-00011. [DOI] [PubMed] [Google Scholar]
  • 25.Deutsch JE, Merians AS, Adamovich S, Poizner H, Burdea GC. Development and application of virtual reality technology to improve hand use and gait of individuals post-stroke. Restor Neurol Neurosci. 2004;22:371–386. [PubMed] [Google Scholar]
  • 26.Fung J, Richards CL, Malouin F, McFadyen BJ, Lamontagne A. A treadmill and motion coupled virtual reality system for gait training post-stroke. Cyberpsychol Behav. 2006;9:157–162. doi: 10.1089/cpb.2006.9.157. [DOI] [PubMed] [Google Scholar]
  • 27.Holden MK. Virtual environments for motor rehabilitation: review. Cyberpsychol Behav. 2005;8:187–211. doi: 10.1089/cpb.2005.8.187. [DOI] [PubMed] [Google Scholar]
  • 28.Katz N, Ring H, Naveh Y, Kizony R, Feintuch U, Weiss PL. Interactive virtual environment training for safe street crossing of right hemisphere stroke patients with unilateral spatial neglect. Disabil Rehabil. 2005;27:1235–1243. doi: 10.1080/09638280500076079. [DOI] [PubMed] [Google Scholar]
  • 29.Kuttuva M, Boian R, Merians A, et al. The Rutgers Arm, a rehabilitation system in virtual reality: a pilot study. Cyberpsychol Behav. 2006;9:148–152. doi: 10.1089/cpb.2006.9.148. [DOI] [PubMed] [Google Scholar]
  • 30.Viau A, Feldman AG, McFadyen BJ, Levin MF. Reaching in reality and virtual reality: a comparison of movement kinematics in healthy subjects and in adults with hemiparesis. J Neuroengineering Rehabil. 2004;1:11–11. doi: 10.1186/1743-0003-1-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Ward NS, Cohen LG. Mechanisms underlying recovery of motor function after stroke. Arch Neurol. 2004;61:1844–1848. doi: 10.1001/archneur.61.12.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Calautti C, Baron J-C. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke. 2003;34:1553–1566. doi: 10.1161/01.STR.0000071761.36075.A6. [DOI] [PubMed] [Google Scholar]
  • 33.Wall PD, Egger M. Formation of new connexions in adult rat brains after partial deafferentation. Nature. 1971;232:542–545. doi: 10.1038/232542a0. [DOI] [PubMed] [Google Scholar]
  • 34.Raisman G, Field PM. A quantitative investigation of the development of collateral reinnervation after partial deafferentation of the septal nuclei. Brain Res. 1973;50:241–264. doi: 10.1016/0006-8993(73)90729-4. [DOI] [PubMed] [Google Scholar]
  • 35.Chklovskii DB, Mel BW, Svoboda K. Cortical rewiring and information storage. Nature. 2004;431:782–788. doi: 10.1038/nature03012. [DOI] [PubMed] [Google Scholar]
  • 36.Bliss TV, Gardner-Medwin AR. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232:357–374. doi: 10.1113/jphysiol.1973.sp010274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232:331–356. doi: 10.1113/jphysiol.1973.sp010273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Byrnes ML, Thickbroom GW, Phillips BA, Mastaglia FL. Longterm changes in motor cortical organization after recovery from subcortical stroke. Brain Res. 2001;889:278–287. doi: 10.1016/s0006-8993(00)03089-4. [DOI] [PubMed] [Google Scholar]
  • 39.Finger S, Koehler PJ, Jagella C. The Monakow concept of diaschisis: origins and perspectives. Arch Neurol. 2004;61:283–288. doi: 10.1001/archneur.61.2.283. [DOI] [PubMed] [Google Scholar]
  • 40.Flint AC, Naley MC, Wright CB. Ataxic hemiparesis from strategic frontal white matter infarction with crossed cerebellar diaschisis. Stroke. 2006;37:e1–2. doi: 10.1161/01.STR.0000195179.93268.e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Infeld B, Davis SM, Lichtenstein M, Mitchell PJ, Hopper JL. Crossed cerebellar diaschisis and brain recovery after stroke. Stroke. 1995;26:90–95. doi: 10.1161/01.str.26.1.90. [DOI] [PubMed] [Google Scholar]
  • 42.Miura H, Nagata K, Hirata Y, Satoh Y, Watahiki Y, Hatazawa J. Evolution of crossed cerebellar diaschisis in middle cerebral artery infarction. J Neuroimaging. 1994;4:91–96. doi: 10.1111/jon19944291. [DOI] [PubMed] [Google Scholar]
  • 43.Pantano P, Lenzi GL, Guidetti B, et al. Crossed cerebellar diaschisis in patients with cerebral ischemia assessed by SPECT and 123I-HIPDM. Eur Neurol. 1987;27:142–148. doi: 10.1159/000116147. [DOI] [PubMed] [Google Scholar]
  • 44.Sobesky J, Thiel A, Ghaemi M, et al. Crossed cerebellar diaschisis in acute human stroke: a PET study of serial changes and response to supratentorial reperfusion. J Cereb Blood Flow Metab. 2005;25:1685–1691. doi: 10.1038/sj.jcbfm.9600162. [DOI] [PubMed] [Google Scholar]
  • 45.Cappa SF, Perani D, Grassi F, et al. A PET follow-up study of recovery after stroke in acute aphasics. Brain Lang. 1997;56:55–67. doi: 10.1006/brln.1997.1737. [DOI] [PubMed] [Google Scholar]
  • 46.Rizzo M, Robin DA. Bilateral effects of unilateral visual cortex lesions in human. Brain. 1996;119:951–963. doi: 10.1093/brain/119.3.951. [DOI] [PubMed] [Google Scholar]
  • 47.Seitz RJ, Azari NP, Knorr U, Binkofski F, Herzog H, Freund HJ. The role of diaschisis in stroke recovery. Stroke. 1999;30:1844–1850. doi: 10.1161/01.str.30.9.1844. [DOI] [PubMed] [Google Scholar]
  • 48.Kwakkel G, Kollen B, Lindeman E. Understanding the pattern of functional recovery after stroke: facts and theories. Restor Neurol Neurosci. 2004;22:281–299. [PubMed] [Google Scholar]
  • 49.Feeney DM. From laboratory to clinic: noradrenergic enhancement of physical therapy for stroke or trauma patients. Adv Neurol. 1997;73:383–394. [PubMed] [Google Scholar]
  • 50.Martinsson L, Eksborg S. Drugs for stroke recovery: the example of amphetamines. Drugs Aging. 2004;21:67–79. doi: 10.2165/00002512-200421020-00001. [DOI] [PubMed] [Google Scholar]
  • 51.Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 1996;272:1791–1794. doi: 10.1126/science.272.5269.1791. [DOI] [PubMed] [Google Scholar]
  • 52.Nudo RJ, Milliken GW. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol. 1996;75:2144–2149. doi: 10.1152/jn.1996.75.5.2144. [DOI] [PubMed] [Google Scholar]
  • 53.Jaillard A, Martin CD, Garambois K, Lebas JF, Hommel M. Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. Brain. 2005;128:1122–1138. doi: 10.1093/brain/awh456. [DOI] [PubMed] [Google Scholar]
  • 54.Cramer SC, Nelles G, Benson RR, et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke. 1997;28:2518–2527. doi: 10.1161/01.str.28.12.2518. [DOI] [PubMed] [Google Scholar]
  • 55.Cramer SC, Shah R, Juranek J, Crafton KR, Le V. Activity in the peri-infarct rim in relation to recovery from stroke. Stroke. 2006;37:111–115. doi: 10.1161/01.STR.0000195135.70379.1f. [DOI] [PubMed] [Google Scholar]
  • 56.Loubinoux I, Carel C, Pariente J, et al. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage. 2003;20:2166–2180. doi: 10.1016/j.neuroimage.2003.08.017. [DOI] [PubMed] [Google Scholar]
  • 57.Werhahn KJ, Conforto AB, Kadom N, Hallett M, Cohen LG. Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol. 2003;54:464–472. doi: 10.1002/ana.10686. [DOI] [PubMed] [Google Scholar]
  • 58.Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG. Reorganization of the human ipsilesional premotor cortex after stroke. Brain. 2004;127:747–758. doi: 10.1093/brain/awh082. [DOI] [PubMed] [Google Scholar]
  • 59.Calautti C, Leroy F, Guincestre JY, Marie RM, Baron JC. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport. 2001;12:3883–3886. doi: 10.1097/00001756-200112210-00005. [DOI] [PubMed] [Google Scholar]
  • 60.Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke. 2000;31:656–661. doi: 10.1161/01.str.31.3.656. [DOI] [PubMed] [Google Scholar]
  • 61.Feydy A, Carlier R, Roby-Brami A, et al. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke. 2002;33:1610–1617. doi: 10.1161/01.str.0000017100.68294.52. [DOI] [PubMed] [Google Scholar]
  • 62.Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA. 2002;99:14518–14523. doi: 10.1073/pnas.222536799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63.Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci. 2006;26:6096–6102. doi: 10.1523/JNEUROSCI.4564-05.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Rossini PM, Calautti C, Pauri F, Baron JC. Post-stroke plastic reorganisation in the adult brain. Lancet Neurol. 2003;2:493–502. doi: 10.1016/s1474-4422(03)00485-x. [DOI] [PubMed] [Google Scholar]
  • 65.Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 2004;55:400–409. doi: 10.1002/ana.10848. [DOI] [PubMed] [Google Scholar]
  • 66.Meyer BU, Roricht S, Grafin von Einsiedel H, Kruggel F, Weindl A. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain. 1995;118:429–440. doi: 10.1093/brain/118.2.429. [DOI] [PubMed] [Google Scholar]
  • 67.Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res. 2004;154:1–10. doi: 10.1007/s00221-003-1684-1. [DOI] [PubMed] [Google Scholar]
  • 68.Liepert J, Hallett M, Samii A, et al. Motor cortex excitability in patients with cerebellar degeneration. Clin Neurophysiol. 2000;111:1157–1164. doi: 10.1016/s1388-2457(00)00308-4. [DOI] [PubMed] [Google Scholar]
  • 69.Cicinelli P, Pasqualetti P, Zaccagnini M, Traversa R, Oliveri M, Rossini PM. Interhemispheric asymmetries of motor cortex excitability in the postacute stroke stage: a paired-pulse transcranial magnetic stimulation study. Stroke. 2003;34:2653–2658. doi: 10.1161/01.STR.0000092122.96722.72. [DOI] [PubMed] [Google Scholar]
  • 70.Manganotti P, Patuzzo S, Cortese F, Palermo A, Smania N, Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol. 2002;113:936–943. doi: 10.1016/s1388-2457(02)00062-7. [DOI] [PubMed] [Google Scholar]
  • 71.Kapur N. Paradoxical functional facilitation in brain-behaviour research: a critical review. Brain. 1996;119:1775–1790. doi: 10.1093/brain/119.5.1775. [DOI] [PubMed] [Google Scholar]
  • 72.Finger S, Beyer T, Koehler PJ. Dr. Otto Soltmann (1876) on development of the motor cortex and recovery after its removal in infancy. Brain Res Bull. 2000;3:133–140. doi: 10.1016/s0361-9230(00)00318-x. [DOI] [PubMed] [Google Scholar]
  • 73.Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci. 1996;16:785–807. doi: 10.1523/JNEUROSCI.16-02-00785.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Xerri C, Merzenich MM, Peterson BE, Jenkins W. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol. 1998;79:2119–2148. doi: 10.1152/jn.1998.79.4.2119. [DOI] [PubMed] [Google Scholar]
  • 75.Brown JA, Lutsep HL, Weinand M, Cramer SC. Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery. 2006;58:464–473. doi: 10.1227/01.NEU.0000197100.63931.04. [DOI] [PubMed] [Google Scholar]
  • 76.Teskey GC, Flynn C, Goertzen CD, Monfils MH, Young NA. Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol Res. 2003;25:794–800. doi: 10.1179/016164103771953871. [DOI] [PubMed] [Google Scholar]
  • 77.Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406:147–150. doi: 10.1038/35018000. [DOI] [PubMed] [Google Scholar]
  • 78.Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res. 2003;148:1–16. doi: 10.1007/s00221-002-1234-2. [DOI] [PubMed] [Google Scholar]
  • 79.Paulus W. Transcranial direct current stimulation (tDCS) Suppl Clin Neurophysiol. 2003;56:249–254. doi: 10.1016/s1567-424x(09)70229-6. [DOI] [PubMed] [Google Scholar]
  • 80.Wassermann EM, Grafman J. Recharging cognition with DC brain polarization. Trends Cogn Sci. 2005;9:503–505. doi: 10.1016/j.tics.2005.09.001. [DOI] [PubMed] [Google Scholar]
  • 81.Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W. Modulation of cortical excitability by weak direct current stimulation: technical, safety and functional aspects. Suppl Clin Neurophysiol. 2003;56:255–276. doi: 10.1016/s1567-424x(09)70230-2. [DOI] [PubMed] [Google Scholar]
  • 82.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;117:845–850. doi: 10.1016/j.clinph.2005.12.003. [DOI] [PubMed] [Google Scholar]
  • 83.Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol. 1998;108:1–16. doi: 10.1016/s0168-5597(97)00096-8. [DOI] [PubMed] [Google Scholar]
  • 84.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;64:872–875. doi: 10.1212/01.WNL.0000152986.07469.E9. [DOI] [PubMed] [Google Scholar]
  • 85.Lang N, Siebner R, 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;22:495–504. doi: 10.1111/j.1460-9568.2005.04233.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 86.Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci. 2004;19:1950–1962. doi: 10.1111/j.1460-9568.2004.03277.x. [DOI] [PubMed] [Google Scholar]
  • 87.Wagner T, Fregni F, Eden U, et al. Transcranial magnetic stimulation and stroke: a computer-based human model study. Neuroimage. 2006;30:857–870. doi: 10.1016/j.neuroimage.2005.04.046. [DOI] [PubMed] [Google Scholar]
  • 88.Kobayashi M, Hutchinson S, Theoret H, Schlaug G, Pascual-Leone A. Repetitive TMS of the motor cortex improves ipsilateral sequential simple finger movements. Neurology. 2004;62:91–98. doi: 10.1212/wnl.62.1.91. [DOI] [PubMed] [Google Scholar]
  • 89.Kim YH, You SH, Ko MH, et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 2006. [DOI] [PubMed]
  • 90.Tegenthoff M, Ragert P, Pleger B, et al. Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS. PLoS Biol. 2005;3:e362–e362. doi: 10.1371/journal.pbio.0030362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 91.Rosen SC, Stamm JS. Transcortical polarization: facilitation of delayed response performance by monkeys. Exp Neurol. 1972;35:282–289. doi: 10.1016/0014-4886(72)90154-9. [DOI] [PubMed] [Google Scholar]
  • 92.Elbert T, Rockstroh B, Lutzenberger W, Birbaumer N. The influence of low-level, event-related DC-currents during time estimation in humans. Int J Neurosci. 1981;15:103–106. doi: 10.3109/00207458108985850. [DOI] [PubMed] [Google Scholar]
  • 93.Elbert T, Rockstroh B, Lutzenberger W, Birbaumer N. Influence of low-level transcortical DC-currents on response speed in humans. Int J Neurosci. 1981;14:101–114. doi: 10.3109/00207458108985821. [DOI] [PubMed] [Google Scholar]
  • 94.Nitsche MA, Schauenburg A, Lang N, et al. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J Cogn Neurosci. 2003;15:619–626. doi: 10.1162/089892903321662994. [DOI] [PubMed] [Google Scholar]
  • 95.Fregni F, Boggio PS, Mansur CG, et al. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport. 2005;16:1551–1555. doi: 10.1097/01.wnr.0000177010.44602.5e. [DOI] [PubMed] [Google Scholar]
  • 96.Kincses TZ, Antal A, Nitsche MA, Bartfai O, Paulus W. Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human. Neuropsychologia. 2004;42:113–117. doi: 10.1016/s0028-3932(03)00124-6. [DOI] [PubMed] [Google Scholar]
  • 97.Antal A, Nitsche MA, Kruse W, Kincses TZ, Hoffmann KP, Paulus W. Direct current stimulation over V5 enhances visuomotor coordination by improving motion perception in humans. J Cogn Neurosci. 2004;6:521–527. doi: 10.1162/089892904323057263. [DOI] [PubMed] [Google Scholar]
  • 98.Bear MF, Malenka R. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol. 1994;4:389–399. doi: 10.1016/0959-4388(94)90101-5. [DOI] [PubMed] [Google Scholar]
  • 99.Woody CD, Gruen E, Birt D. Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res. 1991;539:76–84. doi: 10.1016/0006-8993(91)90688-r. [DOI] [PubMed] [Google Scholar]
  • 100.Dancause N, Barbay S, Frost SB, et al. Extensive cortical rewiring after brain injury. J Neurosci. 2005;25:10167–10179. doi: 10.1523/JNEUROSCI.3256-05.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 101.Hummel F, Celnik P, Giraux P, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128:490–499. doi: 10.1093/brain/awh369. [DOI] [PubMed] [Google Scholar]
  • 102.Hummel F, Cohen LG. Improvement of motor function with noninvasive cortical stimulation in a patient with chronic stroke. Neurorehabil Neural Repair. 2005;19:14–19. doi: 10.1177/1545968304272698. [DOI] [PubMed] [Google Scholar]
  • 103.Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA. An objective and standardized test of hand function. Arch Phys Med Rehabil. 1969;50:311–319. [PubMed] [Google Scholar]
  • 104.Kraft GH, Fitts SS, Hammond MC. Techniques to improve function of the arm and hand in chronic hemiplegia. Arch Phys Med Rehabil. 1992;73:220–227. [PubMed] [Google Scholar]
  • 105.Alon G, Sunnerhagen KS, Geurts AC, Ohry A. A home-based, self-administered stimulation program to improve selected hand functions of chronic stroke. Neurorehabilitation. 2003;18:215–225. [PubMed] [Google Scholar]
  • 106.Wu CW, Seo HJ, Cohen LG. Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke. Arch Phys Med Rehabil. 2006;87:351–357. doi: 10.1016/j.apmr.2005.11.019. [DOI] [PubMed] [Google Scholar]
  • 107.Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology. 2005;65:466–468. doi: 10.1212/01.wnl.0000173067.84247.36. [DOI] [PubMed] [Google Scholar]
  • 108.Swinnen SP. Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci. 2002;3:348–359. doi: 10.1038/nrn807. [DOI] [PubMed] [Google Scholar]
  • 109.Plewnia C, Lotze M, Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. Neuroreport. 2003;14:609–612. doi: 10.1097/00001756-200303240-00017. [DOI] [PubMed] [Google Scholar]
  • 110.Schambra HM, Sawaki L, Cohen LG. Modulation of excitability of human motor cortex (M1) by 1 Hz transcranial magnetic stimulation of the contralateral M1. Clin Neurophysiol. 2003;114:130–133. doi: 10.1016/s1388-2457(02)00342-5. [DOI] [PubMed] [Google Scholar]
  • 111.Kobayashi M, Hutchinson S, Schlaug G, Pascual-Leone A. Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to inter-hemispheric interactions. Neuroimage. 2003;20:2259–2270. doi: 10.1016/s1053-8119(03)00220-9. [DOI] [PubMed] [Google Scholar]
  • 112.Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke. 2005;36:2681–2686. doi: 10.1161/01.STR.0000189658.51972.34. [DOI] [PubMed] [Google Scholar]
  • 113.Mansur CG, Fregni F, Boggio PS, et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology. 2005;64:1802–1804. doi: 10.1212/01.WNL.0000161839.38079.92. [DOI] [PubMed] [Google Scholar]
  • 114.Naeser MA, Martin PI, Nicholas M, et al. Improved picture naming in chronic aphasia after TMS to part of right Broca’s area: an open-protocol study. Brain Lang. 2005;93:95–105. doi: 10.1016/j.bandl.2004.08.004. [DOI] [PubMed] [Google Scholar]
  • 115.Naeser MA, Martin PI, Nicholas M, et al. Improved naming after TMS treatments in a chronic, global aphasia patient-case report. Neurocase. 2005;11:182–193. doi: 10.1080/13554790590944663. [DOI] [PMC free article] [PubMed] [Google Scholar]

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