Abstract
Stroke is the major cause of disability; nonetheless, cerebral plasticity mechanisms carry out different strategies to compensate the brain damage; therefore, the understanding of these processes are crucial for optimizing clinical and functional recovery. In the last decade, there has been remarkable progress in unraveling the pathophysiological mechanisms leading to altered motor function, speech disorder and visuo-spatial impairment especially by applying neuromodulation techniques such as non-invasive brain stimulation (NIBS). Accordingly, several approaches have been performed in order to directly verify the efficacy of NIBS in improving these altered functions. Here, we summarize the main neurophysiological findings in the field of post-stroke recovery and especially the major results obtained from application of NIBS in the acute and chronic phase of stroke patients.
This is a preview of subscription content, log in via an institution.
References
Ameli M, Grefkes C, Kemper F, Riegg FP, Rehme AK, Karbe H, Fink GR, Nowak DA. Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke. Ann Neurol. 2009;66:298–309.
Barwood CH, Murdoch BE, Whelan B-M, Lloyd D, Riek S, O’Sullivan JD, Coulthard A, Wong A. Improved language performance subsequent to low-frequency rTMS in patients with chronic non-fluent aphasia post-stroke. Eur J Neurol. 2011;18:935–43.
Boggio PS, Nunes A, Rigonatti SP, Nitsche MA, Pascual-Leone A, Fregni F. Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restorative Neurol Neurosci. 2007;25:123–9.
Bolognini N, Vallar G, Casati C, Abdul Latif L, El-Nazer R, Williams J, Banco E, et al. Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabil Neural Repair. 2011;25:819–29.
Brighina F, Bisiach E, Oliveri M, Piazza A, La Bua V, Daniele O, Fierro B. 1 Hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neurosci Lett. 2003;336:131–3.
Cazzoli D, Müri RM, Schumacher R, von Arx S, Chaves S, Gutbrod K, et al. Theta burst stimulation reduces disability during the activities of daily living in spatial neglect. Brain. 2012;135:3426–39.
Chang WH, Kim Y-H, Bang OY, Kim ST, Park YH, Lee PKW. Long-term effects of rTMS on motor recovery in patients after subacute stroke. J Rehabil Med. 2010;428:758–64.
Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48:1398–403.
Conforto AB, Anjos SM, Saposnik G, Mello EA, Nagaya EM, Santos W, Ferreiro KN, Melo ES, Reis FI, Scaff M, Cohen LG. Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol. 2011.
Di Lazzaro V, Pilato F, Saturno E, Oliviero A, Dileone M, Mazzone P, Insola A, Tonali PA, Ranieri F, Huang YZ, Rothwell JC. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol. 2005;565:945–50.
Ellison A, Schindler I, Pattison LL, Milner AD. An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain. 2004;127:2307–15.
Floel A, Hummel F, Duque J, Knecht S, Cohen LG. Influence of somatosensory input on interhemispheric interactions in patients with chronic stroke. Neurorehabil Neural Repair. 2008;22(5):477–85.
Flöel A, Meinzer M, Kirstein R, Nijhof S, Deppe M, Knecht S, Breitenstein C. Short-term anomia training and electrical brain stimulation. Stroke. 2011;427:2065–7.
Fregni FBPS, Mansur CG, Wagner T, Ferreira MJL, Lima MC, Rigonatti SP, et al. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. NeuroReport. 2005;1614:1551–5.
Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira MJ, Wagner T, Fecteau S, Rigonatti SP, Riberto M, Freedman SD, Pascual-Leone A. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke. 2006;378:2115–22.
Fregni F, Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol. 2007;3(7):383–93. Review.
Fridriksson J, Bonilha L, Baker JM, Moser D, Rorden C. Activity in preserved left hemisphere regions predicts anomia severity in aphasia. Cereb Cortex. 2010;205:1013–9.
Fridriksson J, Richardson JD, Baker JM, Rorden C. Transcranial direct current stimulation improves naming reaction time in fluent aphasia: a doubleblind, sham-controlled study. Stroke. 2011;423:819–21.
Hallett M. Transcranial magnetic stimulation: a primer. Neuron. 2007;552:187–99.
Hausmann A, Weis C, Marksteiner J, Hinterhuber H, Humpel C. Chronic repetitive transcranial magnetic stimulation enhances c-fos in the parietal cortex and hippocampus. Brain Res. 2000;762:355–62.
Hesse S, Waldner A, Mehrholz J, Tomelleri C, Pohl M, Werner C. Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: an exploratory, randomized multicenter trial. Neurorehabil Neural Repair. 2011;25:838–46.
Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;452:201–6.
Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol. 2006;58:708–12.
Hummel FC, Celnik P, Pascual-Leone A, Fregni F, Byblow WD, Buetefisch CM, Rothwell J, Cohen LG, Gerloff C. Controversy: noninvasive and invasive cortical stimulation show efficacy in treating stroke patients. Brain Stimul. 2008;14:370–82.
Karnath HO, Rennig J, Johannsen L, Rorden C. The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain. 2011;134:903–12.
Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology. 2005;653:466–8.
Kim Y-H, You SH, Ko M-H, Park J-W, Lee KH, Jang SH, Yoo W-K, Hallett M. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke. 2006;376:1471–6.
Kim D-Y, Lim J-Y, Kang EK, You DS, Oh M-K, Oh B-M, Paik N-J. Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil. 2010;8911:879–86.
Kim BR, Chun MH, Kim DY, Lee SJ. Effect of high- and low-frequency repetitive transcranial magnetic stimulation on visuospatial neglect in patients with acute stroke: a double-blind, sham-controlled trial. Arch Phys Med Rehabil. 2013;94:803–7.
Koch G, Oliveri M, Cheeran B, Ruge D, Lo Gerfo E, Salerno S, Torriero S, Marconi B, Mori F, Driver J, Rothwell JC, Caltagirone C. Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. Brain. 2008;131:3147–55.
Koch G, Cercignani M, Bonnì S, Giacobbe V, Bucchi G, Versace V, Caltagirone C, Bozzali M. Asymmetry of parietal interhemispheric connections in humans. J Neurosci. 2011;31(24):8967–75.
Koch G, Bonnì S, Giacobbe V, Bucchi G, Basile B, Lupo F, Versace V, Bozzali M, Caltagirone C. Theta-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology. 2012;78:24–30.
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;125Pt(10):2238–47.
Lim JY, Kang EK, Paik N-J. Repetitive transcranial magnetic stimulation to hemispatial neglect in patients after stroke: an open-label pilot study. J Rehabil Med. 2010;425:447–52.
Lindenberg R, Renga V, Zhu LL, Nair D, Schlaug G. Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology. 2010;7524:2176–84.
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;2622:6096–102.
Mansur CG, Fregni F, Boggio PS, Riberto M, Gallucci-Neto J, Santos CM, Wagner T, Rigonatti SP, Marcolin MA, Pascual-Leone A. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology. 2005;6410:1802–4.
Monti A, Cogiamanian F, Marceglia S, Ferrucci R, Mameli F, Mrakic-Sposta S, Vergari M, Zago S, Priori A. Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatry. 2008;794:451–3.
Müller MB, Toschi N, Kresse AE, Post AKM. Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology. 2000;232:205–15.
Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527:633–9.
Nitsche MA, Jaussi W, Liebetanz D, Lang N, Tergau F, Paulus W. Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology. 2004;298:1573–8.
Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;13:206–23.
Nowak D, Grefkes C, Ameli M, Fink GR. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabil Neural Repair. 2009;23:641–56.
Nyffeler T, Cazzoli D, Hess CW, Müri RM. One session of repeated parietal theta burst stimulation trains induces long-lasting improvement of visual neglect. Stroke. 2009;408:2791–6.
Oliveri M, Rossini PM, Traversa R, Cicinelli P, Filippi MM, Pasqualetti P, Tomaiuolo F, Caltagirone C. Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain. 1999;122:1731–9.
Oliveri M, Bisiach E, Brighina F, Piazza A, La Bua V, Buffa D, Fierro B. rTMS of the unaffected hemisphere transiently reduces contralesional visuospatial hemineglect. Neurology. 2001a;577:1338–40.
Oliveri M, Bisiach E, Brighina F, Piazza A, La Bua V, Buffa D, et al. rTMS of the unaffected hemisphere transiently reduces contralesional visuospatial hemineglect. Neurology. 2001b;57:1338–40.
Paulus W. Transcranial direct current stimulation tDCS. Suppl Clin Neurophysiol. 2003;56:249–54.
Pedersen PM, Vinter K, Olsen TS. Aphasia after stroke: type, severity and prognosis. Copenhagen aphasia study. Cerebrovasc Dis. 2004;171:35–43.
Plautz EJ, Barbay S, Frost SB, Friel KM, Dancause N, Zoubina EV, Stowe AM, Quaney BM, Nudo RJ. Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurol Res. 2003;258:801–10.
Rossi C, Sallustio F, Di Legge S, Stanzione P, Koch G. Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur J Neurol. 2012.
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;12012:2008–203.
Schlaug G, Marchina S, Wan CY. The use of non-invasive brain stimulation techniques to facilitate recovery from post-stroke aphasia. Neuropsychol Rev. 2011;213:288–301.
Shindo K, Sugiyama K, Huabao L, Nishijima K, Kondo T, Izumi S. Long-term effect of low-frequency repetitive transcranial magnetic stimulation over the unaffected posterior parietal cortex in patients with unilateral spatial neglect. J Rehabil Med. 2006;38:65–7.
Song W, Du B, Xu Q, Hu J, Wang M, Luo Y. Low-frequency transcranial magnetic stimulation for visual spatial neglect: a pilot study. J Rehabil Med. 2009;41:162–5.
Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kincses ZT, Morris PG, Matthews PM, Johansen-Berg H. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci. 2009;2916:5202–6.
Stagg CJ, Bestmann S, Constantinescu AO, Moreno LM, Allman C, Mekle R, Woolrich M, Near J, Johansen-Berg H, Rothwell JC. Relationship between physiological measures of excitability and levels of glutamate and GABA in the human motor cortex. J Physiol. 2011;589:5845–55.
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;3612:2681–6.
Takeuchi N, Tada T, Toshima M, Chuma T, Matsuo Y, Ikoma K. Inhibition of the unaffected motor cortex by 1 Hz repetitive transcranical magnetic stimulation enhances motor performance and training effect of the paretic hand in patients with chronic stroke. J Rehabil Med. 2008;404:298–303.
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;4113:1049–54.
Traversa R, Cicinelli P, Pasqualetti P, Filippi M, Rossini PM. Follow-up of interhemispheric differences of motor evoked potentials from the ‘affected’ and ‘unaffected’ hemispheres in human stroke. Brain Res. 1998;803:1–8.
Weiduschat N, Thiel A, Rubi-Fessen I, Hartmann A, Kessler J, Merl P, Kracht L, Rommel T, Heiss WD. Effects of repetitive transcranial magnetic stimulation in aphasic stroke: a randomized controlled pilot study. Stroke. 2011;422:409–15.
You DS, Kim D-Y, Chun MH, Jung SE, Park SJ. Cathodal transcranial direct current stimulation of the right Wernicke’s area improves comprehension in subacute stroke patients. Brain Lang. 2011;1191:1–5.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Di Lorenzo, F., Koch, G. (2017). Integrated Methods of Neuromodulation for Guiding Recovery Following Stroke. In: Petrosini, L. (eds) Neurobiological and Psychological Aspects of Brain Recovery. Contemporary Clinical Neuroscience. Springer, Cham. https://doi.org/10.1007/978-3-319-52067-4_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-52067-4_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-52065-0
Online ISBN: 978-3-319-52067-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)