Non-invasive Brain Stimulation (NIBS) in Motor Recovery After Stroke: Concepts to Increase Efficacy

Abstract

Purpose of Review

Non-invasive brain stimulation (NIBS) is a promising tool for promoting motor recovery after stroke. However, the effects of NIBS on functional recovery are heterogeneous and not yet satisfactory in the majority of the patients. Thus, there is a strong need for further development of NIBS-based interventions with the aim of increasing the efficacy on motor recovery. Here, we review the up-to-date use of NIBS in motor rehabilitation, discuss the results critically and provide an outlook on novel NIBS strategies.

Recent Findings

So far, mainly NIBS to the primary motor cortex as a ‘one suits all’ strategy has been used to enhance motor recovery. It did not achieve satisfactory effects on motor recovery.

Summary

Current NIBS-based approaches applied to enhance motor recovery after stroke led to heterogeneous and not yet satisfactory effects in patients. To achieve more homogeneous improvements with maximal magnitude, it is necessary to change the strategy from imprecision medicine approaches towards patient-tailored precision medicine approaches that take into account the specifics of each individual patient. To accomplish this, it is mandatory to define systems-neuroscience ‘biomarkers’ allowing to stratify the patients towards individualized treatment.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.

    Rathore SS, Hinn AR, Cooper LS, Tyroler HA, Rosamond WD. Characterization of incident stroke signs and symptoms: findings from the atherosclerosis risk in communities study. Stroke. 2002;33(11):2718–21. doi:10.1161/01.str.0000035286.87503.31.

    Article  PubMed  Google Scholar 

  2. 2.

    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):845–50. doi:10.1016/j.clinph.2005.12.003.

    Article  PubMed  Google Scholar 

  3. 3.

    Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety of TMSCG. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120(12):2008–39. doi:10.1016/j.clinph.2009.08.016.

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Bikson M, Grossman P, Thomas C, Zannou AL, Jiang J, Adnan T, et al. Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimul. 2016;9(5):641–61. doi:10.1016/j.brs.2016.06.004.

    Article  PubMed  Google Scholar 

  5. 5.

    Hummel FC, Celnik P, Pascual-Leone A, Fregni F, Byblow WD, Buetefisch CM, et al. Controversy: noninvasive and invasive cortical stimulation show efficacy in treating stroke patients. Brain Stimul. 2008;1(4):370–82. doi:10.1016/j.brs.2008.09.003.

    Article  PubMed  Google Scholar 

  6. 6.

    Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128(Pt 3):490–9. doi:10.1093/brain/awh369.

    Article  PubMed  Google Scholar 

  7. 7.

    Stagg CJ, Bachtiar V, O'Shea J, Allman C, Bosnell RA, Kischka U, et al. Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke. Brain. 2012;135(Pt 1):276–84. doi:10.1093/brain/awr313.

    Article  PubMed  Google Scholar 

  8. 8.

    Grefkes C, Fink GR. Noninvasive brain stimulation after stroke: it is time for large randomized controlled trials! Curr Opin Neurol. 2016;29(6):714–20. doi:10.1097/WCO.0000000000000395.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Wessel MJ, Zimerman M, Hummel FC. Non-invasive brain stimulation: an interventional tool for enhancing behavioral training after stroke. Front Hum Neurosci. 2015;9:265. doi:10.3389/fnhum.2015.00265.

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Lindenberg R, Zhu LL, Ruber T, Schlaug G. Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging. Hum Brain Mapp. 2012;33(5):1040–51. doi:10.1002/hbm.21266.

    Article  PubMed  Google Scholar 

  11. 11.

    Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. The PREP algorithm predicts potential for upper limb recovery after stroke. Brain. 2012;135(Pt 8):2527–35. doi:10.1093/brain/aws146.

    Article  PubMed  Google Scholar 

  12. 12.

    Zimerman M, Heise KF, Hoppe J, Cohen LG, Gerloff C, Hummel FC. Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke. 2012;43(8):2185–91. doi:10.1161/STROKEAHA.111.645382.

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after scute ischemic stroke. Neurology. 2005;65:466–8.

    Article  PubMed  Google Scholar 

  14. 14.

    Ameli M, Grefkes C, Kemper F, Riegg FP, Rehme AK, Karbe H, et al. 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(3):298–309. doi:10.1002/ana.21725.

    Article  PubMed  Google Scholar 

  15. 15.

    Nowak DA, Grefkes C, Dafotakis M, Eickhoff S, Küst J, Karbe H, et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol. 2008;65(6):741–7.

    Article  PubMed  Google Scholar 

  16. 16.

    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(9):838–46. doi:10.1177/1545968311413906.

    Article  PubMed  Google Scholar 

  17. 17.

    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. 2013;20(1):202–4. doi:10.1111/j.1468-1331.2012.03703.x.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    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(12):2681–6. doi:10.1161/01.STR.0000189658.51972.34.

    Article  PubMed  Google Scholar 

  19. 19.

    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;40(4):298–303. doi:10.2340/16501977-0181.

    Article  PubMed  Google Scholar 

  20. 20.

    Grefkes C, Fink GR. Connectivity-based approaches in stroke and recovery of function. Lancet Neurol. 2014;13(2):206–16. doi:10.1016/s1474-4422(13)70264-3.

    Article  PubMed  Google Scholar 

  21. 21.

    Grefkes C, Ward N. Cortical reorganization after stroke: how much and how functional? Neuroscientist. 2014;20(1):56–70. doi:10.1177/1073858413491147.

    Article  PubMed  Google Scholar 

  22. 22.

    Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain. 2003;126(Pt 11):2476–96. doi:10.1093/brain/awg245.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Rehme AK, Eickhoff SB, Wang LE, Fink GR, Grefkes C. Dynamic causal modeling of cortical activity from the acute to the chronic stage after stroke. NeuroImage. 2011;55(3):1147–58. doi:10.1016/j.neuroimage.2011.01.014.

    Article  PubMed  Google Scholar 

  24. 24.

    Rehme AK, Fink GR, von Cramon DY, Grefkes C. The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. Cereb Cortex. 2011;21(4):756–68. doi:10.1093/cercor/bhq140.

    Article  PubMed  Google Scholar 

  25. 25.

    Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. 2006;129(Pt 3):809–19. doi:10.1093/brain/awl002.

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Rose DK, Patten C, McGuirk TE, Lu X, Triggs WJ. Does inhibitory repetitive transcranial magnetic stimulation augment functional task practice to improve arm recovery in chronic stroke? Stroke Res Treat. 2014;2014:305236. doi:10.1155/2014/305236.

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Tedesco Triccas L, Burridge JH, Hughes AM, Pickering RM, Desikan M, Rothwell JC, et al. Multiple sessions of transcranial direct current stimulation and upper extremity rehabilitation in stroke: a review and meta-analysis. Clin Neurophysiol. 2016;127(1):946–55. doi:10.1016/j.clinph.2015.04.067.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Graef P, Dadalt ML, Rodrigues DA, Stein C, Pagnussat AS. Transcranial magnetic stimulation combined with upper-limb training for improving function after stroke: a systematic review and meta-analysis. J Neurol Sci. 2016;369:149–58. doi:10.1016/j.jns.2016.08.016.

    Article  PubMed  Google Scholar 

  29. 29.

    Elsner B, Kugler J, Pohl M, Mehrholz J. Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Database Syst Rev. 2013;11:CD009645. doi:10.1002/14651858.CD009645.pub2.

    Google Scholar 

  30. 30.

    Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol. 2006;5(8):708–12. doi:10.1016/s1474-4422(06)70525-7.

    Article  PubMed  Google Scholar 

  31. 31.

    Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48(5):1398–403.

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Stefan K, Kunesch E, Cohen L, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000;123:572–84.

    Article  PubMed  Google Scholar 

  33. 33.

    Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45(2):201–6. doi:10.1016/j.neuron.2004.12.033.

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1(3):206–23. doi:10.1016/j.brs.2008.06.004.

    Article  PubMed  Google Scholar 

  35. 35.

    Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;527(3):633–9.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Antal A, Boros K, Poreisz C, Chaieb L, Terney D, Paulus W. Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul. 2008;1(2):97–105. doi:10.1016/j.brs.2007.10.001.

    Article  PubMed  Google Scholar 

  37. 37.

    Antal A, Paulus W. Transcranial alternating current stimulation (tACS). Front Hum Neurosci. 2013;7:317. doi:10.3389/fnhum.2013.00317.

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Hallett M. Transcranial magnetic stimulation: a primer. Neuron. 2007;55(2):187–99. doi:10.1016/j.neuron.2007.06.026.

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Ziemann U. Thirty years of transcranial magnetic stimulation: where do we stand? Exp Brain Res. 2017;235(4):973–84. doi:10.1007/s00221-016-4865-4.

    Article  PubMed  Google Scholar 

  40. 40.

    Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 2004;55:400–9.

    Article  PubMed  Google Scholar 

  41. 41.

    Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. Transcallosal inhibition in chronic subcortical stroke. NeuroImage. 2005;28(4):940–6. doi:10.1016/j.neuroimage.2005.06.033.

    Article  PubMed  Google Scholar 

  42. 42.

    •• Volz LJ, Rehme AK, Michely J, Nettekoven C, Eickhoff SB, Fink GR, et al. Shaping early reorganization of neural networks promotes motor function after stroke. Cereb Cortex. 2016;26(6):2882–94. doi:10.1093/cercor/bhw034. The study demonstrated an alternation of motor network connectivity and its association with better motor outcome after the combination of intermittent theta-burst stimulation and physiotherapy on 5 consecutive days. The study suggests the importance of motor network connectivity for stroke recovery.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Grefkes C, Nowak DA, Wang LE, Dafotakis M, Eickhoff SB, Fink GR. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. NeuroImage. 2010;50(1):233–42. doi:10.1016/j.neuroimage.2009.12.029.

    Article  PubMed  Google Scholar 

  44. 44.

    Ackerley SJ, Stinear CM, Barber PA, Byblow WD. Combining theta burst stimulation with training after subcortical stroke. Stroke. 2010;41(7):1568–72. doi:10.1161/STROKEAHA.110.583278.

    Article  PubMed  Google Scholar 

  45. 45.

    Marquez J, van Vliet P, McElduff P, Lagopoulos J, Parsons M. Transcranial direct current stimulation (tDCS): does it have merit in stroke rehabilitation? A systematic review. Int J Stroke. 2015;10(3):306–16. doi:10.1111/ijs.12169.

    Article  PubMed  Google Scholar 

  46. 46.

    Rehme AK, Eickhoff SB, Rottschy C, Fink GR, Grefkes C. Activation likelihood estimation meta-analysis of motor-related neural activity after stroke. NeuroImage. 2012;59(3):2771–82. doi:10.1016/j.neuroimage.2011.10.023.

    Article  PubMed  Google Scholar 

  47. 47.

    Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. NeuroImage. 2004;23(3):827–39. doi:10.1016/j.neuroimage.2004.07.058.

    Article  PubMed  Google Scholar 

  48. 48.

    Volz LJ, Sarfeld AS, Diekhoff S, Rehme AK, Pool EM, Eickhoff SB, et al. Motor cortex excitability and connectivity in chronic stroke: a multimodal model of functional reorganization. Brain Struct Funct. 2015;220:1093–107. doi:10.1007/s00429-013-0702-8.

    Article  PubMed  Google Scholar 

  49. 49.

    Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Kust J, Karbe H, et al. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol. 2008;63(2):236–46. doi:10.1002/ana.21228.

    Article  PubMed  Google Scholar 

  50. 50.

    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(22):6096–102. doi:10.1523/JNEUROSCI.4564-05.2006.

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Bradnam LV, Stinear CM, Barber PA, Byblow WD. Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cereb Cortex. 2012;22(11):2662–71. doi:10.1093/cercor/bhr344.

    Article  PubMed  Google Scholar 

  52. 52.

    Park CH, Chang WH, Ohn SH, Kim ST, Bang OY, Pascual-Leone A, et al. Longitudinal changes of resting-state functional connectivity during motor recovery after stroke. Stroke. 2011;42(5):1357–62. doi:10.1161/STROKEAHA.110.596155.

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Wang L, Yu C, Chen H, Qin W, He Y, Fan F, et al. Dynamic functional reorganization of the motor execution network after stroke. Brain. 2010;133:1224–38. doi:10.1093/brain/awq043.

    Article  PubMed  Google Scholar 

  54. 54.

    Liuzzi G, Horniss V, Lechner P, Hoppe J, Heise K, Zimerman M, et al. Development of movement-related intracortical inhibition in acute to chronic subcortical stroke. Neurology. 2014;82(3):198–205. doi:10.1212/WNL.0000000000000028.

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Schulz R, Buchholz A, Frey BM, Bonstrup M, Cheng B, Thomalla G, et al. Enhanced effective connectivity between primary motor cortex and intraparietal sulcus in well-recovered stroke patients. Stroke. 2016;47(2):482–9. doi:10.1161/STROKEAHA.115.011641.

    Article  PubMed  Google Scholar 

  56. 56.

    Ward N. Assessment of cortical reorganisation for hand function after stroke. J Physiol. 2011;589(Pt 23):5625–32. doi:10.1113/jphysiol.2011.220939.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG. Reorganization of the human ipsilesional premotor cortex after stroke. Brain. 2004;127(Pt 4):747–58. doi:10.1093/brain/awh082.

    Article  PubMed  Google Scholar 

  58. 58.

    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 U S A. 2002;99(22):14518–23.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Mintzopoulos D, Astrakas LG, Khanicheh A, Konstas AA, Singhal A, Moskowitz MA, et al. Connectivity alterations assessed by combining fMRI and MR-compatible hand robots in chronic stroke. NeuroImage. 2009;47(Suppl 2):T90–7. doi:10.1016/j.neuroimage.2009.03.007.

    Article  PubMed  Google Scholar 

  60. 60.

    Wang C-C, Wang C-P, Tsai P-Y, Hsieh C-Y, Chan R-C, Yeh S-C. Inhibitory repetitive transcranial magnetic stimulation of the contralesional premotor and primary motor cortices facilitate poststroke motor recovery. Restor Neurol Neurosci. 2014;32(6):825–35.

    CAS  PubMed  Google Scholar 

  61. 61.

    Cunningham DA, Varnerin N, Machado A, Bonnett C, Janini D, Roelle S, et al. Stimulation targeting higher motor areas in stroke rehabilitation: a proof-of-concept, randomized, double-blinded placebo-controlled study of effectiveness and underlying mechanisms. Restor Neurol Neurosci. 2015;33(6):911–26. doi:10.3233/RNN-150574.

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Kim WS, Jung SH, Oh MK, Min YS, Lim JY, Paik NJ. Effect of repetitive transcranial magnetic stimulation over the cerebellum on patients with ataxia after posterior circulation stroke: a pilot study. J Rehabil Med. 2014;46(5):418–23. doi:10.2340/16501977-1802.

    Article  PubMed  Google Scholar 

  63. 63.

    Rizzo V, Siebner HS, Morgante F, Mastroeni C, Girlanda P, Quartarone A. Paired associative stimulation of left and right human motor cortex shapes interhemispheric motor inhibition based on a Hebbian mechanism. Cereb Cortex. 2009;19(4):907–15. doi:10.1093/cercor/bhn144.

    CAS  Article  PubMed  Google Scholar 

  64. 64.

    Koganemaru S, Mima T, Nakatsuka M, Ueki Y, Fukuyama H, Domen K. Human motor associative plasticity induced by paired bihemispheric stimulation. J Physiol. 2009;587(Pt 19):4629–44. doi:10.1113/jphysiol.2009.174342.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Buch ER, Johnen VM, Nelissen N, O'Shea J, Rushworth MF. Noninvasive associative plasticity induction in a corticocortical pathway of the human brain. J Neurosci. 2011;31(48):17669–79. doi:10.1523/JNEUROSCI.1513-11.2011.

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Arai N, Muller-Dahlhaus F, Murakami T, Bliem B, Lu MK, Ugawa Y, et al. State-dependent and timing-dependent bidirectional associative plasticity in the human SMA-M1 network. J Neurosci. 2011;31(43):15376–83. doi:10.1523/JNEUROSCI.2271-11.2011.

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Koch G, Ponzo V, Di Lorenzo F, Caltagirone C, Veniero D. Hebbian and anti-Hebbian spike-timing-dependent plasticity of human cortico-cortical connections. J Neurosci. 2013;33(23):9725–33. doi:10.1523/JNEUROSCI.4988-12.2013.

    CAS  Article  PubMed  Google Scholar 

  68. 68.

    Veniero D, Ponzo V, Koch G. Paired associative stimulation enforces the communication between interconnected areas. J Neurosci. 2013;33(34):13773–83. doi:10.1523/JNEUROSCI.1777-13.2013.

    CAS  Article  PubMed  Google Scholar 

  69. 69.

    Chao CC, Karabanov AN, Paine R, Carolina de Campos A, Kukke SN, Wu T, et al. Induction of motor associative plasticity in the posterior parietal cortex-primary motor network. Cereb Cortex. 2015;25(2):365–73. doi:10.1093/cercor/bht230.

    Article  PubMed  Google Scholar 

  70. 70.

    •• Schulz R, Koch P, Zimerman M, Wessel M, Bonstrup M, Thomalla G, et al. Parietofrontal motor pathways and their association with motor function after stroke. Brain. 2015;138(Pt 7):1949–60. doi:10.1093/brain/awv100. The study assessed, using DTI, the influence of structural connectivity on residual motor function in chronic stroke patients. The study demonstrated that, in addition to the CST integrity, a significant contribution of cortico-cortical connectivity to residual motor function, suggesting the importance of cortico-cortical connectivity for stroke recovery, especially between the ventral premotor cortex and the primary motor cortex.

    Article  PubMed  Google Scholar 

  71. 71.

    • Horn U, Grothe M, Lotze M. MRI biomarkers for hand-motor outcome prediction and therapy monitoring following stroke. Neural Plast. 2016;2016:9265621. doi:10.1155/2016/9265621. This review discusses the importance of determining MRI-based biomarkers for better therapy approaches as well as neuro-rehabilitation.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Koch PJ, Hummel FC. Toward precision medicine: tailoring interventional strategies based on noninvasive brain stimulation for motor recovery after stroke. Curr Opin Neurol. 2017; doi:10.1097/WCO.0000000000000462.

  73. 73.

    O'Shea J, Boudrias MH, Stagg CJ, Bachtiar V, Kischka U, Blicher JU, et al. Predicting behavioural response to TDCS in chronic motor stroke. NeuroImage. 2014;85(Pt 3):924–33. doi:10.1016/j.neuroimage.2013.05.096.

    Article  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Chang WH, Uhm KE, Shin Y, Pascual-Leone A, Kim YH. Factors influencing the response to high-frequency repetitive transcranial magnetic stimulation in patients with subacute stroke. Restor Neurol Neurosci. 2016;34(5):747–55.

    PubMed  Google Scholar 

  75. 75.

    Kim D-Y, Lim J-Y, Kang EK, You DS, Oh M-K, Oh B-M, et al. Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil. 2010;89(11):879–86. doi:10.1097/PHM.0b013e3181f70aa7.

    Article  PubMed  Google Scholar 

  76. 76.

    Frost SB, Barbay S, Friel KM, Plautz EJ, Nudo RJ. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J Neurophysiol. 2003;89:3205–14.

    CAS  Article  PubMed  Google Scholar 

  77. 77.

    Dancause N, Barbay S, Frost SB, Zoubina EV, Plautz EJ, Mahnken JD, et al. Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. J Neurophysiol. 2006;96(6):3506–11. doi:10.1152/jn.00792.2006.

    Article  PubMed  Google Scholar 

  78. 78.

    Ward NS, Newton JM, Swayne OB, Lee L, Frackowiak RS, Thompson AJ, et al. The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke. Eur J Neurosci. 2007;25(6):1865–73. doi:10.1111/j.1460-9568.2007.05434.x.

    Article  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Schulz R, Park E, Lee J, Chang W, Lee A, Kim YH, et al. Interactions between the corticospinal tract and premotor-motor pathways in stroke recovery. Stroke. in press

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Correspondence to Friedhelm C. Hummel.

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Takuya Morishita and Friedhelm C. Hummel declare that they have no conflicts of interest. Dr. Friedhelm Hummel is supported by the Defitech foundation and the Wyss Foundation.

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Morishita, T., Hummel, F.C. Non-invasive Brain Stimulation (NIBS) in Motor Recovery After Stroke: Concepts to Increase Efficacy. Curr Behav Neurosci Rep 4, 280–289 (2017). https://doi.org/10.1007/s40473-017-0121-x

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Keywords

  • Non-invasive brain stimulation
  • Transcranial magnetic stimulation
  • Transcranial direct current stimulation
  • Stroke recovery
  • Clinical application