BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 1, Issue 4 , Pages 370-382 , October 2008

Controversy: Noninvasive and invasive cortical stimulation show efficacy in treating stroke patients

  • Friedhelm C. Hummel, MD

      Affiliations

    • Brain Imaging and Neurostimulation Lab, Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    • ,
  • Pablo Celnik, MD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, Department of Neurology, Johns Hopkins University, Baltimore, Maryland
    • ,
  • Alvero Pascual-Leone, MD

      Affiliations

    • Berenson-Allen Center for Noninvasive Brain Stimulation, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachussets
    • ,
  • Felipe Fregni, MD, PhD

      Affiliations

    • Berenson-Allen Center for Noninvasive Brain Stimulation, Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, Massachussets
    • ,
  • Winston D. Byblow, MD

      Affiliations

    • Movement Neuroscience Laboratory, Department of Sport & Exercise Science, University of Auckland, Auckland, New Zealand
    • ,
  • Cathrin M. Buetefisch, MD

      Affiliations

    • Neurological Therapeutic Center, Heinrich-Heine University Dusseldorf, Germany
    • ,
  • John Rothwell, MD

      Affiliations

    • Department of Neurology, Department of Physiology, West Virginia University, Morgantown, West Virginia
    • ,
  • Leonardo G. Cohen, MD

      Affiliations

    • Human Cortical Physiology Section and Stroke Neurorehabilitation Clinic, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland
    • ,
  • Christian Gerloff, MD

      Affiliations

    • Brain Imaging and Neurostimulation Lab, Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    • Corresponding Author InformationCorrespondence: Christian Gerloff, MD, Department of Neurology, University Medical Center Hamburg-Eppendorf, Martinistr, 52 20246 Hamburg, Germany.

Received 9 June 2008 ,Revised 3 September 2008 ,Accepted 5 September 2008.

References 

  1. Kapur N. Paradoxical functional facilitation in brain-behaviour research: a critical review. Brain. 1996;119(Pt 5):1775–1790
  2. French B, Thomas LH, Leathley MJ, et al. Repetitive task training for improving functional ability after stroke. Cochrane Database Syst Rev. 2007;(4):CD006073
  3. Pollock A, Baer GD, Langhorne P, Pomeroy VM. Physiotherapy treatment approaches for stroke [published online ahead of print January 10, 2008]. Stroke doi:0000.
  4. Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke?. Lancet Neurol. 2006;5(8):708–712
  5. McDonnell MN, Hillier SL, Miles TS, Thompson PD, Ridding MC. Influence of combined afferent stimulation and task-specific training following stroke: a pilot randomized controlled trial. Neurorehabil Neural Repair. 2007;21(5):435–443
  6. Celnik P, Hummel F, Harris-Love M, Wolk R, Cohen LG. Somatosensory stimulation enhances the effects of training functional hand tasks in patients with chronic stroke. Arch Phys Med Rehabil. 2007;88(11):1369–1376
  7. Scheidtmann K, Fries W, Muller F, Koenig E. Effect of levodopa in combination with physiotherapy on functional motor recovery after stroke: a prospective, randomised, double-blind study. Lancet. 2001;358(9284):787–790
  8. Volpe BT, Lynch D, Rykman-Berland A, et al. Intensive sensorimotor arm training mediated by therapist or robot improves hemiparesis in patients with chronic stroke. Neurorehabil Neural Repair. 2008;22(3):305–310
  9. Stinear CM, Barber PA, Coxon JP, Fleming MK, Byblow WD. Priming the motor system enhances the effects of upper limb therapy in chronic stroke. Brain. 2008;131(Pt 5):1381–1390
  10. 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
  11. Hummel F, Cohen LG. Improvement of motor function with noninvasive cortical stimulation in a patient with chronic stroke. Neurorehabil Neural Repair. 2005;19(1):14–19
  12. Hummel FC, Voller B, Celnik P, et al. Effects of brain polarization on reaction times and pinch force in chronic stroke. BMC Neurosci. 2006;7:73
  13. 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):2681–2686
  14. 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
  15. Takeuchi N, Toshima M, Chuma T, Matsuo Y, Ikoma K. Repetitive transcranial magnetic stimulation of the unaffected hemisphere in a patient who was forced to use the affected hand. Am J Phys Med Rehabil. 2008;87(1):74–77
  16. 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(10):1802–1804
  17. Martin PI, Naeser MA, Theoret H, et al. Transcranial magnetic stimulation as a complementary treatment for aphasia. Semin Speech Lang. 2004;25(2):181–191
  18. Fregni F, Boggio PS, Valle AC, et al. A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke. 2006;37(8):2115–2122
  19. Fregni F, Boggio PS, Mansur CG, et al. Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport. 2005;16(14):1551–1555
  20. Boggio PS, Alonso-Alonso M, Mansur CG, et al. Hand function improvement with low-frequency repetitive transcranial magnetic stimulation of the unaffected hemisphere in a severe case of stroke. Am J Phys Med Rehabil. 2006;85(11):927–930
  21. 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;37(6):1471–1476
  22. Khedr EM, Ahmed MA, Fathy N, Rothwell JC. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology. 2005;65(3):466–468
  23. Brown JA, Lutsep H, Cramer SC, Weinand M. Motor cortex stimulation for enhancement of recovery after stroke: case report. Neurol Res. 2003;25(8):815–818
  24. 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(3):464–473
  25. Huang M, Harvey RL, Stoykov ME, et al. Cortical stimulation for upper limb recovery following ischemic stroke: a small phase II pilot study of a fully implanted stimulator. Top Stroke Rehabil. 2008;15(2):160–172
  26. Shadmehr R, Wise SP. Computational neurobiology of reaching and pointing: a foundation for motor learning. Cambridge, MA: MIT Press; 2005;
  27. Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. [see comments] Science. 1996;272(5269):1791–1794
  28. Reis J, Robertson E, Krakauer JW, et al. Controversy: cant DCS and TMS enhance motor learning and memory formation? [published online before print October 2008.] Brain Stimulation doi:10.1016/j.brs.2008.09.003.
  29. Pascual-Leone A, Amedi A, Fregni F, Merabet LB. The plastic human brain cortex. Annu Rev Neurosci. 2005;28:377–401
  30. Siebner HR, Rothwell J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res. 2003;148(1):1–16
  31. Wassermann EM, Grafman J. Recharging cognition with DC brain polarization. Trends Cogn Sci. 2005;9(11):503–505
  32. Talelli P, Rothwell J. Does brain stimulation after stroke have a future?. Curr Opin Neurol. 2006;19(6):543–550
  33. Alonso-Alonso M, Fregni F, Pascual-Leone A. Brain stimulation in poststroke rehabilitation. Cerebrovasc Dis. 2007;24(Suppl 1):157–166
  34. Butefisch CM, Khurana V, Kopylev L, Cohen LG. Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J Neurophysiol. 2004;91:2110–2116
  35. Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain. 2000;123(Pt 3):572–584
  36. Stefan K, Cohen LG, Duque J, et al. Formation of a motor memory by action observation. J Neurosci. 2005;25(41):9339–9346
  37. Bliem B, Muller-Dahlhaus JF, Dinse HR, Ziemann U. Homeostatic metaplasticity in the human somatosensory cortex. J Cogn Neurosci. 2008;20:1517–1528
  38. Muller JF, Orekhov Y, Liu Y, Ziemann U. Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur J Neurosci. 2007;25(11):3461–3468
  39. Wolters A, Sandbrink F, Schlottmann A, et al. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol. 2003;89(5):2339–2345
  40. Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. Transcallosal inhibition in chronic subcortical stroke. Neuroimage. 2005;28(4):940–946
  41. Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 2004;55(3):400–409
  42. Hilgetag CC, Theoret H, Pascual-Leone A. Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex. Nat Neurosci. 2001;4(9):953–957
  43. Kinsbourne M. Direction of gaze and distribution of cerebral thought processes. Neuropsychologia. 1974;12(2):279–281
  44. Calford MB, Tweedale R. Interhemispheric transfer of plasticity in the cerebral cortex. Science. 1990;249(4970):805–807
  45. Plewnia C, Lotze M, Gerloff C. Disinhibition of the contralateral motor cortex by low-frequency rTMS. Neuroreport. 2003;14(4):609–612
  46. 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(1):130–133
  47. Gangitano M, Valero-Cabre A, Tormos JM, Mottaghy FM, Romero JR, Pascual-Leone A. Modulation of input-output curves by low and high frequency repetitive transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol. 2002;113(8):1249–1257
  48. Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 1982;2(1):32–48
  49. Siebner HR, Lang N, Rizzo V, et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci. 2004;24(13):3379–3385
  50. Matthews PM, Johansen-Berg H, Reddy H. Non-invasive mapping of brain functions and brain recovery: applying lessons from cognitive neuroscience to neurorehabilitation. Restor Neurol Neurosci. 2004;22(3-5):245–260
  51. Ward NS. Functional reorganization of the cerebral motor system after stroke. Curr Opin Neurol. 2004;17(6):725–730
  52. Calautti C, Baron JC. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke. 2003;34(6):1553–1566
  53. Richards LG, Stewart KC, Woodbury ML, Senesac C, Cauraugh JH. Movement-dependent stroke recovery: a systematic review and meta-analysis of TMS and fMRI evidence. Neuropsychologia. 2008;46(1):3–11
  54. Talelli P, Greenwood RJ, Rothwell JC. Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol. 2006;117(8):1641–1659
  55. Shimizu T, Hosaki A, Hino T, et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain. 2002;125(Pt 8):1896–1907
  56. Adkins DL, Hsu JE, Jones TA. Motor cortical stimulation promotes synaptic plasticity and behavioral improvements following sensorimotor cortex lesions. Exp Neurol. 2008;212:14–28
  57. Adkins DL, Campos P, Quach D, Borromeo M, Schallert K, Jones TA. Epidural cortical stimulation enhances motor function after sensorimotor cortical infarcts in rats. Exp Neurol. 2006;200(2):356–370
  58. Adkins-Muir DL, Jones TA. Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol Res. 2003;25(8):780–788
  59. Kleim JA, Bruneau R, VandenBerg P, MacDonald E, Mulrooney R, Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol Res. 2003;25(8):789–793
  60. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain. 2003;126(Pt 11):2476–2496
  61. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Longitudinal changes in cerebral response to proprioceptive input in individual patients after stroke: an FMRI study. Neurorehabil Neural Repair. 2006;20(3):398–405
  62. Ward NS, Newton JM, Swayne OB, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. 2006;129(Pt 3):809–819
  63. Butefisch CM, Wessling M, Netz J, Seitz RJ, Homberg V. Relationship between interhemispheric inhibition and motor cortex excitability in subacute stroke patients. Neurorehabil Neural Repair. 2008;22(1):4–21
  64. Cicinelli P, Traversa R, Rossini PM. Post-stroke reorganization of brain motor output to the hand: a 2-4 month follow-up with focal magnetic transcranial stimulation. Electroencephalogr Clin Neurophysiol. 1997;105(6):438–450
  65. Braun C, Staudt M, Schmitt C, Preissl H, Birbaumer N, Gerloff C. Crossed cortico-spinal motor control after capsular stroke. Eur J Neurosci. 2007;25(9):2935–2945
  66. Gerloff C, Bushara K, Sailer A, et al. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain. 2006;129(Pt 3):791–808
  67. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain. 2003;126(Pt 6):1430–1448
  68. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. The influence of time after stroke on brain activations during a motor task. Ann Neurol. 2004;55(6):829–834
  69. 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(8):794–800
  70. Levy R, Ruland S, Weinand M, Lowry D, Dafer R, Bakay R. Cortical stimulation for the rehabilitation of patients with hemiparetic stroke: a multicenter feasibility study of safety and efficacy. J Neurosurg. 2008;108(4):707–714
  71. Wagner T, Fregni F, Eden U, et al. Transcranial magnetic stimulation and stroke: a computer-based human model study. Neuroimage. 2006;30(3):857–870
  72. 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. Restor Neurol Neurosci. 2007;25(2):123–129
  73. 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):6096–6102
  74. Ward NS. The neural substrates of motor recovery after focal damage to the central nervous system. Arch Phys Med Rehabil. 2006;87(12 Suppl 2):S30–S35
  75. Dancause N, Barbay S, Frost SB, Mahnken JD, Nudo RJ. Interhemispheric connections of the ventral premotor cortex in a new world primate. J Comp Neurol. 2007;505(6):701–715
  76. Dancause N, Barbay S, Frost SB, et al. Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cereb Cortex. 2006;16(8):1057–1068
  77. Dancause N, Barbay S, Frost SB, et al. Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. J Neurophysiol. 2006;96(6):3506–3511
  78. Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77(4-5):677–682
  79. Dum RP, Strick PL. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci. 2005;25(6):1375–1386
  80. Davare M, Lemon R, Olivier E. Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J Physiol. 2008;586(Pt 11):2735–2742
  81. 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(6):3205–3214
  82. 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):747–758
  83. 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):14518–14523
  84. 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(4):464–472
  85. Newton JM, Ward NS, Parker GJ, et al. Non-invasive mapping of corticofugal fibres from multiple motor areas—relevance to stroke recovery. Brain. 2006;129(Pt 7):1844–1858
  86. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. 2007;130(Pt 1):170–180
  87. 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
  88. Hummel FC, Cohen LG. Drivers of brain plasticity. Curr Opin Neurol. 2005;18(6):667–674
  89. Wagner T, Valero-Cabre A, Pascual-Leone A. Noninvasive human brain stimulation. Annu Rev Biomed Eng. 2007;9:527–565
  90. Nitsche MA, Cohen LG, Wassermann E, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimulation. 2008;1:206–223
  91. Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406(6792):147–150
  92. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG. Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. Brain. 1997;120(Pt 9):1587–1602
  93. Nitsche MA, Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol. 2000;3(527 Pt):633–639
  94. Nitsche MA, Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57(10):1899–1901
  95. Nitsche MA, Seeber A, Frommann K, et al. Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex. J Physiol. 2005;568:291–303
  96. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45(2):201–206
  97. Plewnia C, Reimold M, Najib A, et al. Dose-dependent attenuation of auditory phantom perception (tinnitus) by PET-guided repetitive transcranial magnetic stimulation. Hum Brain Mapp. 2007;28(3):238–246
  98. Brown JA. Recovery of motor function after stroke. Prog Brain Res. 2006;157:223–228
  99. Hiscock A, Miller S, Rothwell J, Tallis RC, Pomeroy VM. Informing dose-finding studies of repetitive transcranial magnetic stimulation to enhance motor function: a qualitative systematic review. Neurorehabil Neural Repair. 2008;22(3):228–249
  100. Sohn YH, Hallett M. Surround inhibition in human motor system. Exp Brain Res. 2004;158(4):397–404
  101. Voller B, St Clair Gibson A, Lomarev M, et al. Long-latency afferent inhibition during selective finger movement. J Neurophysiol. 2005;94(2):1115–1119
  102. Gerachshenko T, Rymer WZ, Stinear JW. Abnormal corticomotor excitability assessed in biceps brachii preceding pronator contraction post-stroke. Clin Neurophysiol. 2008;119(3):683–692
  103. Nitsche MA, Liebetanz D, Tergau F, Paulus W. [Modulation of cortical excitability by transcranial direct current stimulation]. Nervenarzt. 2002;73(4):332–335
  104. 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
  105. Liepert J, Zittel S, Weiller C. Improvement of dexterity by single session low-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex in acute stroke: a double-blind placebo-controlled crossover trial. Restor Neurol Neurosci. 2007;25(5-6):461–465
  106. Talelli P, Greenwood RJ, Rothwell JC. Exploring theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol. 2007;118(2):333–342
  107. Kirton A, Chen R, Friefeld S, Gunraj C, Pontigon AM, Deveber G. Contralesional repetitive transcranial magnetic stimulation for chronic hemiparesis in subcortical paediatric stroke: a randomised trial. Lancet Neurol. 2008;7(6):507–513
  108. Feys H, De Weerdt W, Verbeke G, et al. Early and repetitive stimulation of the arm can substantially improve the long-term outcome after stroke: a 5-year follow-up study of a randomized trial. Stroke. 2004;35(4):924–929
  109. Duncan PW, Lai SM, Keighley J. Defining post-stroke recovery: implications for design and interpretation of drug trials. Neuropharmacology. 2000;39(5):835–841
  110. Wood-Dauphinee S, Shapiro S, Bass E, et al. A randomized trial of team care following stroke. Stroke. 1984;15(5):864–872
  111. Wood-Dauphinee SL, Williams JI, Shapiro SH. Examining outcome measures in a clinical study of stroke. Stroke. 1990;21(5):731–739
  112. Gladstone DJ, Danells CJ, Armesto A, et al. Physiotherapy coupled with dextroamphetamine for rehabilitation after hemiparetic stroke: a randomized, double-blind, placebo-controlled trial. Stroke. 2006;37(1):179–185
  113. Duncan P, Studenski S, Richards L, et al. Randomized clinical trial of therapeutic exercise in subacute stroke. Stroke. 2003;34(9):2173–2180
  114. Martinsson L, Eksborg S, Wahlgren NG. Intensive early physiotherapy combined with dexamphetamine treatment in severe stroke: a randomized, controlled pilot study. Cerebrovasc Dis. 2003;16(4):338–345
  115. Kwakkel G, Kollen B, Twisk J. Impact of time on improvement of outcome after stroke. Stroke. 2006;37(9):2348–2353
  116. Hesse S, Werner C, Schonhardt EM, Bardeleben A, Jenrich W, Kirker SG. Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: a pilot study. Restor Neurol Neurosci. 2007;25(1):9–15
  117. Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA. An objective and standardized test of hand function. Arch Phys Med Rehabil. 1969;50(6):311–319
  118. Wolf SL, McJunkin JP, Swanson ML, Weiss PS. Pilot normative database for the Wolf Motor Function Test. Arch Phys Med Rehabil. 2006;87(3):443–445
  119. Wolf SL, Winstein CJ, Miller JP, et al. Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA. 2006;296(17):2095–2104
  120. Malcolm MP, Triggs WJ, Light KE, et al. Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial. Am J Phys Med Rehabil. 2007;86(9):707–715
  121. Kuo MF, Paulus W, Nitsche MA. Boosting focally-induced brain plasticity by dopamine. Cereb Cortex. 2008;18(3):648–651
  122. Nitsche MA, Lampe C, Antal A, et al. Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur J Neurosci. 2006;23(6):1651–1657
  123. Nitsche MA, Jaussi W, Liebetanz D, Lang N, Tergau F, Paulus W. Consolidation of human motor cortical neuroplasticity by D-cycloserine. Neuropsychopharmacology. 2004;29(8):1573–1578
  124. Ertelt D, Small S, Solodkin A, et al. Action observation has a positive impact on rehabilitation of motor deficits after stroke. Neuroimage. 2007;36(Suppl 2):T164–T173
  125. Celnik P, Webster B, Glasser DM, Cohen LG. Effects of action observation on physical training after stroke. Stroke. 2008;39:1814–1820
  126. Ward NS. Neural plasticity and recovery of function. Prog Brain Res. 2005;150:527–535
  127. Kim WK, Choi YB, Rayudu PV, et al. Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO. Neuron. 1999;24(2):461–469

PII: S1935-861X(08)00336-7

doi: 10.1016/j.brs.2008.09.003

BRAIN STIMULATION: Basic, Translational, and Clinical Research in Neuromodulation
Volume 1, Issue 4 , Pages 370-382 , October 2008

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