New modalities of brain stimulation for stroke rehabilitation

Experimental Brain Research

Volumn 224, Issue 3, 2013, Pages 335-358

  Edwardson, M A ^a   Lucas, T H ^b   Carey, J R ^c   Fetz, E E ^d  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Activity dependent; Epidural cortical stimulation; Motor cortex; Stroke rehabilitation; Transcranial direct current stimulation; Transcranial magnetic stimulation

Indexed keywords

ARTICLE; BRAIN DEPTH STIMULATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; EPIDURAL CORTICAL STIMULATION; HUMAN; INTERMETHOD COMPARISON; MOTOR CORTEX; NERVE CELL PLASTICITY; PRIORITY JOURNAL; REHABILITATION CARE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

BRAIN; ELECTRIC STIMULATION THERAPY; FUNCTIONAL LATERALITY; HUMANS; RECOVERY OF FUNCTION; STROKE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84873735203     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-012-3315-1     Document Type: Article

References (163)

1. Abraham WC (2008) Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 9:387-399
2. Ackerley SJ, Stinear CM, Barber PA, Byblow WD (2010) Combining theta burst stimulation with training after subcortical stroke. Stroke 41:1568-1572
3. Adkins DL, Campos P, Quach D et al (2006) Epidural cortical stimulation enhances motor function after sensorimotor cortical infarcts in rats. Exp Neurol 200:356-370
4. Adkins DL, Hsu JE, Jones TA (2008) Motor cortical stimulation promotes synaptic plasticity and behavioral improvements following sensorimotor cortex lesions. Exp Neurol 212:14-28
5. Adkins-Muir DL, Jones TA (2003) Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol Res 25:780-788
6. Ameli M, Grefkes C, Kemper F et al (2009) Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke. Ann Neurol 66:298-309
7. Baba T, Kameda M, Yasuhara T et al (2009) Electrical stimulation of the cerebral cortex exerts antiapoptotic, angiogenic, and anti-inflammatory effects in ischemic stroke rats through phosphoinositide 3-kinase/Akt signaling pathway. Stroke 40:e598-e605
8. Baker SN, Olivier E, Lemon RN (1995) Task-related variation in corticospinal output evoked by transcranial magnetic stimulation in the macaque monkey. J Physiol 488:795-801
9. Barker A, Jalinous R, Freeston I (1985) Non-invasive magnetic stimulation of the human motor cortex. Lancet 1:1106-1107
10. Bezard E, Boraud T, Nguyen JP et al (1999) Cortical stimulation and epileptic seizure: a study of the potential risk in primates. Neurosurgery 45:346-350
11. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472
12. Bi G, Poo M (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Ann Rev Neurosci 24:139-166
13. Bienenstock E, Cooper L, Munro P (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48
14. Bindman L, Lippold O (1964) The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J Physiol 172:369-382
15. Boggio PS, Nunes A, Rigonatti SP et al (2007) Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor Neurol Neurosci 25:123-129
16. Bolognini N, Pascual-Leone A, Fregni F (2009) Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil 6:8
17. Bolognini N, Vallar G, Casati C et al (2011) Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabil Neural Repair 25:819-829
18. Bradnam LV, Stinear CM, Barber PA, Byblow WD (2011) Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cereb Cortex. doi: 10.1093/cercor/bhr344
19. Brown P (1994) Pathophysiology of spasticity. J Neurol Neurosurg Psychol 57:773-777
20. Brown JA, Lutsep H, Cramer SC, Weinand M (2003) Motor cortex stimulation for enhancement of recovery after stroke: case report. Neurol Res 25:815-818
21. Brown JA, Lutsep HL, Weinand M, Cramer SC (2006) Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery 58:464-473
22. Buetefisch C, Heger R, Schicks W et al (2011) Hebbian-type stimulation during robot-assisted training in patients with stroke. Neurorehabil Neural Repair 25:645-655
23. Bütefisch CM, Khurana V, Kopylev L, Cohen LG (2004) Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation. J Neurophys 91:2110-2116
24. Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Ann Rev Neurosci 31:25-46
25. Carey JR, Kimberley TJ, Lewis SM et al (2002) Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125:773-788
26. Carey JR, Anderson DC, Gillick BT et al (2010) 6-Hz primed low-frequency rTMS to contralesional M1 in two cases with middle cerebral artery stroke. Neurosci Lett 469:338-342
27. Celnik P, Paik NJ, Vandermeeren Y et al (2009) Effects of combined peripheral nerve stimulation and brain polarization on performance of a motor sequence task after chronic stroke. Stroke 40:1764-1771
28. Chang WH, Kim YH, Bang OY et al (2010) Long-term effects of rTMS on motor recovery in patients after subacute stroke. J Rehabil Med 42:758-764
29. Chang WH, Kim YH, Yoo WK et al (2012) rTMS with motor training modulates cortico-basal ganglia-thalamocortical circuits in stroke patients. Restor Neurol Neurosci 31:1-11
30. Cheeran B, Cohen L, Dobkin B (2009) The future of restorative neurosciences in stroke: driving the translational research pipeline from basic science to rehabilitation of people after stroke. Neurorehabil Neural Repair 23:97-107
31. Chen R, Classen J, Gerloff C et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398-1403
32. Conforto AB, Anjos SM, Saposnik G et al (2011) Transcranial magnetic stimulation in mild to severe hemiparesis early after stroke: a proof of principle and novel approach to improve motor function. J Neurol 259:1399-1405
33. Cramer SC (2008) Repairing the human brain after stroke: I Mechanisms of spontaneous recovery. Ann Neurol 63:272-287
34. Cramer SC, Crafton KR (2006) Somatotopy and movement representation sites following cortical stroke. Exp Brain Res 168:25-32
35. Crammond DJ, Kalaska JF (2000) Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. J Neurophys 84:986-1005
36. Dafotakis M, Grefkes C, Eickhoff SB et al (2008) Effects of rTMS on grip force control following subcortical stroke. Exp Neurol 211:407-412
37. Dahl AE, Askim T, Stock R et al (2008) Short- and long-term outcome of constraint-induced movement therapy after stroke: a randomized controlled feasibility trial. Clin Rehabil 22:436-447
38. DiLazzaro V, Restuccia D, Oliviero A et al (1998) Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 119:265-268
39. DiLazzaro V, Dileone M, Pilato F et al (2011) Modulation of motor cortex neuronal networks by rTMS: comparison of local and remote effects of six different protocols of stimulation. J Neurophys 105:2150-2156
40. Edwardson M, Fetz EE, Avery DH (2011) Seizure produced by 20 Hz transcranial magnetic stimulation during isometric muscle contraction in a healthy subject. Clin Neurophysiol 122:2326-2327
41. Emara TH, Moustafa RR, Elnahas NM et al (2010) Repetitive transcranial magnetic stimulation at 1 and 5 Hz produces sustained improvement in motor function and disability after ischaemic stroke. Eur J Neurol 17:1203-1209
42. Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45-56
43. Ferbert A, Priori A, Rothwell J, Day B (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525-546
44. Fetz E, Nishimura Y, Eaton R, Perlmutter S (2010) Primate corticospinal connections can be strengthened by prolonged spike-triggered stimulation of spinal cord during free behavior. Program No. 899.2 2010 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2010. Online
45. Fregni F, Boggio PS, Mansur CG et al (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. NeuroReport 16:1551-1555
46. Fregni F, Boggio PS, Valle AC et al (2006) A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 37:2115-2122
47. Fricke K, Seeber AA, Thirugnanasambandam N et al (2011) Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J Neurophys 105:1141-1149
48. Fritsch B, Reis J, Martinowich K, Schambra H (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66:198-204
49. Furubayashi T, Terao Y, Arai N et al (2008) Short and long duration transcranial direct current stimulation (tDCS) over the human hand motor area. Exp Brain Res 185:279-286
50. Geroin C, Picelli A, Munari D et al (2011) Combined transcranial direct current stimulation and robot-assisted gait training in patients with chronic stroke: a preliminary comparison. Clin Rehabil 25:537-548
51. Grefkes C, Eickhoff SB, Nowak DA et al (2008a) Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. NeuroImage 41:1382-1394
52. Grefkes C, Nowak DA, Eickhoff SB et al (2008b) Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:236-246
53. Harvey RL, Winstein CJ (2009) Design for the Everest randomized trial of cortical stimulation and rehabilitation for arm function following stroke. Neurorehabil Neural Repair 23:32-44
54. Hausmann A, Weis C, Marksteiner J et al (2000) Chronic repetitive transcranial magnetic stimulation enhances c-fos in the parietal cortex and hippocampus. Brain Res Mol Brain Res 76:355-362
55. Hebb DO (1949) The organization of behavior. A neuropsychological theory. Wiley, New York
56. Hesse S, Werner C, Schonhardt EM et al (2007) Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: a pilot study. Restor Neurol Neurosci 25:9-15
57. Hesse S, Waldner A, Mehrholz J et al (2011) Combined transcranial direct current stimulation and robot-assisted arm training in subacute stroke patients: an exploratory, randomized multicenter trial. Neurorehabil Neural Repair 25:838-846
58. Hlustík P, Mayer M (2006) Paretic hand in stroke: from motor cortical plasticity research to rehabilitation. Cogn Behav Neurol 19:34-40
59. Hsu WY, Cheng CH, Liao KK et al (2012) Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke 43:1849-1857
60. Hsu YF, Huang YZ, Lin YY et al (2012) Intermittent theta burst stimulation over ipsilesional primary motor cortex of subacute ischemic stroke patients: a pilot study. Brain Stim. doi: 10.1016/j.brs.2012.04.007
61. Huang YZ, Edwards MJ, Rounis E et al (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201-206
62. Huang M, Harvey RL, Stoykov ME et al (2008) Cortical stimulation for upper limb recovery following ischemic stroke: a small phase II pilot study of a fully implanted stimulator. Top Stroke Rehabil 15:160-172
63. Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18:563-570
64. Hummel F, Celnik P, Giraux P et al (2005) Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain 128:490-499
65. Islam N, Moriwaki A, Hattori Y et al (1995) c-Fos expression mediated by N-methyl-D-aspartate receptors following anodal polarization in the rat brain. Exp Neurol 133:25-31
66. Jackson A, Mavoori J, Fetz EE (2006) Long-term motor cortex plasticity induced by an electronic neural implant. Nature 444:56-60
67. Jung P, Ziemann U (2009) Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J Neurosci 29:5597-5604
68. Kakuda W, Abo M, Kaito N et al (2010a) Six-day course of repetitive transcranial magnetic stimulation plus occupational therapy for post-stroke patients with upper limb hemiparesis: a case series study. Disabil Rehabil 32:801-807
69. Kakuda W, Abo M, Kobayashi K et al (2010b) Low-frequency repetitive transcranial magnetic stimulation and intensive occupational therapy for poststroke patients with upper limb hemiparesis: preliminary study of a 15-day protocol. Int J Rehabil Res 33:339-345
70. Kakuda W, Abo M, Kobayashi K et al (2011a) Combination treatment of low-frequency rTMS and occupational therapy with levodopa administration: an intensive neurorehabilitative approach for upper limb hemiparesis after stroke. Int J Neurosci 121:373-378
71. Kakuda W, Abo M, Kobayashi K et al (2011b) Application of combined 6-Hz primed low-frequency rTMS and intensive occupational therapy for upper limb hemiparesis after stroke. NeuroRehabilitation 29:365-371
72. Kakuda W, Abo M, Kobayashi K et al (2011c) Baseline severity of upper limb hemiparesis influences the outcome of low-frequency rTMS combined with intensive occupational therapy in patients who have had a stroke. Phys Med Rehabil 3:516-522
73. Kakuda W, Abo M, Kobayashi K et al (2011d) Anti-spastic effect of low-frequency rTMS applied with occupational therapy in post-stroke patients with upper limb hemiparesis. Brain Inj 25:496-502
74. Kakuda W, Abo M, Momosaki R et al (2011e) Combined therapeutic application of botulinum toxin type A, low-frequency rTMS, and intensive occupational therapy for post-stroke spastic upper limb hemiparesis. Eur J Phys Med Rehabil 47:1-9
75. Kakuda W, Abo M, Shimizu M et al (2012) A multi-center study on low-frequency rTMS combined with intensive occupational therapy for upper limb hemiparesis in post-stroke patients. J Neuroeng Rehabil 9:1-11
76. Khedr EM, Ahmed MA, Fathy N, Rothwell JC (2005) Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 65:466-468
77. Khedr EM, Abdel-Fadeil MR, Farghali A, Qaid M (2009) Role of 1 and 3 Hz repetitive transcranial magnetic stimulation on motor function recovery after acute ischaemic stroke. Eur J Neurol 16:1323-1330
78. Khedr EM, Etraby AE, Hemeda M et al (2010) Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke. Acta Neurol Scand 121:30-37
79. Kim YH, You SH, Ko MH et al (2006) Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 37:1471-1476
80. Kim DY, Ohn SH, Yang EJ et al (2009) Enhancing motor performance by anodal transcranial direct current stimulation in subacute stroke patients. Am J Phys Med Rehabil 88:829-836
81. Kim DY, Lim JY, Kang EK et al (2010) Effect of transcranial direct current stimulation on motor recovery in patients with subacute stroke. Am J Phys Med Rehabil 89:879-886
82. Kirton A, Chen R, Friefeld S et al (2008) Contralesional repetitive transcranial magnetic stimulation for chronic hemiparesis in subcortical paediatric stroke: a randomised trial. Lancet Neurol 7:507-513
83. Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophys 80:3321-3325
84. Kleim JA, Bruneau R, VandenBerg P et al (2003) Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol Res 25:789-793
85. Kleim JA, Hogg TM, VandenBerg PM et al (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24:628-633
86. Kleim JA, Chan S, Pringle E et al (2006) BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9:735-737
87. Koganemaru S, Mima T, Thabit MN et al (2010) Recovery of upper-limb function due to enhanced use-dependent plasticity in chronic stroke patients. Brain 133:3373-3384
88. Lemon R (1979) Short-latency peripheral inputs to the motor cortex in conscious monkeys. Brain Res 161:150-155
89. Levy R, Ruland S, Weinand M et al (2008) Cortical stimulation for the rehabilitation of patients with hemiparetic stroke: a multicenter feasibility study of safety and efficacy. J Neurosurg 108:707-714
90. Liepert J, Zittel S, Weiller C (2007) 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 25:461-465
91. Lindberg PG, Gäverth J, Fagergren A et al (2009) Cortical activity in relation to velocity dependent movement resistance in the flexor muscles of the hand after stroke. Neurorehabil Neural Repair 23:800-810
92. Lindenberg R, Renga V, Zhu LL et al (2010) Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients. Neurology 75:2176-2184
93. Lindenberg R, Zhu LL, Schlaug G (2012) Combined central and peripheral stimulation to facilitate motor recovery after stroke: the effect of number of sessions on outcome. Neurorehabil Neural Repair 26:479-483
94. Lucas T (2009) Activity-dependent motor cortex reorganization induced with recurrent intracortical stimulation triggered from forelimb muscles. University of Washington, Dissertation
95. Lucas T, Fetz E (2011) Neuroprosthetic myo-cortical feedback induces reorganization of motor cortex output. Program No. 84.12/RR. 2011 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2011. Online
96. Madhavan S, Weber KA, Stinear JW (2011) Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation. Exp Brain Res 209:9-17
97. Maeda F, Keenan JP, Tormos JM et al (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800-805
98. Mahmoudi H, Borhani Haghighi A, Petramfar P et al (2011) Transcranial direct current stimulation: electrode montage in stroke. Disabil Rehabil 33:1383-1388
99. Malcolm MP, Triggs WJ, Light KE et al (2007) Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial. Am J Phys Med Rehabil 86:707-715
100. Mansur CG, Fregni F, Boggio PS et al (2005) A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64:1802-1804
101. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215
102. McNeil J, Binette J (2001) Prevalence of disabilities and associated health conditions among adults - United States, 1999. Morb Mortal Wkly Rep 50:120-125
103. Meehan SK, Dao E, Linsdell MA, Boyd LA (2011) Continuous theta burst stimulation over the contralesional sensory and motor cortex enhances motor learning post-stroke. Neurosci Lett 500:26-30
104. Meliza CD, Dan Y (2006) Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49:183-189
105. Moliadze V, Zhao Y, Eysel U, Funke K (2003) Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 553:665-679
106. Moon SK, Shin YI, Kim HI et al (2009) Effect of prolonged cortical stimulation differs with size of infarct after sensorimotor cortical lesions in rats. Neurosci Lett 460:152-155
107. Morrell MJ (2011) Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology 77:1295-1304
108. Mrachacz-Kersting N, Kristensen SR, Niazi IK, Farina D (2012) Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity. J Physiol 590:1669-1682
109. Müller-Dahlhaus F, Ziemann U, Classen J (2010) Plasticity resembling spike-timing dependent synaptic plasticity: the evidence in human cortex. Front Synaptic Neurosci 2:34
110. Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400-409
111. Murphy J, Kwan H, MacKay W, Wong Y (1982) Activity of primate precentral neurons during voluntary movements triggered by visual signals. Brain Res 236:429-449
112. Nair DG, Renga V, Lindenberg R et al (2011) Optimizing recovery potential through simultaneous occupational therapy and non-invasive brain-stimulation using tDCS. Restor Neurol Neurosci 29:1-10
113. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(Pt 3):633-639
114. Nouri S, Cramer SC (2011) Anatomy and physiology predict response to motor cortex stimulation after stroke. Neurology 77:1076-1083
115. Nowak L, Bregestovski P, Ascher P (1984) Magnesium gates glutamate-activated channels in mouse central neurons. Nature 307:462-465
116. Nowak DA, Grefkes C, Dafotakis M et al (2008) 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 65:741-747
117. Nowak DA, Bösl K, Podubeckà J, Carey JR (2010) Noninvasive brain stimulation and motor recovery after stroke. Restor Neurol Neurosci 28:531-544
118. Pascual-Leone A, Valls-Solé J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847-858
119. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389-443
120. Plautz EJ, Barbay S, Frost SB et al (2003) Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurol Res 25:801-810
121. Plow EB, Carey JR, Nudo RJ, Pascual-Leone A (2009) Invasive cortical stimulation to promote recovery of function after stroke: a critical appraisal. Stroke 40:1926-1931
122. Priori A, Berardelli A, Rona S (1998) Polarization of the human motor cortex through the scalp. NeuroReport 9:2257-2260
123. Purpura DP, McMurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophys 28:166-185
124. Rebesco JM, Stevenson IH, Körding KP et al (2010) Rewiring neural interactions by micro-stimulation. Front Syst Neurosci 4:1-15
125. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008-2039
126. Rossi C, Sallustio F, Di Legge S et al (2012) Transcranial direct current stimulation of the affected hemisphere does not accelerate recovery of acute stroke patients. Eur J Neurol. doi: 10.1111/j.1468-1331.2012.03703.x
127. Roth Y, Amir A, Levkovitz Y, Zangen A (2007) Three-dimensional distribution of the electric field induced in the brain by transcranial magnetic stimulation using figure-8 and deep H-coils. J Clin Neurophysiol 24:31-38
128. Sasaki N, Mizutani S, Kakuda W, Abo M (2011) Comparison of the Effects of High- and Low-frequency Repetitive Transcranial Magnetic Stimulation on Upper Limb Hemiparesis in the Early Phase of Stroke. J Stroke Cerebrovasc Dis. doi: 10.1016/j.jstrokecerebrovasdis.2011.10.004
129. Seniów J, Bilik M, Lesniak M et al (2012) Transcranial magnetic stimulation combined with physiotherapy in rehabilitation of poststroke hemiparesis: a randomized, double-blind, placebo-controlled study. Neurorehabil Neural Repair 26:1072-1079
130. Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37-53
131. Stagg CJ, Bachtiar V, O'Shea J et al (2012) Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke. Brain 135:276-284
132. Stanslaski S, Afshar P, Cong P et al (2012) Design and validation of a fully implantable, chronic, closed-loop neuromodulation device with concurrent sensing and stimulation. IEEE Trans Neural Syst Rehabil Eng 20:410-421
133. Stefan K, Kunesch E, Cohen LG et al (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572-584
134. Takeuchi N, Chuma T, Matsuo Y et al (2005) Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36:2681-2686
135. Takeuchi N, Tada T, Toshima M et al (2008) 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 40:298-303
136. Takeuchi N, Tada T, Toshima M et al (2009) Repetitive transcranial magnetic stimulation over bilateral hemispheres enhances motor function and training effect of paretic hand in patients after stroke. J Rehabil Med 41:1049-1054
137. Talelli P, Greenwood RJ, Rothwell JC (2007) Exploring Theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol 118:333-342
138. Talelli P, Wallace A, Dileone M et al (2012) Theta burst stimulation in the rehabilitation of the upper Limb: a semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil Neural Repair 26:976-987
139. Tanaka S, Takeda K, Otaka Y et al (2011) Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke. Neurorehabil Neural Repair 25:565-569
140. Teskey GC, Monfils MH, VandenBerg PM, Kleim JA (2002) Motor map expansion following repeated cortical and limbic seizures is related to synaptic potentiation. Cereb Cortex 12:98-105
141. Teskey GC, Flynn C, Goertzen CD et al (2003) Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol Res 25:794-800
142. Thabit MN, Ueki Y, Koganemaru S et al (2010) Movement-related cortical stimulation can induce human motor plasticity. J Neurosci 30:11529-11536
143. Theilig S, Podubecka J, Bösl K et al (2011) Functional neuromuscular stimulation to improve severe hand dysfunction after stroke: does inhibitory rTMS enhance therapeutic efficiency? Exp Neurol 230:149-155
144. Thickbroom GW (2007) Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res 180:583-593
145. Thielscher A, Wichmann FA (2009) Determining the cortical target of transcranial magnetic stimulation. NeuroImage 47:1319-1330
146. Todd G, Flavel SC, Ridding MC (2006) Low-intensity repetitive transcranial magnetic stimulation decreases motor cortical excitability in humans. J Appl Physiol 101:500-505
147. Trepel C, Racine RJ (1998) Long-term potentiation in the neocortex of the adult, freely moving rat. Cereb Cortex 8:719-729
148. Tsubokawa T, Katayama Y, Yamamoto T et al (1993) Chronic motor cortex stimulation in patients with thalamic pain. J Neurosurg 78:393-401
149. Vines BW, Cerruti C, Schlaug G (2008) Dual-hemisphere tDCS facilitates greater improvements for healthy subjects' non-dominant hand compared to uni-hemisphere stimulation. BMC neuroscience 9:103
150. Wang HY, Crupi D, Liu J et al (2011) Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J Neurosci 31:11044-11054
151. Wang RY, Tseng HY, Liao KK et al (2011) rTMS combined with task-oriented training to improve symmetry of interhemispheric corticomoto excitability and gait performance after stroke: a randomized trial. Neurorehabil Neural Repair 26:222-230
152. Wassermann EM, Mcshane LM, Hallett M, Cohen LG (1992) Noninvasive mapping of muscle representations in motor cortex. Electroencephalogr Clin Neurophsiol 85:1-8
153. Weiss SR, Eidsath A, Li XL et al (1998) Quenching revisited: low level direct current inhibits amygdala-kindled seizures. Exp Neurol 154:185-192
154. Wolf SL, Winstein CJ, Miller J et al (2006) Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA 296:2095-2104
155. Wolters A, Sandbrink F, Schlottmann A et al (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophys 89:2339-2345
156. Wu D, Qian L, Zorowitz RD et al (2012) Effects on decreasing upper-limb post-stroke muscle tone using transcranial direct current stimulation: a randomized sham-controlled study. Arch Phys Med Rehab. doi: 10.1016/j.apmr.2012. 07.022
157. Yamamoto T, Katayama Y, Watanabe M et al (2011) Changes in motor function induced by chronic motor cortex stimulation in post-stroke pain patients. Stereot Funct Neuros 89:381-389
158. Yoon KJ, Lee YT, Han TR (2011) Mechanism of functional recovery after repetitive transcranial magnetic stimulation (rTMS) in the subacute cerebral ischemic rat model: neural plasticity or anti-apoptosis? Exp Brain Res 214:549-556
159. Yoon KJ, Oh B-M, Kim D-Y (2012) Functional improvement and neuroplastic effects of anodal transcranial direct current stimulation (tDCS) delivered 1 day vs. 1 week after cerebral ischemia in rats. Brain Res 1452:61-72
160. Yozbatiran N, Alonso-Alonso M, See J et al (2009) Safety and behavioral effects of high-frequency repetitive transcranial magnetic stimulation in stroke. Stroke 40:309-312
161. Zemke AC, Heagerty PJ, Lee C, Cramer SC (2003) Motor cortex organization after stroke is related to side of stroke and level of recovery. Stroke 34:e23-e28
162. Zhang L, Tao H, Holt C et al (1998) A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37-44
163. Zhou Q, Zhang Q, Zhao X et al (2010) Cortical electrical stimulation alone enhances functional recovery and dendritic structures after focal cerebral ischemia in rats. Brain Res 1311:148-157