A review of transcranial magnetic stimulation and multimodal neuroimaging to characterize post-stroke neuroplasticity

Frontiers in Neurology

Volumn 6, Issue OCT, 2015, Pages

  Auriat, Angela M ^a   Neva, Jason L ^a   Peters, Sue ^a   Ferris, Jennifer K ^a   Boyd, Lara A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Diffusion tensor imaging; Electroencephalography; Functional MRI; Magnetic resonance spectroscopy; Multimodal neuroimaging; Sensorimotor recovery; Stroke; Transcranial magnetic stimulation

Indexed keywords

4 AMINOBUTYRIC ACID;

AREA UNDER THE CURVE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN MAPPING; BRAIN SIZE; CEREBROVASCULAR ACCIDENT; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; DORSOLATERAL PREFRONTAL CORTEX; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; EVOKED MUSCLE RESPONSE; FACILITATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; LIMB MOVEMENT; MOTOR THRESHOLD; MULTIMODAL IMAGING; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERCEPTIVE THRESHOLD; PREMOTOR CORTEX; PYRAMIDAL TRACT; RESTING STATE NETWORK; REVIEW; SENSORIMOTOR CORTEX; SOMATOSENSORY SYSTEM; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84946553659     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2015.00226     Document Type: Review

References (239)

1. The GUSTO Investigators. An international randomized trial comparing four thrombolytic strategies for acute myocardial infarction. N Engl J Med (1993) 329:673-82. doi: 10.1056/NEJM199309023291001.
2. Edwards JD, Koehoorn M, Boyd LA, Levy AR. Is health-related quality of life improving after stroke? A comparison of health utilities indices among Canadians with stroke between 1996 and 2005. Stroke (2010) 41:996-1000. doi:10.1161/STROKEAHA.109.576678.
3. Boyd LA, Winstein CJ. Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. Phys Ther (2003) 83(11):976-89.
4. Taub E, Miller NE, Novack TA, Cook EW, Fleming WC, Nepomuceno CS, et al. Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil (1993) 74:347-54.
5. Boyd LA, Winstein CJ. Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learn Mem (2004) 11:388-96. doi:10.1101/lm.80104.
6. Boyd LA, Winstein CJ. Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurorehabil Neural Repair (2004) 18:134-43. doi:10.1177/0888439004269072.
7. Boyd LA, Quaney BM, Pohl PS, Winstein CJ. Learning implicitly: effects of task and severity after stroke. Neurorehabil Neural Repair (2006) 21:444-54. doi:10.1177/1545968307300438.
8. Boyd LA, Edwards JD, Siengsukon CS, Vidoni ED, Wessel BD, Linsdell MA. Motor sequence chunking is impaired by basal ganglia stroke. Neurobiol Learn Mem (2009) 92:35-44. doi:10.1016/j.nlm.2009.02.009.
9. Vidoni ED, Boyd LA. Preserved motor learning after stroke is related to the degree of proprioceptive deficit. Behav Brain Funct (2009) 5:36. doi:10.1186/1744-9081-5-36.
10. Pohl PS, Winstein CJ. Practice effects on the less-affected upper extremity after stroke. Arch Phys Med Rehabil (1999) 80:668-75. doi:10.1016/S0003-9993(99)90170-3.
11. Winstein CJ, Merians AS, Sullivan KJ. Motor learning after unilateral brain damage. Neuropsychologia (1999) 37:975-87. doi:10.1016/S0028-3932(98)00145-6.
12. Velicki MR, Winstein CJ, Pohl PS. Impaired direction and extent specification of aimed arm movements in humans with stroke-related brain damage. Exp Brain Res (2000) 130:362-74. doi:10.1007/s002219900262.
13. Boyd LA, Vidoni ED, Daly JJ. Answering the call: the influence of neuroimaging and electrophysiological evidence on rehabilitation. Phys Ther (2007) 87:684-703. doi:10.2522/ptj.20060164.
14. Meehan SK, Randhawa B, Wessel B, Boyd LA. Implicit sequence-specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: an {fMRI} study. Hum Brain Mapp (2011) 32:290-303. doi:10.1002/hbm.21019.
15. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci (1996) 16:785-807.
16. Grefkes C, Nowak DA, EickhoffSB, Dafotakis M, Kust J, Karbe H, et al. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Annals of neurology (2008) 63:236-46. doi:10.1002/ana.21228.
17. Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science (1996) 272:1791-4. doi:10.1126/science.272.5269.1791.
18. Alexander LD, Black SE, Gao F, Szilagyi G, Danells CJ, McIlroy WE. Correlating lesion size and location to deficits after ischemic stroke: the influence of accounting for altered peri-necrotic tissue and incidental silent infarcts. Behav Brain Funct (2010) 6:6. doi:10.1186/1744-9081-6-6.
19. Sterr A, Dean PJ, Szameitat AJ, Conforto AB, Shen S. Corticospinal tract integrity and lesion volume play different roles in chronic hemiparesis and its improvement through motor practice. Neurorehabil Neural Repair (2014) 28:335-43. doi:10.1177/1545968313510972.
20. Carrera E, Tononi G. Diaschisis: past, present, future. Brain (2014) 137(Pt 9):2408-22. doi:10.1093/brain/awu101.
21. Kraemer M, Schormann T, Hagemann G. Delayed shrinkage of the brain after ischemic stroke: preliminary observations with {voxel-guided} morphometry. J Neuroimaging (2004) 14(3):265-72. doi:10.1111/j.1552-6569.2004.tb00249.x.
22. Dade LA, Gao FQ, Kovacevic N, Roy P, Rockel C, CM O, et al. Semiautomatic brain region extraction: a method of parcellating brain regions from structural magnetic resonance images. Neuroimage (2004) 22:1492-502. doi:10.1016/j.neuroimage.2004.03.023.
23. Ramirez J, Scott CJ, McNeely AA, Berezuk C, Gao F, Szilagyi GM, et al. Lesion explorer: a video-guided, standardized protocol for accurate and reliable {MRI-derived} volumetrics in Alzheimer's disease and normal elderly. J Vis Exp (2013) (86):e50887:1-12. doi:10.3791/50887.
24. Brodie SM, Borich MR, Boyd LA. Impact of 5-Hz rTMS over the primary sensory cortex is related to white matter volume in individuals with chronic stroke. Eur J Neurosci (2014) 40:3405-12. doi:10.1111/ejn.12717.
25. Naama L-C, Ramirez J, Lobaugh NJ, Black SE. Misclassified tissue volumes in Alzheimer disease patients with white matter hyperintensities: importance of lesion segmentation procedures for volumetric analysis. Stroke (2008) 39:1134-41. doi:10.1161/STROKEAHA.107.498196.
26. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage (1999) 9:179-94. doi:10.1006/nimg.1998.0395.
27. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron (2002) 33:341-55. doi:10.1016/S0896-6273(02)00569-X.
28. Jang SH. Prediction of motor outcome for hemiparetic stroke patients using diffusion tensor imaging?: a review. NeuroRehabilitation (2010) 27:367-72. doi:10.3233/NRE-2010-0621.
29. Borich MR, Mang C, Boyd LA. Both projection and commissural pathways are disrupted in individuals with chronic stroke: investigating microstructural white matter correlates of motor recovery. BMC Neurosci (2012) 13:107. doi:10.1186/1471-2202-13-107.
30. Lindenberg R, Zhu LL, Rüber T, Schlaug G. Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging. Hum Brain Mapp (2012) 33:1040-51. doi:10.1002/hbm.21266.
31. 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) 130:170-80. doi:10.1093/brain/awl333.
32. Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke. Neurology (2010) 74:280-7. doi:10.1212/WNL.0b013e3181ccc6d9.
33. Borich MR, Brown KE, Boyd LA. Motor skill learning is associated with diffusion characteristics of white matter in individuals with chronic stroke. J Neurol Phys Ther (2014) 37:1-10. doi:10.1097/NPT.0b013e3182a3d353.
34. Carey JR, Deng H, Gillick BT, Cassidy JM, Anderson DC, Zhang L, et al. Serial treatments of primed low-frequency rTMS in stroke: characteristics of responders vs. nonresponders. Restor Neurol Neurosci (2014) 32:323-35. doi:10.3233/RNN-130358.
35. Demirtas-tatlidede A, Alonso-alonso M, Shetty RP, Ronen I, Alvaro P-L, Fregni F. Long-term effects of contralesional {rTMS} in severe stroke: safety, cortical excitability, and relationship with transcallosal motor fibers. NeuroRehabilitation (2014) 36:51-9. doi:10.3233/NRE-141191.
36. Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson (1996) 111:209-19. doi:10.1006/jmrb.1996.0086.
37. Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci (2008) 34:51-61. doi:10.1007/s12031-007-0029-0.
38. Basser P. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed (1995) 8:333-44. doi:10.1002/nbm.1940080707.
39. Borich MR, Wadden KP, Boyd LA. Establishing the reproducibility of two approaches to quantify white matter tract integrity in stroke. Neuroimage (2012) 59:2393-400. doi:10.1016/j.neuroimage.2011.09.009.
40. Danielian L, Iwata N, Thomasson D, Floeter M. Reliability of fiber tracking measurements in diffusion tensor imaging for longitudinal study. Neuroimage (2011) 49:1572-80. doi:10.1016/j.neuroimage.2009.08.062.Reliability.
41. Auriat AM, Borich MR, Snow NJ, Wadden KP, Boyd LA. Comparing a diffusion tensor and non-tensor approach to white matter fiber tractography in chronic stroke. Neuroimage Clin (2015) 7:771-81. doi:10.1016/j.nicl.2015.03.007.
42. Farquharson S, Tournier JD, Calamante F, Fabinya G, Schneider-Kolsky M, Jackson GD, et al. White matter fiber tractography: why we need to move beyond DTI. J Neurosurg (2013) 118:1367-77. doi:10.3171/2013.2.JNS121294.
43. Tournier J-D, Mori S, Leemans A. Diffusion tensor imaging and beyond. Magn Reson Med (2011) 65:1532-56. doi:10.1002/mrm.22924.
44. Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex (2008) 44:936-52. doi:10.1016/j.cortex.2008.05.002.
45. Hallett M, Wassermann E, Cohen L, Chmielowska J, GerloffC. Cortical mechanisms of recovery of function after stroke. NeuroRehabilitation (1998) 10:131-42. doi:10.3233/NRE-1998-10205.
46. DavidoffR. The pyramidal tract. Neurology (1990) 40:332-9. doi:10.1212/WNL.40.2.332.
47. Takenobu Y, Hayashi T, Moriwaki H, Nagatsuka K, Naritomi H, Fukuyama H. Motor recovery and microstructural change in rubro-spinal tract in subcortical stroke. Neuroimage Clin (2014) 4:201-8. doi:10.1016/j.nicl.2013.12.003.
48. Schaechter JD, Fricker ZP, Perdue KL, Helmer KG, Vangel MG, Greve DN, et al. Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients. Hum Brain Mapp (2009) 30:3461-74. doi:10.1002/hbm.20770.
49. Cho SH, Kim DG, Kim DS, Kim YH, Lee CH, Jang SH. Motor outcome according to the integrity of the corticospinal tract determined by diffusion tensor tractography in the early stage of corona radiata infarct. Neurosci Lett (2007) 426:123-7. doi:10.1016/j.neulet.2007.08.049.
50. Cho SH, Kim SH, Choi BY, Cho SH, Kang JH, Lee CH, et al. Motor outcome according to diffusion tensor tractography findings in the early stage of intracerebral hemorrhage. Neurosci Lett (2007) 421:142-6. doi:10.1016/j.neulet.2007.04.052.
51. Schlaug G, Siewert B, Benfield A, Edelman R, Warach S. Time course of the apparent diffusion coefficient (ADC) abnormality in human stroke. Neurology (1997) 49:113-9. doi:10.1212/WNL.49.1.113.
52. Schwamm LH, Koroshetz WJ, Sorensen AG, Wang B, Copen WA, Budzik R, et al. Time course of lesion development in patients with acute stroke: serial diffusion-and hemodynamic-weighted magnetic resonance imaging. Stroke (1998) 29:2268-76. doi:10.1161/01.STR.29.11.2268.
53. Grässel D, Ringer T, Fitzek C, Fitzek S, Kohl M, Kaiser W, et al. Wallerian degeneration of pyramidal tract after paramedian pons infarct. Cerebrovasc Dis (2010) 30:380-8. doi:10.1159/000319573.
54. Groisser BN, Copen WA, Singhal AB, Hirai KK, Schaechter JD. Corticospinal tract diffusion abnormalities early after stroke predict motor outcome. Neurorehabil Neural Repair (2014) 28(8):751-60. doi:10.1177/1545968314521896.
55. Bozzali M, Mastropasqua C, Cercignani M, Giulietti G, Bonnl S, Caltagirone C, et al. Microstructural damage of the posterior corpus callosum contributes to the clinical severity of neglect. PLoS One (2012) 7:e48079. doi:10.1371/journal.pone.0048079.
56. Gujar SK, Maheshwari S, Bjorkman-Burtscher I, Sundgren PC. Magnetic resonance spectroscopy. J Neuroophthalmol (2005) 25:217-26. doi:10.1089/ars.2010.3453.
57. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, De Beer R, et al. Java-based graphical user interface for the MRUI quantitation package. MAGMA (2001) 12:141-52. doi:10.1016/S1352-8661(01)00111-9.
58. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med (1993) 30:672-9. doi:10.1002/mrm.1910300604.
59. Gruetter R, Weisdorf SA, Rajanayagan V, Terpstra M, Merkle H, Truwit CL, et al. Resolution improvements in in vivo 1H NMR spectra with increased magnetic field strength. J Magn Reson (1998) 135:260-4. doi:10.1006/jmre.1998.1542.
60. Paiva FF, Otaduy MCG, Souza RO, Moll J, Bramati IE, et al. Comparison of human brain metabolite levels using 1H MRS at 1.5T and 3.0T. Dement Neuropsychol (2013) 7:216-20.
61. Puts N, Edden R. In vivo magnetic spectroscopy of GABA: a methodological review. Prog Nucl Magn Reson Spectrosc (2012) 60:1-26. doi:10.1016/j.pnmrs.2011.06.001.In.
62. Castillo M, Kwock L, Mukherji SK. Clinical applications of proton MR spectroscopy. AJNR Am J Neuroradiol (1996) 17:1-15.
63. Kim JP, Lentz MR, Westmoreland SV, Greco JB, Ratai EM, Halpern E, et al. Relationships between astrogliosis and 1H MR spectroscopic measures of brain choline/creatine and myo-inositol/creatine in a primate model. AJNR Am J Neuroradiol (2005) 26(4):752-9.
64. Cirstea CM, Nudo RJ, Craciunas SC, Popescu EA, Choi I-Y, Lee P, et al. Neuronal-glial alterations in non-primary motor areas in chronic subcortical stroke. Brain Res (2012) 1463:75-84. doi:10.1016/j.brainres.2012.04.052.
65. Cirstea CM, Brooks WM, Craciunas SC, Popescu EA, Choi I-Y, Lee P, et al. Primary motor cortex in stroke: a functional MRI-guided proton MR spectroscopic study. Stroke (2011) 42:1004-9. doi:10.1161/STROKEAHA.110.601047.
66. Tran T, Ross B, Lin A. Magnetic resonance spectroscopy in neurological diagnosis. Neurol Clin (2009) 27:21-60. doi:10.1016/j.ncl.2008.09.007.
67. Maniega SM, Cvoro V, Armitage PA, Marshall I, Bastin ME, Wardlaw JM. Choline and creatine are not reliable denominators for calculating metabolite ratios in acute ischemic stroke. Stroke (2008) 39:2467-9. doi:10.1161/STROKEAHA.107.507020.
68. Novotny EJ, Fulbright RK, Pearl PL, Gibson KM, Rothman DL. Magnetic resonance spectroscopy of neurotransmitters in human brain. Ann Neurol (2003) 54(Suppl 6):S25-31. doi:10.1002/ana.10697.
69. Gideon P, Henriksen O, Sperling B, Christiansen P, Olsen TS, Jørgensen HS, et al. Early time course of N-acetylaspartate, creatine and phosphocreatine, and compounds containing choline in the brain after acute stroke. A proton magnetic resonance spectroscopy study. Stroke (1992) 23:1566-72. doi:10.1161/01.STR.23.11.1566.
70. Gideon P, Sperling B, Arlien-Søborg P, Olsen TS, Henriksen O. Long-term follow-up of cerebral infarction patients with proton magnetic resonance spectroscopy. Stroke (1994) 25:967-73. doi:10.1161/01.STR.25.5.967.
71. Bivard A, Krishnamurthy V, Stanwell P, Yassi N, Spratt NJ, Nilsson M, et al. Spectroscopy of reperfused tissue after stroke reveals heightened metabolism in patients with good clinical outcomes. J Cereb Blood Flow Metab (2014) 34:1944-50. doi:10.1038/jcbfm.2014.166.
72. Parsons MW, Li T, Barber PA, Yang Q, Darby DG, Desmond PM, et al. Combined 1H MR spectroscopy and diffusion-weighted MRI improves the prediction of stroke outcome. Neurology (2000) 55:498-506. doi:10.1212/WNL.55.4.498.
73. Dani KA, An L, Henning EC, Shen J, Warach S. Multivoxel MR spectroscopy in acute ischemic stroke: comparison to the stroke protocol MRI. Stroke (2012) 43:2962-7. doi:10.1161/STROKEAHA.112.656058.
74. Craciunas SC, Brooks WM, Nudo RJ, Popescu EA, Choi I-YY, Lee P, et al. Motor and premotor cortices in subcortical stroke: proton magnetic resonance spectroscopy measures and arm motor impairment. Neurorehabil Neural Repair (2013) 27(5):411-20. doi:10.1177/1545968312469835.
75. Kobayashi M, Takayama H, Suga S, Mihara B. Longitudinal changes of metabolites in frontal lobes after hemorrhagic stroke of basal ganglia: a proton magnetic resonance spectroscopy study. Stroke (2001) 32:2237-45. doi:10.1161/hs1001.096621.
76. Federico F, Simone IL, Lucivero V, Giannini P, Laddomada G, Mezzapesa DM, et al. Prognostic value of proton magnetic resonance spectroscopy in ischemic stroke. Arch Neurol (1998) 55(4):489-94. doi:10.1001/archneur.55.4.489.
77. Blicher JU, Near J, Næss-Schmidt E, Stagg CJ, Johansen-Berg H, Nielsen JF, et al. GABA levels are decreased after stroke and GABA changes during rehabilitation correlate with motor improvement. Neurorehabil Neural Repair (2015) 29:278-86. doi:10.1177/1545968314543652.
78. Liebetanz D, Fauser S, Michaelis T, Czéh B, Watanabe T, Paulus W, et al. Safety aspects of chronic low-frequency transcranial magnetic stimulation based on localized proton magnetic resonance spectroscopy and histology of the rat brain. J Psychiatr Res (2003) 37:277-86. doi:10.1016/S0022-3956(03)00017-7.
79. Luborzewski A, Schubert F, Seifert F, Danker-Hopfe H, Brakemeier EL, Schlattmann P, et al. Metabolic alterations in the dorsolateral prefrontal cortex after treatment with high-frequency repetitive transcranial magnetic stimulation in patients with unipolar major depression. J Psychiatr Res (2007) 41:606-15. doi:10.1016/j.jpsychires.2006.02.003.
80. Yang X-R, Kirton A, Wilkes TC, Pradhan S, Liu I, Jaworska N, et al. Glutamate alterations associated with transcranial magnetic stimulation in youth depression: a case series. J ECT (2014) 1-6. doi:10.1097/YCT.0000000000000094.
81. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, et al. Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol (2009) 101:2872-7. doi:10.1152/jn.91060.2008.
82. Stagg CJ, Bachtiar V, Johansen-Berg H. The role of GABA in human motor learning. Curr Biol (2011) 21:480-4. doi:10.1016/j.cub.2011.01.069.
83. Norris DG. Principles of magnetic resonance assessment of brain function. J Magn Reson Imaging (2006) 23:794-807. doi:10.1002/jmri.20587.
84. Fox MD, Greicius M. Clinical applications of resting state functional connectivity. Front Syst Neurosci (2010) 4:19. doi:10.3389/fnsys.2010.00019.
85. Auer D. Spontaneous low-frequency blood oxygenation level-dependent fluctuations and functional connectivity analysis of the "resting" brain. Magn Reson Imaging (2008) 26:1055-64. doi:10.1016/j.mri.2008.05.008.
86. Lundgren J, Flodström K, Sjögren K, Liljequist B, Fugl-Meyer AR. Site of brain lesion and functional capacity in rehabilitated hemiplegics. Scand J Rehabil Med (1982) 14:141-3.
87. Miyai I, Blau AD, Reding MJ, Volpe BT. Patients with stroke confined to basal ganglia have diminished response to rehabilitation efforts. Neurology (1997) 48:95-101. doi:10.1212/WNL.48.1.95.
88. Ju Y, Hussain M, Asmaro K, Zhao X, Liu L, Li J, et al. Clinical and imaging characteristics of isolated pontine infarcts: a one-year follow-up study. Neurol Res (2013) 35:498-504. doi:10.1179/1743132813Y.0000000207.
89. Rehme AK, Grefkes C. Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol (2012) 591:17-31. doi:10.1113/jphysiol.2012.243469.
90. Roh J, Rymer WZ, Perreault EJ, Yoo SB, Beer RF. Alterations in upper limb muscle synergy structure in chronic stroke survivors. J Neurophysiol (2013) 109:768-81. doi:10.1152/jn.00670.2012.
91. Lee MY, Choi JH, Park RJ, Kwon YH, Chang JS, Lee J, et al. Clinical characteristics and brain activation patterns of mirror movements in patients with corona radiata infarct. Eur Neurol (2010) 64:15-20. doi:10.1159/000313979.
92. Seto E, Sela G, McIlroy WE, Black SE, Staines WR, Bronskill MJ, et al. Quantifying head motion associated with motor tasks used in fMRI. Neuroimage (2001) 14:284-97. doi:10.1006/nimg.2001.0829.
93. Jung T, Kim JY, Seo JH, Jin SU, Joong Lee H, Lee S, et al. Combined information from resting-state functional connectivity and passive movements with functional magnetic resonance imaging differentiate fast late-onset motor recovery from progressive recovery in hemiplegic stroke patients: a pilot study. J Rehabil Med (2013) 45:546-52. doi:10.2340/16501977-1165.
94. Sun L, Yin D, Zhu Y, Fan M, Zang L, Wu Y, et al. Cortical reorganization after motor imagery training in chronic stroke patients with severe motor impairment: a longitudinal fMRI study. Neuroradiology (2013) 55:913-25. doi:10.1007/s00234-013-1188-z.
95. Park C, 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) 42:1357-62. doi:10.1161/STROKEAHA.110.596155.
96. Varkuti B, Guan C, Pan Y, Phua KS, Ang KK, Kuah CWK, et al. Resting state changes in functional connectivity correlate with movement recovery for BCI and robot-assisted upper-extremity training after stroke. Neurorehabil Neural Repair (2012) 27(1):53-62. doi:10.1177/1545968312445910.
97. Golestani A-MM, Tymchuk S, Demchuk A, Goodyear BG, Group V-2 S. Longitudinal evaluation of resting-state {FMRI} after acute stroke with hemiparesis. Neurorehabil Neural Repair (2013) 27:153-63. doi:10.1177/1545968312457827.
98. Carter AR, Shulman GL, Corbetta M. Why use a connectivity-based approach to study stroke and recovery of function? Neuroimage (2012) 62:2271-80. doi:10.1016/j.neuroimage.2012.02.070.
99. Ward N. Assessment of cortical reorganisation for hand function after stroke. J Physiol (2011) 589:5625-32. doi:10.1113/jphysiol.2011.220939.
100. Grefkes C, Ward NS. Cortical reorganization after stroke: how much and how functional? Neuroscientist (2014) 20:56-70. doi:10.1177/1073858413491147.
101. Boyd LA, Vidoni ED, Wessel BD. Motor learning after stroke: is skill acquisition a prerequisite for contralesional neuroplastic change? Neurosci Lett (2010) 482:21-5. doi:10.1016/j.neulet.2010.06.082.
102. Hanlon CA, Buffington AL, McKeown MJ. New brain networks are active after right {MCA} stroke when moving the ipsilesional arm. Neurology (2005) 64:114-20. doi:10.1212/01.WNL.0000148726.45458.A9.
103. Olejniczak P. Neurophysiologic basis of EEG. J Clin Neurophysiol (2006) 23:186-9. doi:10.1097/01.wnp.0000220079.61973.6c.
104. Jordan KG. Emergency EEG and continuous EEG monitoring in acute ischemic stroke. J Clin Neurophysiol (2004) 21(5):341-52.
105. Giaquinto S, Cobianchi A, Macera F, Nolfe G. EEG recordings in the course of recovery from stroke. Stroke (1994) 25:2204-9. doi:10.1161/01.STR.25.11.2204.
106. Dubovik S, Pignat JM, Ptak R, Aboulafia T, Allet L, Gillabert N, et al. The behavioral significance of coherent resting-state oscillations after stroke. Neuroimage (2012) 61:249-57. doi:10.1016/j.neuroimage.2012.03.024.
107. Finnigan SP, Walsh M, Rose SE, Chalk JB. Quantitative EEG indices of sub-acute ischaemic stroke correlate with clinical outcomes. Clin Neurophysiol (2007) 118:2525-32. doi:10.1016/j.clinph.2007.07.021.
108. Dubovik S, Ptak R, Aboulafia T, Magnin C, Gillabert N, Allet L, et al. EEG alpha band synchrony predicts cognitive and motor performance in patients with ischemic stroke. Behav Neurol (2013) 26(3):187-9. doi:10.3233/BEN-2012-129007.
109. Guggisberg AG. Two intrinsic coupling types for resting-state integration in the human brain. Brain Topogr (2015) 28:318-29. doi:10.1007/s10548-014-0394-2.
110. Pellegrino G, Pellegrino G, Tombini M, Assenza G, Bravi M, Sterzi S, et al. Inter-hemispheric coupling changes associate with motor improvements after robotic stroke rehabilitation. Restor Neurol Neurosci (2012) 30:497-510. doi:10.3233/RNN-2012-120227.
111. Di Lazzaro V, Ziemann U. The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front Neural Circuits (2013) 7:18. doi:10.3389/fncir.2013.00018.
112. Rossini P, Barker A, Berardelli A, Caramia M, Caruso G, Cracco R, et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report. Electroencephalogr Clin Neurophysiol (1994) 91:79-92. doi:10.1016/0013-4694(94)90029-9.
113. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W. Magnetic stimulation: motor evoked potentials. The international federation of clinical neurophysiology. Electroencephalogr Clin Neurophysiol Suppl (1999) 52:97-103.
114. Devanne H, Lavoie BA, Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res (1997) 114:329-38. doi:10.1007/PL00005641.
115. Ridding MC, Rothwell JC. Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol (1997) 105:340-4. doi:10.1016/S0924-980X(97)00041-6.
116. Singh AM, Neva JL, Staines WR. Acute exercise enhances the response to paired associative stimulation-induced plasticity in the primary motor cortex. Exp Brain Res (2014) 232(11):3675-85. doi:10.1007/s00221-014-4049-z.
117. Hess CW, Mills KR, Murray NM. Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol (1987) 388:397-419. doi:10.1113/jphysiol.1987.sp016621.
118. Penfield W, Rasmussen T. The Cerebral Cortex of Man. A Clinical Study of Localization of Function. New York, NY: The Macmillian Company (1950).
119. Levy WJ, Amassian VE, Schmid UD, Jungreis C. Mapping of motor cortex gyral sites non-invasively by transcranial magnetic stimulation in normal subjects and patients. Electroencephalogr Clin Neurophysiol (1991) 43:51-75.
120. Wassermann EM, McShane LM, Hallett M, Cohen LG. Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol (1992) 85:1-8. doi:10.1016/0168-5597(92)90094-R.
121. Wilson SA, Thickbroom GW, Mastaglia FL. Transcranial magnetic stimulation mapping of the motor cortex in normal subjects: the representation of two intrinsic hand muscles. J Neurol Sci (1993) 18:134-44. doi:10.1016/0022-510X(93)90102-5.
122. Mortifee P, Stewart H, Schulzer M, Eisen A. Reliability of transcranial magnetic stimulation for mapping the human motor cortex. Electroencephalogr Clin Neurophysiol (1994) 93:131-7. doi:10.1016/0168-5597(94)90076-0.
123. Thickbroom GW, Sammut R, Mastaglia FL. Magnetic stimulation mapping of motor cortex: factors contributing to map area. Electroencephalogr Clin Neurophysiol (1998) 109:79-84. doi:10.1016/S0924-980X(98)00006-X.
124. Thickbroom GW, Byrnes ML, Mastaglia FL. A model of the effect of MEP amplitude variation on the accuracy of TMS mapping. Clin Neurophysiol (1999) 110:941-3. doi:10.1016/S1388-2457(98)00080-7.
125. Thickbroom G, Byrnes M, Archer S, Kermode A, Mastaglia F. Corticomotor organisation and motor function in multiple sclerosis. J Neurol (2005) 252:765-71. doi:10.1007/s00415-005-0728-9.
126. Pearce AJ, Thickbroom GW, Byrnes ML, Mastaglia FL. Functional reorganisation of the corticomotor projection to the hand in skilled racquet players. Exp Brain Res (2000) 130:238-43. doi:10.1007/s002219900236.
127. Thielscher A, Kammer T. Linking physics with physiology in TMS: a sphere field model to determine the cortical stimulation site in TMS. Neuroimage (2002) 17:1117-30. doi:10.1006/nimg.2002.1282.
128. Uy J, Ridding MC, Miles TS. Stability of maps of human motor cortex made with transcranial magnetic stimulation. Brain Topogr (2002) 14:293-7. doi:10.1023/A:1015752711146.
129. Kleim JA, Kleim ED, Cramer SC. Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation. Nat Protoc (2007) 2:1675-84. doi:10.1038/nprot.2007.206.
130. Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res (1999) 128:539-42. doi:10.1007/s002210050878.
131. Fuhr P, Agostino R, Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol (1991) 81:257-62. doi:10.1016/0168-5597(91)90011-L.
132. Ingulleri M, Berardelli A, Cauccu G, Marfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol (1993) 466:521-34.
133. Werhahn K, Kunesch E, Noschtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol (1999) 517:591-7. doi:10.1111/j.1469-7793.1999.0591t.x.
134. Ferbert A, Priori A, Rothwell J, Day B, Colebatch JG, Marsden C. Interhemispheric inhibition of the human motor cortex. J Physiol (1992) 453:525-46. doi:10.1113/jphysiol.1992.sp019243.
135. Meyer B, Röricht S, Von Einsiedel H, Kruggel F, Weindl A. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain (1995) 118:429-40. doi:10.1093/brain/118.2.429.
136. Meyer BU, Röricht S, Woiciechowsky C. Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices. Ann Neurol (1998) 43:360-9. doi:10.1002/ana.410430314.
137. Kujirai T, Caramia MD, Rothwell JC, Day BJ, Thompson PD, Ferbert A, et al. Corticocortical inhibition in the human motor cortex. J Physiol (1993) 471:501-19. doi:10.1113/jphysiol.1993.sp019912.
138. Valls-Sole J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol (1992) 85:355-64. doi:10.1016/0168-5597(92)90048-G.
139. Wassermann EM, Samii A, Mercuri B, Ikoma K, Oddo D, Grill SE, et al. Responses to paired transcranial magnetic stimuli in resting, active, recently activated muscle. Exp Brain Res (1996) 109:158-63. doi:10.1007/BF00228638.
140. Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol (1996) 496:873-81. doi:10.1113/jphysiol.1996.sp021734.
141. Roick H, Von Giesen H, Benecke R, von Giesen HJ. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res (1993) 94:489-98. doi:10.1007/BF00230207.
142. Siebner HR, Willoch F, Peller M, Auer C, Boecker H, Conrad B, et al. Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport (1998) 9:943-8. doi:10.1097/00001756-199803300-00033.
143. McDonnell MN, Orekhov Y, Ziemann U. The role of GABA B receptors in intracortical inhibition in the human motor cortex. Exp Brain Res (2006) 173:86-93. doi:10.1007/s00221-006-0365-2.
144. Chen R, Tam A, Bütefisch C, Corwell B, Ziemann U, Rothwell JC, et al. Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol (1998) 80:2870-81.
145. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology (1998) 51:1320-4. doi:10.1212/WNL.51.5.1320.
146. Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res (2004) 154:1-10. doi:10.1007/s00221-003-1684-1.
147. Manganotti P, Zanette G, Bonato C, Tinazzi M, Polo A, Fiaschi A. Crossed and direct effects of digital nerves stimulation on motor evoked potential: a study with magnetic brain stimulation. Electroencephalogr Clin Neurophysiol (1997) 105:280-9. doi:10.1016/S0924-980X(97)00018-0.
148. Tokimura H, Ridding MC, Tokimura Y, Amassian VE, Rothwell JC. Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. Electroencephalogr Clin Neurophysiol (1996) 101:263-72. doi:10.1016/0924-980X(96)95664-7.
149. Sailer A, Molnar GF, Cunic DI, Chen R. Effects of peripheral sensory input on cortical inhibition in humans. J Physiol (2002) 544:617-29. doi:10.1113/jphysiol.2002.028670.
150. Sailer A, Molnar GF, Paradiso G, Gunraj CA, Lang AE, Chen R. Short and long latency afferent inhibition in Parkinson's disease. Brain (2003) 126:1883-94. doi:10.1093/brain/awg183.
151. Delvaux V, Alagona G, Gérard P, De Pasqua V, Pennisi G, de Noordhout AM. Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation. Clin Neurophysiol (2003) 114:1217-25. doi:10.1016/S1388-2457(03)00070-1.
152. Heald A, Bates D, Cartlidge N, French J, Miller S. Longitudinal study of central motor conduction time following stroke. 2. Central motor conduction measured within 72 h after stroke as a predictor of functional outcome at 12 months. Brain (1993) 116:1371-85. doi:10.1093/brain/116.6.1371.
153. Catano A, Houa M, Caroyer J, Ducarne H, Noel P. Magnetic transcranial stimulation in non-haemorrhagic sylvian strokes: interest of facilitation for early functional prognosis. Electroencephalogr Clin Neurophysiol (1995) 97:349-54. doi:10.1016/0924-980X(95)00127-7.
154. D'Olhaberriague L, Gamissans JME, Marrugat J, Valls A, Ley CO, Seoane JL. Transcranial magnetic stimulation as a prognostic tool in stroke. J Neurol Sci (1997) 147:73-80. doi:10.1016/S0022-510X(96)05312-9.
155. Escudero JV, Sancho J, Bautista D, Escudero M, López-Trigo J. Prognostic value of motor evoked potential obtained by transcranial magnetic brain stimulation in motor function recovery in patients with acute ischemic stroke. Stroke (1998) 29:1854-9. doi:10.1161/01.STR.29.9.1854.
156. Hendricks HT, Pasman JW, Merx JL, van Limbeek J, Zwarts MJ. Analysis of recovery processes after stroke by means of transcranial magnetic stimulation. J Clin Neurophysiol (2003) 20:188-95. doi:10.1097/00004691-200305000-00004.
157. Trompetto C, Assini A, Buccolieri A, Marchese R, Abbruzzese G. Motor recovery following stroke: a transcranial magnetic stimulation study. Clin Neurophysiol (2000) 111:1860-7. doi:10.1016/S1388-2457(00)00419-3.
158. Manganotti P, Patuzzo S, Cortese F, Palermo A, Smania N, Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol (2002) 113:936-43. doi:10.1016/S1388-2457(02)00062-7.
159. Pennisi G, Alagona G, Rapisarda G, Nicoletti F, Costanzo E, Ferri R, et al. Transcranial magnetic stimulation after pure motor stroke. Clin Neurophysiol (2002) 113:1536-43. doi:10.1016/S1388-2457(02)00255-9.
160. Traversa R, Cicinelli P, Bassi A, Rossini P, Bernardi G. Mapping of motor cortical reorganization after stroke a brain stimulation study with focal magnetic pulses. Stroke (1997) 28(1):110-7. doi:10.1161/01.STR.28.1.110.
161. Traversa R, Cicinelli P, Oliveri M, Giuseppina Palmieri M, Maddalena Filippi M, Pasqualetti P, et al. Neurophysiological follow-up of motor cortical output in stroke patients. Clin Neurophysiol (2000) 111:1695-703. doi:10.1016/S1388-2457(00)00373-4.
162. 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. doi:10.1016/S0006-8993(98)00505-8.
163. 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) 105:438-50. doi:10.1016/S0924-980X(97)00052-0.
164. Liepert J, Miltner WH, Bauder H, Sommer M, Dettmers C, Taub E, et al. Motor cortex plasticity during constraint-induced movement therapy in stroke patients. Neurosci Lett (1998) 250:5-8. doi:10.1016/S0304-3940(98)00386-3.
165. Liepert J, Bauder H, Miltner WHR, Taub E, Weiller C. Treatment-induced cortical reorganization after stroke in humans. Stroke (2000) 31(6):1210-6. doi:10.1161/01.STR.31.6.1210.
166. Sawaki L, Butler AJ, Leng X, Wassenaar PA, Mohammad YM, Blanton S, et al. Constraint-induced movement therapy results in increased motor map area in subjects 3 to 9 months after stroke. Neurorehabil Neural Repair (2008) 22:505-13. doi:10.1177/1545968308317531.
167. Ro T, Noser E, Boake C, Johnson R, Gaber M, Speroni A, et al. Functional reorganization and recovery after constraint-induced movement therapy in subacute stroke: case reports. Neurocase (2006) 12:50-60. doi:10.1080/13554790500493415.
168. Traversa R, Cicinelli P, Filippi M, Oliveri M, Palmieri MG, Pasqualetti P, et al. A method to monitor motor cortical excitability in human stroke through motor evoked potentials. Brain Res Brain Res Protoc (1999) 4:44-8. doi:10.1016/S1385-299X(98)00063-4.
169. Ahonen J, Jehkonen M, Dastidar P, Molnar G, Hakkinen V. Cortical silent period evoked by transcranial magnetic stimulation in ischemic stroke. Electroencephalogr Clin Neurophysiol (1998) 109:224-9. doi:10.1016/S0924-980X(98)00014-9.
170. Liepert J, Storch P, Fritsch A, Weiller C. Motor cortex disinhibition in acute stroke. Clin Neurophysiol (2000) 111:671-6. doi:10.1016/S1388-2457(99)00312-0.
171. Liepert J, Restemeyer C, Kucinski T, Zittel S, Weiller C. Motor strokes: the lesion location determines motor excitability changes. Stroke (2005) 36:2648-53. doi:10.1161/01.STR.0000189629.10603.02.
172. Liepert J, Hamzei F, Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve (2000) 23:1761-3. doi:10.1002/1097-4598(200011)23:11<1761::AID-MUS14>3.0.CO;2-M.
173. Bütefisch CM, Netz J, Weßling M, Seitz RJ, Hömberg V. Remote changes in cortical excitability after stroke. Brain (2003) 126:470-81. doi:10.1093/brain/awg044.
174. Swayne OB, Rothwell JC, Ward NS, Greenwood RJ. Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex (2008) 18:1909-22. doi:10.1093/cercor/bhm218.
175. Di Lazzaro V, Profice P, Pilato F, Capone F, Ranieri F, Florio L, et al. The level of cortical afferent inhibition in acute stroke correlates with long-term functional recovery in humans. Stroke (2012) 43:250-2. doi:10.1161/STROKEAHA.111.631085.
176. Pennisi G, Rapisarda G, Bella R, Calabrese V, Maertens De Noordhout A, Delwaide PJ. Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. Stroke (1999) 30:2666-70. doi:10.1161/01.STR.30.12.2666.
177. Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain (2002) 125:1896-907. doi:10.1093/brain/awf183.
178. Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG. Reorganization of the human ipsilesional premotor cortex after stroke. Brain (2004) 127:747-58. doi:10.1093/brain/awh082.
179. Catano A, Houa M, Caroyer JM, Ducarne H, Noël P. Magnetic transcranial stimulation in acute stroke: early excitation threshold and functional prognosis. Electroencephalogr Clin Neurophysiol (1996) 101:233-9. doi:10.1016/0924-980X(96)95656-8.
180. Byrnes ML, Thickbroom GW, Phillips BA, Mastaglia FL. Long-term changes in motor cortical organisation after recovery from subcortical stroke. Brain Res (2001) 889:278-87. doi:10.1016/S0006-8993(00)03089-4.
181. Foltys H, Krings T, Meister IG, Sparing R, Boroojerdi B, Thron A, et al. Motor representation in patients rapidly recovering after stroke: a functional magnetic resonance imaging and transcranial magnetic stimulation study. Clin Neurophysiol (2003) 114:2404-15. doi:10.1016/S1388-2457(03)00263-3.
182. Boroojerdi B, Diefenbach K, Ferbert A. Transcallosal inhibition in cortical and subcortical cerebral vascular lesions. J Neurol Sci (1996) 144:160-70. doi:10.1016/S0022-510X(96)00222-5.
183. Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol (2004) 55:400-9. doi:10.1002/ana.10848.
184. Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. Transcallosal inhibition in chronic subcortical stroke. Neuroimage (2005) 28:940-6. doi:10.1016/j.neuroimage.2005.06.033.
185. Taub E, Uswatte G, King DK, Morris D, Crago JE, Chatterjee A. A placebo-controlled trial of constraint-induced movement therapy for upper extremity after stroke. Stroke (2006) 37:1045-9. doi:10.1161/01.STR.0000206463.66461.97.
186. Carey JR, Fregni F, Pascual-Leone A. rTMS combined with motor learning training in healthy subjects. Restor Neurol Neurosci (2006) 24(3):191-9.
187. 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) 22:4-21. doi:10.1177/1545968307301769.
188. Borich M, Neva J, Boyd L. Evaluation of differences in brain neurophysiology and morphometry associated with hand function in individuals with chronic stroke. Restor Neurol Neurosci (2015) 33:31-42. doi:10.3233/RNN-140425.
189. Mang CS, Borich MR, Brodie SM, Boyd LA. Diffusion imaging and transcranial magnetic stimulation assessment of transcallosal pathways in chronic stroke. Clin Neurophysiol (2015) 126(10):1959-71. doi:10.1016/j.clinph.2014.12.018.
190. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron (2005) 45:201-6. doi:10.1016/j.neuron.2004.12.033.
191. Huang YZ, Rothwell JC, Lu CS, Wang J, Weng YH, Lai SC, et al. The effect of continuous theta burst stimulation over premotor cortex on circuits in primary motor cortex and spinal cord. Clin Neurophysiol (2009) 120:796-801. doi:10.1016/j.clinph.2009.01.003.
192. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M, Valls-Solé J. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain (1994) 117:847-58. doi:10.1093/brain/117.4.847.
193. Brodie SM, Meehan SK, Borich MR, Boyd LA. 5 Hz repetitive transcranial magnetic stimulation over the ipsilesional sensory cortex enhances motor learning after stroke. Front Hum Neurosci (2014) 8:143. doi:10.3389/fnhum.2014.00143.
194. Meehan SK, Dao E, Linsdell MA, Boyd LA. Continuous theta burst stimulation over the contralesional sensory and motor cortex enhances motor learning post-stroke. Neurosci Lett (2011) 500:26-30. doi:10.1016/j.neulet.2011.05.237.
195. Pascual-Leone A, Tommas JM, Keenan J, Canete C, Catala MD. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol (1998) 15:333-43. doi:10.1097/00004691-199807000-00005.
196. Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC. The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex (2013) 23:1593-605. doi:10.1093/cercor/bhs147.
197. Suppa A, Ortu E, Zafar N, Deriu F, Paulus W, Berardelli A, et al. Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. J Physiol (2008) 18:4489-500. doi:10.1113/jphysiol.2008.156596.
198. Neva JL, Vesia M, Singh AM, Staines WR. Modulation of left primary motor cortex excitability after bimanual training and intermittent theta burst stimulation to left dorsal premotor cortex. Behav Brain Res (2014) 261:289-96. doi:10.1016/j.bbr.2013.12.029.
199. Legon W, Dionne JK, Staines WR. Continuous theta burst stimulation of the supplementary motor area: effect upon perception and somatosensory and motor evoked potentials. Brain Stimul (2013) 6:877-83. doi:10.1016/j.brs.2013.04.007.
200. Stinear CM, Barber PA, Coxon JP, Verryt TS, Acharya PP, Byblow WD. Repetitive stimulation of premotor cortex affects primary motor cortex excitability and movement preparation. Brain Stimul (2009) 2:152-62. doi:10.1016/j.brs.2009.01.001.
201. Premji A, Rai N, Nelson A. Area 5 influences excitability within the primary motor cortex in humans. PLoS One (2011) 6:e20023. doi:10.1371/journal.pone.0020023.
202. Arasanz CP, Staines WR, Roy EA, Schweizer TA. The cerebellum and its role in word generation: a cTBS study. Cortex (2012) 48:718-24. doi:10.1016/j.cortex.2011.02.021.
203. Bolton DA, Staines WR. Transient inhibition of the dorsolateral prefrontal cortex disrupts attention-based modulation of tactile stimuli at early stages of somatosensory processing. Neuropsychologia (2011) 49:1928-37. doi:10.1016/j.neuropsychologia.2011.03.020.
204. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci (2004) 19:1950-62. doi:10.1111/j.1460-9568.2004.03277.x.
205. Huang YZ, Rothwell JC, Edwards MJ, Chen RS. Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex (2008) 18:563-70. doi:10.1093/cercor/bhm087.
206. Chen R, Yung D, Li J. Organization of ipsilateral excitatory and inhibitory pathways in the human motor cortex. J Neurophysiol (2003) 89:1256-64. doi:10.1152/jn.00950.2002.
207. Corti M, Patten C, Triggs W. Repetitive transcranial magnetic stimulation of motor cortex after stroke. Am J Phys Med Rehabil (2012) 91:254-70. doi:10.1097/PHM.0b013e318228bf0c.
208. Carey JR, Anderson DC, Gillick BT, Whitford M, Pascual-Leone A. 6-Hz primed low-frequency rTMS to contralesional M1 in two cases with middle cerebral artery stroke. Neurosci Lett (2010) 469:338-42. doi:10.1016/j.neulet.2009.12.023.
209. Boggio PS, Alonso-Alonso M, Mansur CG, Rigonatti SP, Schlaug G, Pascual-Leone A, 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) 85:927-30. doi:10.1097/01.phm.0000242635.88129.38.
210. Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira MJL, 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) 37:2115-22. doi:10.1161/01.STR.0000231390.58967.6b.
211. Seniow J, Bilik M, Lesniak M, Waldowski K, Iwanski S, Czlonkowska A. Transcranial magnetic stimulation combined with physiotherapy in rehabilitation of poststroke hemiparesis: a randomized, double-blind, placebo-controlled study. Neurorehabil Neural Repair (2012) 26:1072-9. doi:10.1177/1545968312445635.
212. Talelli P, Wallace A, Dileone M, Hoad D, Cheeran B, Oliver R, et al. Theta burst stimulation in the rehabilitation of the upper limb: a semirandomized, placebo-controlled trial in chronic stroke patients. Neurorehabil Neural Repair (2012) 26:976-87. doi:10.1177/1545968312437940.
213. Cohen L, Ziemann U, Chen R, Classen J, Hallett M, GerloffC, et al. Studies of neuroplasticity with transcranial magnetic stimulation. J Clin Neurophysiol (1998) 15:305-24. doi:10.1097/00004691-199807000-00003.
214. Grefkes C, Fink GR. Connectivity-based approaches in stroke and recovery of function. Lancet Neurol (2014) 13:206-16. doi:10.1016/S1474-4422(13)70264-3.
215. Khedr EM. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology (2005) 65(3):466-8. doi:10.1212/01.wnl.0000173067.84247.36.
216. Kim Y-H, You SH, Ko M-H, Park J-W, Lee KH, Jang SH, et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke (2006) 37:1471-6. doi:10.1161/01.STR.0000221233.55497.51.
217. 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) 66:298-309. doi:10.1002/ana.21725.
218. Malcolm MP, Triggs WJ, Light KE, Gonzalez LJ, Wu S, Reid K, et al. Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial. Am J Phys Med Rehabil (2007) 86:707-15. doi:10.1097/PHM.0b013e31813e0de0.Repetitive.
219. Lee JH, Kim SB, Lee KW, Kim MA, Lee SJ, Choi SJ. Factors associated with upper extremity motor recovery after repetitive transcranial magnetic stimulation in stroke patients. Ann Rehabil Med (2015) 39:268-76. doi:10.5535/arm.2015.39.2.268.
220. Tretriluxana J, Kantak S, Tretriluxana S, Wu AD, Fisher BE. Low frequency repetitive transcranial magnetic stimulation to the non-lesioned hemisphere improves paretic arm reach-to-grasp performance after chronic stroke. Disabil Rehabil Assist Technol (2013) 8:121-4. doi:10.3109/17483107.2012.737136.
221. Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke (2005) 36:2681-6. doi:10.1161/01.STR.0000189658.51972.34.
222. Grefkes C, Nowak DA, Wang LE, Dafotakis M, EickhoffSB, Fink GR. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage (2010) 50:233-42. doi:10.1016/j.neuroimage.2009.12.029.
223. Hsu WY, Cheng CH, Liao KK, Lee IH, Lin YY. Effects of repetitive transcranial magnetic stimulation on motor functions in patients with stroke: a meta-analysis. Stroke (2012) 43:1849-57. doi:10.1161/STROKEAHA.111.649756.
224. Bolognini N, Pascual-Leone A, Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. J Neuroeng Rehabil (2009) 6:8. doi:10.1186/1743-0003-6-8.
225. 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) 2014:1-10. doi:10.1155/2014/305236.
226. Emara T, El Nahas N, Elkader HA, Ashour S, El Etrebi A. MRI can predict the response to therapeutic repetitive transcranial magnetic stimulation (rTMS) in stroke patients. J Vasc Interv Neurol (2009) 2(2):163-8.
227. Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD. The {PREP} algorithm predicts potential for upper limb recovery after stroke. Brain (2012) 135:2527-35. doi:10.1093/brain/aws146.
228. Lüdemann-Podubecká J, Bösl K, Theilig S, Wiederer R, Nowak DA. The effectiveness of 1Hz rTMS over the primary motor area of the unaffected hemisphere to improve hand function after stroke depends on hemispheric dominance. Brain Stimul (2015) 8(4):823-30. doi:10.1016/j.brs.2015.02.004.
229. Cunningham DA, Machado A, Janini D, Varnerin N, Bonnett C, Yue G, et al. The assessment of inter-hemispheric imbalance using imaging and non-invasive brain stimulation in patients with chronic stroke. Arch Phys Med Rehabil (2014) 96(4 Suppl):S94-103. doi:10.1016/j.apmr.2014.07.419.
230. Uhm KE, Kim Y-H, Yoon KJ, Hwang JM, Chang WH. BDNF genotype influence the efficacy of rTMS in stroke patients. Neurosci Lett (2015) 594:117-21. doi:10.1016/j.neulet.2015.03.053.
231. Plow EB, Cunningham DA, Varnerin N, Machado A. Rethinking stimulation of the brain in stroke rehabilitation: why higher motor areas might be better alternatives for patients with greater impairments. Neuroscientist (2014) 21(3):225-40. doi:10.1177/1073858414537381.
232. 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) 25:1865-73. doi:10.1111/j.1460-9568.2007.05434.x.
233. Bestmann S, Swayne O, Blankenburg F, RuffCC, Teo J, Weiskopf N, et al. The role of contralesional dorsal premotor cortex after stroke as studied with concurrent TMS-fMRI. J Neurosci (2010) 30:11926-37. doi:10.1523/JNEUROSCI.5642-09.2010.
234. Lotze M, Beutling W, Loibl M, Domin M, Platz T, Schminke U, et al. Contralesional motor cortex activation depends on ipsilesional corticospinal tract integrity in well-recovered subcortical stroke patients. Neurorehabil Neural Repair (2012) 26:594-603. doi:10.1177/1545968311427706.
235. Borich MR, Brown KE, Lakhani B, Boyd LA. Applications of electroencephalography to characterize brain activity. J Neurol Phys Ther (2015) 39:43-51. doi:10.1097/NPT.0000000000000072.
236. Ilmoniemi RJ, Kicic D. Methodology for combined TMS and EEG. Brain Topogr (2010) 22:233-48. doi:10.1007/s10548-009-0123-4.
237. Komssi S, Kahkonen S, Ilmoniemi RJ, Kähkönen S. The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp (2004) 21:154-64. doi:10.1002/hbm.10159.
238. Kicic D, Lioumis P, Ilmoniemi RJ, Nikulin VV. Bilateral changes in excitability of sensorimotor cortices during unilateral movement: combined electroencephalographic and transcranial magnetic stimulation study. Neuroscience (2008) 152:1119-29. doi:10.1016/j.neuroscience.2008.01.043.
239. Di Pino G, Pellegrino G, Assenza G, Capone F, Ferreri F, Formica D, et al. Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nat Rev Neurol (2014) 10:597-608. doi:10.1038/nrneurol.2014.162.