Imaging the effects of rTMS-induced cortical plasticity

Restorative Neurology and Neuroscience

Volumn 28, Issue 4, 2010, Pages 425-436

  Stagg, Charlotte J ^a   O'Shea, Jacinta ^a   Johansen Berg, Heidi ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

functional magnetic resonance imaging; magnetic resonance spectroscopy; motor cortex; Repetitive transcranial magnetic stimulation; stroke

Indexed keywords

BRAIN REGION; CLINICAL PROTOCOL; CLINICAL TRIAL; EVOKED MUSCLE RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL STATUS; GABAERGIC TRANSMISSION; HUMAN; IMAGE ANALYSIS; IMAGE QUALITY; MOTONEURON; MOTOR CORTEX; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NEUROCHEMISTRY; NEUROIMAGING; NEUROMODULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; STROKE PATIENT; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; BRAIN; BRAIN CHEMISTRY; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MENTAL DISORDERS; MOTOR CORTEX; NERVOUS SYSTEM DISEASES; NEURONAL PLASTICITY; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 77956238063     PISSN: 09226028     EISSN: None     Source Type: Journal    
DOI: 10.3233/RNN-2010-0553     Document Type: Review

References (63)

1. Allen, E.A., Pasley, B.N., Duong, T. & Freeman, R.D. (2007). Transcranial magnetic stimulation elicits coupled neural and hemo-dynamic consequences. Science, 317, 1918-1921.
2. Amassian, V.E., Stewart, M., Quirk, G. & Rosenthal, J. (1987). Physiological nasis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery, 20, 74-93.
3. Ameli, M., Grefkes, C., Kemper, F., Riegg, F., Rehme, A., Karbe, H., Fink, G.R. & Nowak, D. (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.
4. Baudewig, J., Siebner, H.R., Bestmann, S., Tergau, F., Tings, T., Paulus, W. & Frahm, J. (2001). Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport, 12, 3543-3548.
5. Bestmann, S., Baudewig, J., Siebner, H.R., Rothwell, J. & Frahm, J. (2003). Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage, 20, 1685-1696.
6. Bestmann, S., Baudewig, J., Siebner, H.R., Rothwell, J.C. & Frahm, J. (2005). BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage, 28, 22-29.
7. Bestmann, S., Swayne, O., Blankenburg, F., Ruff, C.C., Haggard, P., Weiskopf, N., Josephs, O., Driver, J., Rothwell, J.C. & Ward, N.S. (2008). Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex, 18, 1281-1291.
8. Bohning, D., Shastri, A., McConnell, K., Nahas, Z., Lorberbaum, J., Roberts, D., Teneback, C., Vincent, D. & George, M. (1999). A Combined TMS/fMRI Study of Intensity Dependent TMS Over Motor Cortex. Biol Psych, 45, 385-394.
9. Butefisch, C., Davis, B.C., Wise, S.P., Sawaki, L., Kopylev, L., Classen, J. & Cohen, L.G. (2000). Mechanisms of use-dependent plasticty in the human motor cortex. Proc Natl Acad Sci, 97, 3661-3665.
10. Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E.M., Hallett, M. & Cohen, L.G. (1997). Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48, 1398-1403.
11. Chouinard, P.A., Van Der Werf, Y.D., Leonard, G. & Paus, T. (2003). Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J Neurophysiol, 90, 1071-1083.
12. Conchou, F., Loubinoux, I., Castel-Lacanal, E., Le Tinnier, A., Gerdelat-Mas, A., Faure-Marie, N., Gros, H., Thalamas, C., Calvas, F., Berry, I., Chollet, F. and Moreau, M.S. (2009). Neural substrates of low-frequency repetitive transcranial magnetic stimulation during movement in healthy subjects and acute stroke patients. A PET study. Hum Brain Mapp, 30, 25422557.
13. Damoiseaux, J.S., Rombouts, S.A., Barkhof, F., Scheltens, P., Stam, C.J., Smith, S.M. & Beckmann, C.F. (2006). Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci, 103, 13848-13853.
14. Di Filippo, M., Tozzi, A., Costa, C., Belcastro, V., Tantucci, M., Picconi, B. & Calabresi, P. (2008). Plasticity and repair in the post-ischemic brain. Neuropharmacol, 55, 353-362.
15. Edwards, M.J., Talelli, P. & Rothwell, J.C. (2008). Clinical applications of transcranial magnetic stimulation in patients with movement disorders. Lancet Neurol, 7, 827-840.
16. Engel, D., Pahner, I., Schulze, K., Frahm, C., Jarry, H., Ahnert-Hilger, G. & Draguhn, A. (2001). Plasticity of rat central inhibitory synapses through GABA metabolism. J Physiol, 535, 473-482.
17. Floyer-Lea, A., Wylezinska, M., Kincses, T. & Matthews, P. (2006). Rapid Modulation of GABA Concentration in Human Sensorimotor Cortex During Motor Learning. J Neurophysiol, 95, 1639-1644.
18. Fregni, F., Boggio, P.S., Valle, A.C., Rocha, R.R., Duarte, J., Ferreira, M.J., Wagner, T., Fecteau, S., Rigonatti, S.P., Riberto, M., Freedman, S.D. & Pascual-Leone, A. (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.
19. Fregni, F. & Pascual-Leone, A. (2007). Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol, 3, 383-393.
20. Gerschlager, W., Siebner, H.R. & Rothwell, J. (2001). Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology, 57, 449-455.
21. Goense, J. & Logothetis, N.K. (2008). Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr Biol, 18, 631-640.
22. Golan, H., Talpalar, A.E., Schleifstein-Attias, D. & Grossman, Y. (1996). GABA metabolism controls inhibition efficacy in the mammalian CNS. Neurosci Lett, 217, 25-28.
23. Grefkes, C., Nowak, D., Wang, L.E., Dafotakis, M., Eickhoff, S.B. & Fink, G.R. (2010). Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage, 1-10.
24. Hess, G., Aizenman, C.D. & Donoghue, J.P. (1996). Conditions for the induction oflong-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol, 75, 17651778.
25. Huang, Y.Z., Chen, R., Rothwell, J. & Wen, H.Y. (2007). The aftereffect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 118, 1028-1032.
26. Huang, Y.Z., Edwards, M.J., Rounis, E., Bhatia, K.P. & Rothwell, J. (2005). Theta burst stimulation of the human motor cortex.[see comment]. Neuron, 45, 201-206.
27. Hummel, F. & Cohen, L. (2006). Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol, 5, 708-712.
28. Jezzard, P., Matthews, P. & Smith, S. (2001). Functional Magnetic Resonance Imaging: An Introduction to Methods. Oxford University Press, Oxford.
29. Kim, Y., You, S.H., Ko, M., Park, J., Lee, K.H., Jang, S.H., Yoo, W. & Hallett, M. (2006). Repetitive Transcranial Magnetic Stimulation-Induced Corticomotor Excitability and Associated Motor Skill Acquisition in Chronic Stroke. Stroke 37, 1471-1476.
30. Lam, R., Chan, P., Wilkins-Ho, M. & Yatham, L. (2008). Repetitive transcranial magnetic stimulation for treatment-resistant depression: a systematic review and metaanalysis. Can J Psychiatry, 53, 621-631.
31. Lee, L., Siebner, H.R., Rowe, J.B., Rizzo, V., Rothwell, J., Frackowiak, R.S. & Friston, K.J. (2003). Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci, 23, 5308-5318.
32. Levy, L.M., Ziemann, U., Chen, R. & Cohen, L.G. (2002). Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation. Ann Neurol, 52, 755-761.
33. Liebetanz, D., Fauser, S., Michaelis, T., Cz Czh, B., Watanabe, T., Paulus, W., Frahm, J. & Fuchs, E. (2003). Safety aspects of chronic low-frequency transcranial magnetic stimulation based on localized proton magnetic resonance spectroscopy and histology of the rat brain. J Psychiat Res, 37, 277-286.
34. Logothetis, N.K. & al e. (2001). Neurophysiological investigation o the basis of the fMRI signal. Nature, 412, 150-157.
35. Maeda, F., Keenan, J., Tormos, J., Topka, H. & Pascual-Leone, A. (2000). Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitabiliy. Exp Brain Res, 133,425-430.
36. Mansur, C., Fregni, F., Boggio, P.S., Riberto, M., Gallucci-Neto, J., Santos, C., Wagner, T., Rigonatti, S., Marcolin, M. & Pascual-Leone, A. (2005). Ashamstimulation-controlledtrialofrTMS of the unaffected hemisphere in stroke patients. Neurology, 64, 1802-1804.
37. Michael, N., Gosling, M., Reutemann, M., Kersting, A., Heindel, W., Arolt, V. & Pfleiderer, B. (2003). Metabolic changes after repetitive transcranial magnetic stimulation (rTMS) of the left prefrontal cortex: a sham-controlled proton magnetic resonance spectroscopy (1H MRS) study of healthy brain. Eur J Neurosci, 17, 2462-2468.
38. Moisa, M., Pohmann, R., Uludafü, K. & Thielscher, A. (2010). Interleaved TMS/CASL: Comparison of different rTMS protocols. Neuroimage, 49, 612-620.
39. Murase, N., Duque, J., Mazzocchio, R. & Cohen, L. (2004). Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol, 55, 400-409.
40. Nitsche, M., Liebetanz, D., Antal, A., Lang, N., Tergau, F. & Paulus, W. (2003). Modulation of cortical excitability by weak direct current stimulation - technical, safety and functional aspects. Suppl Clin Neurophysiol, 56, 255-276.
41. Nowak, D., Grefkes, C., Dafotakis, M., Eickhoff, S., Kt, J., Karbe, H. & Fink, G.R. (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.
42. OShea, J., Johansen-Berg, H., Trief, D., Gobel, S. & Rushworth, M.F. (2007). Functionally-Specific Reorganisation in Human Premotor Cortex. Neuron, 54, 479-490.
43. OShea, J. & Walsh, V. (2007). TMS: aprimer. CurrBiol, 17, R196.
44. Paus, T., Jech, R., Thompson, C.J., Comeau, R., Peters, T. & Evans, A.C. (1997). Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci, 17, 3178-3184.
45. Paus, T., Jech, R., Thompson, C.J., Comeau, R., Peters, T. & Evans, A.C. (1998). Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. J Neurophysiol, 79, 1102-1107.
46. Peinemann, A., Reimer, B., Loer, C., Quartarone, A., Munchau, A., Conrad, B. & Siebner, H.R. (2004). Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex. Clin Neurophysiol, 115, 1519-1526.
47. Pleger, B., Blankenburg, F., Bestmann, S., Ruff, C.C., Wiech, K., Stephan, K.E., Friston, K.J. & Dolan, R.J. (2006). Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J Neurosci, 26, 1945-1952.
48. Rogers, B.P., Morgan, V.L., Newton, A.T. & Gore, J.C. (2007). Assessing functional connectivity in the human brain by fMRI. MagnResIm, 25, 1347-1357.
49. Rounis, E., Lee, L., Siebner, H.R., Rowe, J.B., Friston, K.J., Rothwell, J. & Frackowiak, R.S. (2005). Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage, 26, 164-176.
50. Sack, A.T., Kohler, A., Bestmann. S., Linden, D.E., Dechent, P., Goebel, R. & Baudewig, J. (2007). Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex, 17, 2841-2852.
51. Shulman, R. & Rothman, D.L. (1998). Interpreting functional imaging studies in terms of neurotransmitter cycling. Proc Natl Acad Sci, 95, 11993-11998.
52. Siebner, H.R. & Rothwell, J. (2003). Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp BrainRes, 148, 1-16.
53. Stagg, C., Best, J., Stephenson, M., OShea, J., Wylezinska, M., Kincses, Z., Morris, P., Matthews, P. & Johansen-Berg, H. (2009a). Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. JNeurosci, 29, 5202-5206.
54. Stagg, C., Wylezinska, M., Matthews, P., Johansen-Berg, H., Jezzard, P., Rothwell, J. & Bestmann, S. (2009b). Neurochemical Effects of Theta Burst Stimulation as Assessed by Magnetic Resonance Spectroscopy. J Neurophysiol, 101, 2872-2877.
55. Takeuchi, N., Chuma, T., Matsuo, Y., Watanabe, T. & Ikoma, K. (2005). Repetitive Transcranial Magnetic Stimulation of Contralesional Primary Motor Cortex Improves Hand Function after Stroke. Stroke, 36, 2681-2686.
56. Talelli, P., Greenwood, R.J. & Rothwell, J. (2007). Exploring Theta Burst Stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol, 118, 333-342.
57. Tegenthoff, M., Witscher, K., Schwenkreis, P. & Liepert, J. (1999). Pharmacological modulation of training-induced plastic changes in human motor cortex. Electroencephalogr Clin Neurophysiol Suppl, 51, 188-191.
58. Trepel, C. & Racine, R.J. (2000). GABAergic Modulation of Neocortical Long-Term Potentiation in the Freely Moving Rat. Synapse, 35, 120-128.
59. Ward, N.S., Brown, M.M., Thompson, A.J. & Frackowiak, R.S. (2003). Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain, 126, 1430-1448.
60. Ward, N.S. & Cohen, L.G. (2004). Mechanisms underlying recovery of motor function after stroke. Arch Neurol, 61, 1844-1848.
61. Yousry, T., Schmid, U., Alkadhi, H., Schmidt, D., Peraud, A., Buettner, P. & Winkler, P. (1997). Localization of the motor hand areato aknob on the precentral gyrus. Brain, 120, 141-157.
62. Ziemann, U., Muellbacher, W., Hallett, M. & Cohen, L.G. (2001). Modulation of practice-dependent plasticity in human motor cortex. Brain, 124, 1171-1181.
63. Ziemann, U. & Rothwell, J.C. (2000). I-waves in motor cortex. J Clin Neurophysiol, 17,397-405.