Theta burst TMS increases cerebral blood flow in the primary motor cortex during motor performance as assessed by arterial spin labeling (ASL)

NeuroImage

Volumn 61, Issue 3, 2012, Pages 599-605

  Orosz, Ariane ^a   Jann, Kay ^a   Wirth, Miranka ^a,c   Wiest, Roland ^b   Dierks, Thomas ^a   Federspiel, Andrea ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arterial spin labeling fMRI; Cerebral blood flow; Fingertapping; Primary motor cortex; Thetaburst transcranial magnetic stimulation; Virtual lesion

Indexed keywords

ADULT; ARTERIAL SPIN LABELING; ARTICLE; BEHAVIOR MODIFICATION; BRAIN BLOOD FLOW; CONTROLLED STUDY; FEMALE; HAND FUNCTION; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; LOCOMOTION; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NEUROLOGIC EXAMINATION; NORMAL HUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RIGHT HANDEDNESS; SINGLE BLIND PROCEDURE; SPIN LABELING; STIMULUS RESPONSE; TASK PERFORMANCE; THETA BURST STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION; VELOCITY;

ADULT; ALGORITHMS; BEHAVIOR; CEREBROVASCULAR CIRCULATION; CROSS-OVER STUDIES; FEMALE; FINGERS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MOTOR CORTEX; MOVEMENT; PSYCHOMOTOR PERFORMANCE; SPIN LABELS; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84861194573     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.03.084     Document Type: Article

References (66)

1. Abbruzzese G., Trompetto C. Clinical and research methods for evaluating cortical excitability. J. Clin. Neurophysiol. 2002, 19:307-321.
2. Agostino R., Iezzi E., Dinapoli L., Gilio F., Conte A., Mari F., Berardelli A. Effects of 5Hz subthreshold magnetic stimulation of primary motor cortex on fast finger movements in normal subjects. Exp. Brain Res. 2007, 180:105-111.
3. Agostino R., Iezzi E., Dinapoli L., Suppa A., Conte A., Berardelli A. Effects of intermittent theta-burst stimulation on practice-related changes in fast finger movements in healthy subjects. Eur. J. Neurosci. 2008, 28:822-828.
4. Bestmann S., Baudewig J., Siebner H.R., Rothwell J.C., Frahm J. Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage 2003, 20:1685-1696.
5. Boynton G.M., Engel S.A., Glover G.H., Heeger D.J. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 1996, 16:4207-4221.
6. Bradnam L.V., Stinear C.M., Byblow W.D. Theta burst stimulation of human primary motor cortex degrades selective muscle activation in the ipsilateral arm. J. Neurophysiol. 2010, 104:2594-2602.
7. Cardenas-Morales L., Gron G., Kammer T. Exploring the after-effects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study. Hum. Brain Mapp. 2011, 32(11):1948-1960. (Nov).
8. Cardenas-Morales L., Nowak D.A., Kammer T., Wolf R.C., Schonfeldt-Lecuona C. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr. 2010, 22:294-306.
9. Chen R., Gerloff C., Hallett M., Cohen L.G. Involvement of the ipsilateral motor cortex in finger movements of different complexities. Ann. Neurol. 1997, 41:247-254.
10. Chouinard P.A., Van Der Werf Y.D., Leonard G., Paus T. Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J. Neurophysiol. 2003, 90:1071-1083.
11. Claus D., Spitzer A. Magnetic stimulation using double coils-methodology and normal findings. EEG EMG Z. Elektroenzephalogr. Elektromyogr. Verwandte Geb. 1991, 22:21-27.
12. Cramer S.C., Finklestein S.P., Schaechter J.D., Bush G., Rosen B.R. Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. J. Neurophysiol. 1999, 81:383-387.
13. Dai W., Garcia D., de Bazelaire C., Alsop D.C. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn. Reson. Med. 2008, 60:1488-1497.
14. Detre J.A., Alsop D.C. Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. Eur. J. Radiol. 1999, 30:115-124.
15. Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004, 427:311-312.
16. Federspiel A., Muller T.J., Horn H., Kiefer C., Strik W.K. Comparison of spatial and temporal pattern for fMRI obtained with BOLD and arterial spin labeling. J. Neural Transm. 2006, 113:1403-1415.
17. Fox P., Ingham R., George M.S., Mayberg H., Ingham J., Roby J., Martin C., Jerabek P. Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 1997, 8:2787-2791.
18. Friston K.J., Holmes A.P., Poline J.B., Grasby P.J., Williams S.C., Frackowiak R.S., Turner R. Analysis of fMRI time-series revisited. Neuroimage 1995, 2:45-53.
19. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
20. Gentner R., Wankerl K., Reinsberger C., Zeller D., Classen J. Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb. Cortex 2008, 18:2046-2053.
21. Gunther M. Efficient visualization of vascular territories in the human brain by cycled arterial spin labeling MRI. Magn. Reson. Med. 2006, 56:671-675.
22. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000, 406:147-150.
23. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 2005, 45:201-206.
24. Huang Y.Z., Rothwell J.C., Edwards M.J., Chen R.S. Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb. Cortex 2008, 18:563-570.
25. Iezzi E., Conte A., Suppa A., Agostino R., Dinapoli L., Scontrini A., Berardelli A. Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. J. Neurophysiol. 2008, 100:2070-2076.
26. Jancke L., Steinmetz H., Benilow S., Ziemann U. Slowing fastest finger movements of the dominant hand with low-frequency rTMS of the hand area of the primary motor cortex. Exp. Brain Res. 2004, 155:196-203.
27. Jann K., Koenig T., Dierks T., Boesch C., Federspiel A. Association of individual resting state EEG alpha frequency and cerebral blood flow. Neuroimage 2010, 51:365-372.
28. Kobayashi M., Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003, 2:145-156.
29. Lancaster J.L., Rainey L.H., Summerlin J.L., Freitas C.S., Fox P.T., Evans A.C., Toga A.W., Mazziotta J.C. Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum. Brain Mapp. 1997, 5:238-242.
30. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Kochunov P.V., Nickerson D., Mikiten S.A., Fox P.T. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 2000, 10:120-131.
31. Lee L., Siebner H.R., Rowe J.B., Rizzo V., Rothwell J.C., Frackowiak R.S., Friston K.J. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J. Neurosci. 2003, 23:5308-5318.
32. Lisanby S.H., Gutman D., Luber B., Schroeder C., Sackeim H.A. Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biol. Psychiatry 2001, 49:460-463.
33. Lisanby S.H., Kinnunen L.H., Crupain M.J. Applications of TMS to therapy in psychiatry. J. Clin. Neurophysiol. 2002, 19:344-360.
34. Luh W.M., Wong E.C., Bandettini P.A., Hyde J.S. QUIPSS II with thin-slice TI1 periodic saturation: a method for improving accuracy of quantitative perfusion imaging using pulsed arterial spin labeling. Magn. Reson. Med. 1999, 41:1246-1254.
35. Lutz K., Koeneke S., Wustenberg T., Jancke L. Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci. Lett. 2005, 373:61-66.
36. McAllister S.M., Rothwell J.C., Ridding M.C. Cortical oscillatory activity and the induction of plasticity in the human motor cortex. Eur. J. Neurosci. 2011, 33:1916-1924.
37. Moisa M., Pohmann R., Uludag K., Thielscher A. Interleaved TMS/CASL: comparison of different rTMS protocols. Neuroimage 2010, 49:612-620.
38. Nyffeler T., Wurtz P., Pflugshaupt T., von W.R., Luthi M., Hess C.W., Muri R.M. One-Hertz transcranial magnetic stimulation over the frontal eye field induces lasting inhibition of saccade triggering. Neuroreport 2006, 17:273-275.
39. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
40. Pascual-Leone A., Bartres-Faz D., Keenan J.P. Transcranial magnetic stimulation: studying the brain-behaviour relationship by induction of 'virtual lesions'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:1229-1238.
41. Pascual-Leone A., Walsh V., Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience-virtual lesion, chronometry, and functional connectivity. Curr. Opin. Neurobiol. 2000, 10:232-237.
42. Paus T., Jech R., Thompson C.J., Comeau R., Peters T., Evans A.C. Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J. Neurosci. 1997, 17:3178-3184.
43. Ridding M.C., Rothwell J.C. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nat. Rev. Neurosci. 2007, 8:559-567.
44. Ridding M.C., Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J. Physiol. 2010, 588:2291-2304.
45. Rogers B., Zhang W., Narayana S., Lancaster J.L., Robin D.A., Fox P.T. Force sensing system for automated assessment of motor performance during fMRI. J. Neurosci. Methods 2010, 190:92-94.
46. Rossi S., Pasqualetti P., Rossini P.M., Feige B., Ulivelli M., Glocker F.X., Battistini N., Lucking C.H., Kristeva-Feige R. Effects of repetitive transcranial magnetic stimulation on movement-related cortical activity in humans. Cereb. Cortex 2000, 10:802-808.
47. Rossi S., Rossini P.M. TMS in cognitive plasticity and the potential for rehabilitation. Trends Cogn. Sci. 2004, 8:273-279.
48. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 2009, 120:2008-2039.
49. Rounis E., Lee L., Siebner H.R., Rowe J.B., Friston K.J., Rothwell J.C., Frackowiak R.S. Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage 2005, 26:164-176.
50. Ruff C.C., Driver J., Bestmann S. Combining TMS and fMRI: from 'virtual lesions' to functional-network accounts of cognition. Cortex 2009, 45:1043-1049.
51. Sadato N., Campbell G., Ibanez V., Deiber M., Hallett M. Complexity affects regional cerebral blood flow change during sequential finger movements. J. Neurosci. 1996, 16:2691-2700.
52. Siebner H.R., Willoch F., Peller M., Auer C., Boecker H., Conrad B., Bartenstein P. Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation. Neuroreport 1998, 9:943-948.
53. Siebner H.R., Takano B., Peinemann A., Schwaiger M., Conrad B., Drzezga A. Continuous transcranial magnetic stimulation during positron emission tomography: a suitable tool for imaging regional excitability of the human cortex. Neuroimage 2001, 14:883-890.
54. Siebner H.R., Hartwigsen G., Kassuba T., Rothwell J.C. How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition. Cortex 2009, 45:1035-1042.
55. Stefan K., Wycislo M., Gentner R., Schramm A., Naumann M., Reiners K., Classen J. Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb. Cortex 2006, 16:376-385.
56. Stefan K., Gentner R., Zeller D., Dang S., Classen J. Theta-burst stimulation: remote physiological and local behavioral after-effects. Neuroimage 2008, 40:265-274.
57. Stein M., Federspiel A., Koenig T., Wirth M., Strik W., Wiest R., Brandeis D., Dierks T. Structural plasticity in the language system related to increased second language proficiency. Cortex 2012, 48(4):458-465. (Apr).
58. Strafella A.P., Paus T. Cerebral blood-flow changes induced by paired-pulse transcranial magnetic stimulation of the primary motor cortex. J. Neurophysiol. 2001, 85:2624-2629.
59. Suppa A., Ortu E., Zafar N., Deriu F., Paulus W., Berardelli A., Rothwell J.C. Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. J. Physiol. 2008, 586:4489-4500.
60. A Stereotactic Coplanar Atlas of the Human Brain 1988, Thieme, Stuttgart. J. Talairach, P. Tournoux (Eds.).
61. Talelli P., Greenwood R.J., Rothwell J.C. Exploring theta burst stimulation as an intervention to improve motor recovery in chronic stroke. Clin. Neurophysiol. 2007, 118:333-342.
62. Tinazzi M., Zanette G. Modulation of ipsilateral motor cortex in man during unimanual finger movements of different complexities. Neurosci. Lett. 1998, 244:121-124.
63. Verstynen T., Diedrichsen J., Albert N., Aparicio P., Ivry R.B. Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J. Neurophysiol. 2005, 93:1209-1222.
64. Wang J., Alsop D.C., Song H.K., Maldjian J.A., Tang K., Salvucci A.E., Detre J.A. Arterial transit time imaging with flow encoding arterial spin tagging (FEAST). Magn. Reson. Med. 2003, 50:599-607.
65. Wassermann E.M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr. Clin. Neurophysiol. 1998, 108:1-16.
66. Wu W.C., Fernandez-Seara M., Detre J.A., Wehrli F.W., Wang J. A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn. Reson. Med. 2007, 58:1020-1027.