Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling

NeuroImage

Volumn 50, Issue 1, 2010, Pages 233-242

  Grefkes, Christian ^a,b   Nowak, Dennis A ^b,c   Wang, Ling E ^d   Dafotakis, Manuel ^b   Eickhoff, Simon B ^d,e   Fink, Gereon R ^b,d  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c Klinik Kipfenberg   (Germany)

^d JÜLICH RESEARCH CENTRE   (Germany)

^e UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

DCM; FMRI; Rehabilitation; Transcranial magnetic stimulation

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CAUSAL MODELING; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HEMISPHERE; HUMAN; MALE; MOTOR CORTEX; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOTOR SYSTEM; NERVE CELL NETWORK; NEUROMODULATION; PARESIS; PRIORITY JOURNAL; STROKE PATIENT; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; CEREBRAL CORTEX; FEMALE; FRONTAL LOBE; HAND; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; MOTOR CORTEX; NEURAL PATHWAYS; PARESIS; STROKE; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 75449092611     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.12.029     Document Type: Article

References (64)

1. Ameli M., Grefkes C., Kemper F., Riegg F., Rehme A.K., Karbe H., Fink G.R., and Nowak D.A. Differential effects of high-frequency rTMS over ipsilesional primary motor cortex in cortical and subcortical MCA stroke. Ann. Neurol. 66 3 (2009) 298-309
2. Ashburner J., and Friston K. Unified segmentation. Neuroimage 26 (2005) 839-851
3. Biernaskie J., Szymanska A., Windle V., and Corbett D. Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. J. Neurosci. 21 (2005) 989-999
4. Bonita R., and Beaglehole R. Modification of Rankin Scale: recovery of motor function after stroke. Stroke 19 (1988) 1497-1500
5. Bestmann S., Baudewig J., Siebner H.R., Rothwell J.C., and Frahm J. BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage 28 (2005) 22-29
6. Boussaoud D., Tanne-Gariepy J., Wannier T., and Rouiller E.M. Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study. BMC Neurosci. 6 (2005) 67
7. Brott T., Adams Jr. H.P., Olinger C.P., Marler J.R., Barsan W.G., Biller J., Spilker J., Holleran R., Eberle R., and Hertzberg V. Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20 (1989) 864-870
8. Bütefisch C.M., Kleiser R., Müller K., Wittsack H.J., Hömberg V., and Seitz R.J. Recruitment of contralesional motor cortex in stroke patients with recovery of hand function. Neurology 64 (2005) 1067-1069
9. Carey J.R., Kimberley T.J., Lewis S.M., Auerbach E.J., Dorsey L., Rundquist P., and Ugurbil K. Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125 (2002) 773-788
10. Chen W.H., Mima T., Siebner H.R., Oga T., Hidemi H., Satow T., Begum T., Nagamine T., and Shibasaki H. Low-frequency rTMS over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas. Clin. Neurophysiol. 114 (2003) 1628-1637
11. Chollet F., DiPiero V., Wise R.J., Brooks D.J., Dolan R.J., and Frackowiak R.S. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann. Neurol. 29 (1991) 63-71
12. Chouinard P.A., Van Der Werf Y.D., Leonard G., and Paus T. Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J. Neurophysiol. 90 (2003) 1071-1083
13. Conchou F., Loubinoux I., Castel-Lacanal E., Le T.A., Gerdelat-Mas A., Faure-Marie N., Gros H., Thalamas C., Calvas F., Berry I., Chollet F., and Simonetta M.M. 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 (2009) 2542-2557
14. Dum R.P., and Strick P.L. Motor areas in the frontal lobe of the primate. Physiol. Behav. 77 (2002) 677-682
15. Duque J., Hummel F., Celnik P., Murase N., Mazzocchio R., and Cohen L.G. Transcallosal inhibition in chronic subcortical stroke. Neuroimage 28 (2005) 940-946
16. Eickhoff S.B., Dafotakis M., Grefkes C., Shah N.J., Zilles K., and Piza-Katzer H. Central adaptation following heterotopic hand replantation probed by fMRI and effective connectivity analysis. Exp. Neurol. 212 (2008) 132-144
17. Eickhoff S.B., Heim S., Zilles K., and Amunts K. A systems perspective on the effective connectivity of overt speech production. Philos. Transact. A Math Phys. Eng. Sci. 367 (2009) 2399-2421
18. Feydy A., Carlier R., Roby-Brami A., Bussel B., Cazalis F., Pierot L., Burnod Y., and Maier M.A. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 33 6 (2002) 1610-1617
19. Folstein M.F., Folstein S.E., and McHugh P.R. Mini-Mental State. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 (1975) 189-198
20. Friston K.J., Harrison L., and Penny W. Dynamic causal modelling. Neuroimage 19 (2003) 1273-1302
21. Gilio F., Rizzo V., Siebner H.R., and Rothwell J.C. Effects on the right motor hand-area excitability produced by low-frequency rTMS over human contralateral homologous cortex. J. Physiol. 551 (2003) 563-573
22. Grefkes C., Eickhoff S.B., Nowak D.A., Dafotakis M., and Fink G.R. Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 41 (2008) 1382-1394
23. Grefkes C., Nowak D.A., Eickhoff S.B., Dafotakis M., Kust J., Karbe H., and Fink G.R. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann. Neurol. 63 (2008) 236-246
24. Grefkes, C., Wang, L.E., Eickhoff, S.B., Fink, G.R., 2009. Noradrenergic modulation of cortical networks engaged in visuomotor processing. Cereb Cortex. in press doi:10.1093/cercor/bhp144.
25. Hummel F.C., and Cohen L.G. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke?. Lancet Neurol. 5 (2006) 708-712
26. Jantzen K.J., Steinberg F.L., and Kelso J.A.S. Functional MRI reveals the existence of modality and coordination-dependent timing networks. Neuroimage 25 (2005) 1031-1042
27. Jenkins I.H., Jahanshahi M., Jueptner M., Passingham R.E., and Brooks D.J. Self-initiated versus externally triggered movements II. The effect of movement predictability on regional cerebral blood flow. Brain 123 Pt. 6 (2000) 1216-1228
28. Johansen-Berg H., Rushworth M.F., Bogdanovic M.D., Kischka U., Wimalaratna S., and Matthews P.M. The role of ipsilateral premotor cortex in hand movement after stroke. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 14518-14523
29. Kiebel S., and Holmes A. The General Linear Model. In: Frackowiak R.S., Friston K., Frith C.D., Dolan R.J., Price C.J., Zeki S., Ashburner J., and Penny W. (Eds). Human Brain Function. 2nd edition (2004), Elsevier Academic Press, San Diego 725-761
30. Komitova M., Johansson B.B., and Eriksson P.S. On neural plasticity, new neurons and the postischemic milieu: an integrated view on experimental rehabilitation. Exp. Neurol. 199 (2006) 42-55
31. Kwakkel G., Kollen B.J., and Wagenaar R.C. Long term effects of intensity of upper and lower limb training after stroke: a randomised trial. J. Neurol. Neurosurg. Psychiatry 72 (2002) 473-479
32. Lee L., Siebner H.R., Rowe J.B., Rizzo V., Rothwell J.C., Frackowiak R.S., and Friston K.J. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J. Neurosci. 23 (2003) 5308-5318
33. Lotze M., Markert J., Sauseng P., Hoppe J., Plewnia C., and Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J. Neurosci. 26 (2006) 6096-6102
34. Luppino G., Matelli M., Camarda R., and Rizzolatti G. Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J. Comp. Neurol. 1993 (1993) 114-140
35. Lyle R.C. A performance test for assessment of upper limb function in physical rehabilitation treatment and research. Int. J. Rehabil. Res. 4 (1981) 483-492
36. Maeda F., Keenan J.P., Tormos J.M., Topka H., and Pascual-Leone A. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin. Neurophysiol. 111 (2000) 800-805
37. Mansur C.G., Fregni F., Boggio P.S., Riberto M., Gallucci-Neto J., Santos C.M., Wagner T., Rigonatti S.P., Marcolin M.A., and Pascual-Leone A. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64 (2005) 1802-1804
38. Marshall R.S., Perera G.M., Lazar R.M., Krakauer J.W., Constantine R.C., and DeLaPaz R.L. Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31 (2000) 656-661
39. McGuire P.K., Bates J.F., and Goldman-Rakic P.S. Interhemispheric integration: I. Symmetry and convergence of the corticocortical connections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) in the rhesus monkey. Cereb. Cortex 1 (1991) 390-407
40. Murase N., Duque J., Mazzocchio R., and Cohen L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 55 (2004) 400-409
41. Nelles G. Cortical reorganization-effects of intensive therapy. Restor. Neurol. Neurosci. 22 (2004) 239-244
42. Nowak D.A., Grefkes C., Dafotakis M., Küst J., Karbe H., and Fink G.R. Improving dexterity following stroke: effects of low-frequency rTMS over contralesional M1 on movement kinematics and neural activity in subcortical stroke. Arch. Neurol. 65 (2008) 741-747
43. O'Shea J., Johansen-Berg H., Trief D., Gobel S., and Rushworth M.F. Functionally specific reorganization in human premotor cortex. Neuron 54 (2007) 479-490
44. Pal P.K., Hanajima R., Gunraj C.A., Li J.Y., Wagle-Shukla A., Morgante F., and Chen R. Effect of low-frequency repetitive transcranial magnetic stimulation on interhemispheric inhibition. J. Neurophysiol. 94 (2005) 1668-1675
45. Passingham R.E., Chen Y.C., and Thaler D. Supplementary motor cortex and self-initiated movement. In: Ito M. (Ed). Neural Programming (1989), Karger, Tokyo 13-24
46. Penny W.D., Stephan K.E., Mechelli A., and Friston K.J. Modelling functional integration: a comparison of structural equation and dynamic causal models. Neuroimage 23 Suppl. 1 (2004) S264-S274
47. Pleger B., Blankenburg F., Bestmann S., Ruff C.C., Wiech K., Stephan K.E., Friston K.J., and Dolan R.J. Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans. J. Neurosci. 26 (2006) 1945-1952
48. Rizzolatti G., Luppino G., and Matelli M. The organization of the cortical motor system: new concepts. Neuron 31 (1998) 889-901
49. Rouiller E.M., Babalian A., Kazennikov O., Moret V., Yu X.H., and Wiesendanger M. Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys. Exp. Brain Res. 102 (1994) 227-243
50. Rowe J.B., Siebner H., Filipovic S.R., Cordivari C., Gerschlager W., Rothwell J., and Frackowiak R. Aging is associated with contrasting changes in local and distant cortical connectivity in the human motor system. Neuroimage 32 (2006) 747-760
51. Schubotz R.I., and von Cramon D.Y. Functional-Anatomical concepts of human premotor cortex: evidence from fMRI and PET studies. Neuroimage 20 Suppl. 1 (2003) S120-S131
52. Siebner H.R., Peller M., and Lee L. Applications of combined TMS-PET studies in clinical and basic research. Suppl. Clin. Neurophysiol. 56 (2003) 63-72
53. Sparing R., Buelte D., Meister I.G., Paus T., and Fink G.R. Transcranial magnetic stimulation and the challenge of coil placement: a comparison of conventional and stereotaxic neuronavigational strategies. Hum. Brain Mapp. 29 1 (2008) 82-96
54. Stephan K.E., Fink G.R., and Marshall J.C. Mechanisms of hemispheric specialization: insights from analyses of connectivity. Neuropsychologia 45 (2007) 209-228
55. Stephan K.E., Weiskopf N., Drysdale P.M., Robinson P.A., and Friston K.J. Comparing hemodynamic models with DCM. Neuroimage 38 (2007) 387-401
56. Stephan K.E., Penny W.D., Daunizeau J., Moran R.J., and Friston K.J. Bayesian model selection for group studies. Neuroimage 46 4 (2009) 1004-1017
57. Takeuchi N., Chuma T., Matsuo Y., Watanabe I., and Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36 (2005) 2681-2686
58. Talelli P., and Rothwell J. Does brain stimulation after stroke have a future?. Curr. Opin. Neurol. 19 (2006) 543-550
59. Tomassini V., Jbabdi S., Klein J.C., Behrens T.E., Pozzilli C., Matthews P.M., Rushworth M.F., and Johansen-Berg H. Diffusion-weighted imaging tractography-based parcellation of the human lateral premotor cortex identifies dorsal and ventral subregions with anatomical and functional specializations. J. Neurosci. 27 38 (2007) 10259-10269
60. Ward N.S., Brown M.M., Thompson A.J., and Frackowiak R.S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 126 (2003) 2476-2496
61. Weber R., Ramos-Cabrer P., Justicia C., Wiedermann D., Strecker C., Sprenger C., and Hoehn M. Early prediction of functional recovery after experimental stroke: functional magnetic resonance imaging, electrophysiology, and behavioral testing in rats. J. Neurosci. 28 (2008) 1022-1029
62. Weiller C., Chollet F., Friston K.J., Wise R.J., and Frackowiak R.S.J. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann. Neurol. 31 (1992) 463-472
63. Zeki S., Watson J.D., Lueck C.J., Friston K.J., Kennard C., and Frackowiak R.S. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11 (1991) 641-649
64. Ziemann U. Improving disability in stroke with rTMS. Lancet Neurol 4 (2005) 454-455