Inter-individual variability in cortical excitability and motor network connectivity following multiple blocks of rTMS

NeuroImage

Volumn 118, Issue , 2015, Pages 209-218

  Nettekoven, Charlotte ^a,b   Volz, Lukas J ^b   Leimbach, Martha ^b   Pool, Eva Maria ^a,b   Rehme, Anne K ^a,b   Eickhoff, Simon B ^a,c   Fink, Gereon R ^a,b   Grefkes, Christian ^a,b  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cortical plasticity; Dose dependency; DPMC; SMA; Variability

Indexed keywords

ADULT; ARTICLE; CONNECTOME; CONTROLLED STUDY; EVOKED MUSCLE RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INTERMITTENT THETA BURST STIMULATION; MALE; NERVE EXCITABILITY; NEUROIMAGING; NORMAL HUMAN; PREMOTOR CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; TRANSCRANIAL MAGNETIC STIMULATION; MOTOR CORTEX; MOTOR EVOKED POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PHYSIOLOGY; PROCEDURES; SKELETAL MUSCLE; YOUNG ADULT;

ADULT; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; MUSCLE, SKELETAL; NERVE NET; NEURONAL PLASTICITY; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84935024294     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.06.004     Document Type: Article

References (44)

1. Ameli M., Grefkes C., Kemper F., Riegg F.P., Rehme A.K., Karbe H., Fink G.R., Nowak D.A. 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.
2. Andoh J., Zatorre R.J. Interhemispheric connectivity influences the degree of modulation of TMS-induced effects during auditory processing. Front. Psychol. 2011, 2:161.
3. Andoh J., Zatorre R.J. Mapping interhemispheric connectivity using functional MRI after transcranial magnetic stimulation on the human auditory cortex. NeuroImage 2013, 79:162-171.
4. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26:839-851.
5. Benali A., Trippe J., Weiler E., Mix A., Petrasch-Parwez E., Girzalsky W., Eysel U.T., Erdmann R., Funke K. Theta-burst transcranial magnetic stimulation alters cortical inhibition. J. Neurosci. 2011, 31:1193-1203.
6. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 1995, 57:289-300.
7. Cárdenas-Morales L., Volz L.J., Michely J., Rehme A.K., Pool E.M., Nettekoven C., Eickhoff S.B., Fink G.R., Grefkes C. Network connectivity and individual responses to brain stimulation in the human motor system. Cereb. Cortex 2014, 24(7):1697-1707.
8. Di Lazzaro V., Ziemann U. The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front. Neural Circ. 2013, 7:18.
9. Di Lazzaro V., Profice P., Ranieri F., Capone F., Dileone M., Oliviero A., Pilato F. I-wave origin and modulation. Brain Stimul. 2012, 5:512-525.
10. Downar J., Geraci J., Salomons T.V., Dunlop K., Wheeler S., McAndrews M.P., Bakker N., Blumberger D.M., Daskalakis Z.J., Kennedy S.H., Flint A.J., Giacobbe P. Anhedonia and reward-circuit connectivity distinguish nonresponders from responders to dorsomedial prefrontal repetitive transcranial magnetic stimulation in major depression. Biol. Psychiatry 2014, 76:176-185.
11. Eickhoff S.B., Grefkes C. Approaches for the integrated analysis of structure, function and connectivity of the human brain. Clin. EEG Neurosci. 2011, 42:107-121.
12. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 2005, 25:1325-1335.
13. Funke K., Benali A. Modulation of cortical inhibition by rTMS - findings obtained from animal models. J. Physiol. 2011, 589:4423-4435.
14. 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.
15. Gharabaghi A., Kraus D., Leao M.T., Spuler M., Walter A., Bogdan M., Rosenstiel W., Naros G., Ziemann U. Coupling brain-machine interfaces with cortical stimulation for brain-state dependent stimulation: enhancing motor cortex excitability for neurorehabilitation. Front. Hum. Neurosci. 2014, 8:122.
16. Goldsworthy M.R., Muller-Dahlhaus F., Ridding M.C., Ziemann U. Inter-subject variability of LTD-like plasticity in human motor cortex: a matter of preceding motor activation. Brain Stimul. 2014, 7(6):864-870.
17. Grefkes C., Nowak D.A., Wang L.E., Dafotakis M., Eickhoff S.B., Fink G.R. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. NeuroImage 2010, 50:233-242.
18. Hamada M., Murase N., Hasan A., Balaratnam M., Rothwell J.C. The role of interneuron networks in driving human motor cortical plasticity. Cereb. Cortex 2013, 23:1593-1605.
19. Herwig U., Fallgatter A.J., Hoppner J., Eschweiler G.W., Kron M., Hajak G., Padberg F., Naderi-Heiden A., Abler B., Eichhammer P., Grossheinrich N., Hay B., Kammer T., Langguth B., Laske C., Plewnia C., Richter M.M., Schulz M., Unterecker S., Zinke A., Spitzer M., Schonfeldt-Lecuona C. Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial. Br. J. Psychiatry 2007, 191:441-448.
20. Herwig U., Cardenas-Morales L., Connemann B.J., Kammer T., Schönfeldt-Lecuona C. Sham or real - post hoc estimation of stimulation condition in a randomized transcranial magnetic stimulation trial. Neurosci. Lett. 2010, 471:30-33.
21. Hinder M.R., Goss E.L., Fujiyama H., Canty A.J., Garry M.I., Rodger J., Summers J.J. Inter- and intra-individual variability following intermittent theta burst stimulation: implications for rehabilitation and recovery. Brain Stimul. 2014, 7:365-371.
22. 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.
23. 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.
24. Huang Y.Z., Rothwell J.C., Lu C.S., Wang J., Chen R.S. Restoration of motor inhibition through an abnormal premotor-motor connection in dystonia. Mov. Disord. 2010, 25:696-703.
25. Koch G., Schneider S., Baumer T., Franca M., Munchau A., Cheeran B., Fernandez del Olmo M., Cordivari C., Rounis E., Caltagirone C., Bhatia K., Rothwell J.C. Altered dorsal premotor-motor interhemispheric pathway activity in focal arm dystonia. Mov. Disord. 2008, 23:660-668.
26. Lemon R.N. Descending pathways in motor control. Annu. Rev. Neurosci. 2008, 31:195-218.
27. López-Alonso V., Cheeran B., Rio-Rodriguez D., Fernandez-Del-Olmo M. Inter-individual variability in response to non-invasive brain stimulation paradigms. Brain Stimul. 2014, 7:372-380.
28. Martin P.G., Gandevia S.C., Taylor J.L. Theta burst stimulation does not reliably depress all regions of the human motor cortex. Clin. Neurophysiol. 2006, 117:2684-2690.
29. Nettekoven C., Volz L.J., Kutscha M., Pool E.M., Rehme A.K., Eickhoff S.B., Fink G.R., Grefkes C. Dose-dependent effects of theta burst rTMS on cortical excitability and resting-state connectivity of the human motor system. J. Neurosci. 2014, 34:6849-6859.
30. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
31. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 2012, 59:2142-2154.
32. Quartarone A., Bagnato S., Rizzo V., Siebner H.R., Dattola V., Scalfari A., Morgante F., Battaglia F., Romano M., Girlanda P. Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain 2003, 126:2586-2596.
33. 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.
34. Salomons T.V., Dunlop K., Kennedy S.H., Flint A., Geraci J., Giacobbe P., Downar J. Resting-state cortico-thalamic-striatal connectivity predicts response to dorsomedial prefrontal rTMS in major depressive disorder. Neuropsychopharmacology 2014, 39:488-498.
35. Sarfeld A.S., Diekhoff S., Wang L.E., Liuzzi G., Uludag K., Eickhoff S.B., Fink G.R., Grefkes C. Convergence of human brain mapping tools: neuronavigated TMS parameters and fMRI activity in the hand motor area. Hum. Brain Mapp. 2012, 33:1107-1123.
36. Satterthwaite T.D., Elliott M.A., Gerraty R.T., Ruparel K., Loughead J., Calkins M.E., Eickhoff S.B., Hakonarson H., Gur R.C., Gur R.E., Wolf D.H. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. NeuroImage 2012, 64:240-256.
37. Shimazu H., Maier M.A., Cerri G., Kirkwood P.A., Lemon R.N. Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J. Neurosci. 2004, 24:1200-1211.
38. 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.
39. van der Werf Y.D., Sanz-Arigita E.J., Menning S., van den Heuvel O.A. Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation. BMC Neurosci. 2011, 11:145.
40. Vercammen A., Knegtering H., Liemburg E.J., den Boer J.A., Aleman A. Functional connectivity of the temporo-parietal region in schizophrenia: effects of rTMS treatment of auditory hallucinations. J. Psychiatr. Res. 2010, 44:725-731.
41. Volz L.J., Benali A., Mix A., Neubacher U., Funke K. Dose-dependence of changes in cortical protein expression induced with repeated transcranial magnetic theta-burst stimulation in the rat. Brain Stimul. 2013, 6:598-606.
42. Volz L.J., Hamada M., Rothwell J.C., Grefkes C. What makes the muscle twitch: motor system connectivity and TMS-induced activity. Cereb. Cortex 2014, 10.1093/cercor/bhu032.
43. Watanabe T., Hanajima R., Shirota Y., Ohminami S., Tsutsumi R., Terao Y., Ugawa Y., Hirose S., Miyashita Y., Konishi S., Kunimatsu A., Ohtomo K. Bidirectional effects on interhemispheric resting-state functional connectivity induced by excitatory and inhibitory repetitive transcranial magnetic stimulation. Hum. Brain Mapp. 2014, 35(5):1896-1905.
44. zu Eulenburg P., Caspers S., Roski C., Eickhoff S.B. Meta-analytical definition and functional connectivity of the human vestibular cortex. NeuroImage 2012, 60:162-169.