Dose-dependent effects of theta burst rTMS on cortical excitability and resting-state connectivity of the human motor system

Journal of Neuroscience

Volumn 34, Issue 20, 2014, Pages 6849-6859

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

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Functional connectivity; iTBS; Neural plasticity; Premotor cortex; Resting state fMRI; Supplementary motor area

Indexed keywords

GLUTAMATE DECARBOXYLASE 65;

ADULT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ECHO PLANAR IMAGING; EVOKED MUSCLE RESPONSE; EVOKED SOMATOSENSORY RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GABAERGIC TRANSMISSION; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; LONG TERM POTENTIATION; MALE; MOTOR SYSTEM; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE EXCITABILITY; NORMAL HUMAN; PERCEPTIVE THRESHOLD; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

FUNCTIONAL CONNECTIVITY; ITBS; NEURAL PLASTICITY; PREMOTOR CORTEX; RESTING-STATE FMRI; SUPPLEMENTARY MOTOR AREA;

ADULT; CROSS-OVER STUDIES; EVOKED POTENTIALS, MOTOR; FEMALE; HUMANS; MALE; MOTOR CORTEX; NERVE NET; NEURONAL PLASTICITY; SINGLE-BLIND METHOD; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84900405302     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4993-13.2014     Document Type: Article

References (65)

1. Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26:839-851. CrossRef Medline
2. Benali A, Trippe J, Weiler E, Mix A, Petrasch-Parwez E, Girzalsky W, Eysel UT, Erdmann R, Funke K (2011) Theta burst transcranial magnetic stimulation alters cortical inhibition. J Neurosci 31:1193-1203. CrossRef Medline
3. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, 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. CrossRef Medline
4. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2004) Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci 19:1950-1962. CrossRef Medline
5. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J (2005) BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage 28:22-29. CrossRef Medline
6. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48. Medline
7. Cárdenas-Morales L, Grön G, Kammer T (2011) Exploring the aftereffects of theta burst magnetic stimulation on the human motor cortex: a functional imaging study. HumBrain Mapp 32:1948-1960. CrossRef Medline
8. Cárdenas-Morales L, Volz LJ, Michely J, Rehme AK, Pool EM, Nettekoven C, Eickhoff SB, Fink GR, Grefkes C (2013) Network connectivity and individual responses to brain stimulation in the human motor system. Cereb Cortex. Advance online publication. Retrieved Feb. 8, 2013. doi: 10.1093/ cercor/bht023. CrossRef Medline
9. Carroll TJ, Riek S, Carson RG (2001) Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods 112:193-202. CrossRef Medline
10. Chen R, Tam A, Bütefisch C, Corwell B, Ziemann U, Rothwell JC, Cohen LG (1998) Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol 80:2870-2881. Medline
11. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC (2004) The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115: 255-266. CrossRef Medline
12. Di Lazzaro V, Pilato F, Saturno E, Oliviero A, Dileone M, Mazzone P, Insola A, Tonali PA, Ranieri F, Huang YZ, Rothwell JC (2005) Theta burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 565:945-950. CrossRef Medline
13. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P, Insola A, Ranieri F, Meglio M, Tonali PA, Rothwell JC (2008) The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586:3871-3879. CrossRef Medline
14. Di Lazzaro V, Profice P, Ranieri F, Capone F, Dileone M, Oliviero A, Pilato F (2012) I-wave origin and modulation. Brain Stimul 5:512-525. CrossRef Medline
15. Eickhoff SB, Grefkes C (2011) Approaches for the integrated analysis of structure, function and connectivity of the human brain. Clin EEG Neurosci 42:107-121. CrossRef Medline
16. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325-1335. CrossRef Medline
17. Eldaief MC, Halko MA, Buckner RL, Pascual-Leone A (2011) Transcranial magnetic stimulation modulates the brain's intrinsic activity in a frequency-dependent manner. Proc Natl Acad Sci U S A 108:21229-21234. CrossRef Medline
18. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474-480. CrossRef Medline
19. Funke K, Benali A (2011) Modulation of cortical inhibition by rTMS: findings obtained from animal models. J Physiol 589:4423-4435. Medline
20. Gamboa OL, Antal A, Moliadze V, Paulus W (2010) Simply longer is not better: reversal of theta burst aftereffect with prolonged stimulation. Exp Brain Res 204:181-187. CrossRef Medline
21. Gamboa OL, Antal A, Laczo B, Moliadze V, Nitsche MA, Paulus W (2011) Impact of repetitive theta burst stimulation on motor cortex excitability. Brain Stimul 4:145-151. CrossRef Medline
22. Gentner R, Wankerl K, Reinsberger C, Zeller D, Classen J (2008) Depression of human corticospinal excitability induced by magnetic theta burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex 18:2046-2053. CrossRef Medline
23. Geyer S, Matelli M, Luppino G, ZillesK (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol (Berl) 202:443-474. CrossRef Medline
24. Grefkes C, Nowak DA, Wang LE, Dafotakis M, Eickhoff SB, Fink GR (2010) Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage 50:233-242. CrossRef Medline
25. Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC (2013) The role of interneuron networks in driving human motor cortical plasticity. Cereb Cortex 23:1593-1605. CrossRef Medline
26. Herwig U, Fallgatter AJ, Höppner J, Eschweiler GW, 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 MM, Schulz M, Unterecker S, Zinke A, et al. (2007) Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial. Br J Psychiatry 191:441-448. CrossRef Medline
27. Herwig U, Cárdenas-Morales L, Connemann BJ, Kammer T, Schönfeldt-Lecuona C (2010) Sham or real: post hoc estimation of stimulation condition in a randomized transcranial magnetic stimulation trial. Neurosci Lett 471:30-33. CrossRef Medline
28. Hoppenrath K, FunkeK (2013) Time-course of changes in neuronal activity markers following iTBS-TMS of the rat neocortex. Neurosci Lett 536:19-23. CrossRef Medline
29. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201-206. CrossRef Medline
30. Huang YZ, Chen RS, Rothwell JC, Wen HY (2007) The aftereffect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 118:1028-1032. CrossRef Medline
31. Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18:563-570. CrossRef Medline
32. Jakobs O, Langner R, Caspers S, Roski C, Cieslik EC, Zilles K, Laird AR, Fox PT, Eickhoff SB (2012) Across-study and within-subject functional connectivity of a right temporo-parietal junction subregion involved in stimulus-context integration. Neuroimage 60:2389-2398. CrossRef Medline
33. Kobayashi M, Hutchinson S, Théoret H, Schlaug G, Pascual-Leone A (2004) RepetitiveTMSof the motor cortex improves ipsilateral sequential simple finger movements. Neurology 62:91-98. CrossRef Medline
34. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501-519. Medline
35. Nomura EM, Gratton C, Visser RM, Kayser A, Perez F, D'EspositoM (2010) Double dissociation of two cognitive control networks in patients with focal brain lesions. Proc Natl Acad Sci U S A 107:12017-12022. CrossRef Medline
36. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113. CrossRef Medline
37. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Cañete C, Catalá MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333-343. CrossRef Medline
38. Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377-401. CrossRef Medline
39. Paus T, WolforthM (1998) Transcranial magnetic stimulation during PET: reaching and verifying the target site. Hum Brain Mapp 6:399-402. CrossRef Medline
40. Ragert P, Franzkowiak S, Schwenkreis P, Tegenthoff M, Dinse HR (2008) Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex. Exp Brain Res 184:1-11. CrossRef Medline
41. Reetz K, Dogan I, Rolfs A, Binkofski F, Schulz JB, Laird AR, Fox PT, Eickhoff SB (2012) Investigating function and connectivity of morphometric findings: exemplified on cerebellar atrophy in spinocerebellar ataxia 17 (SCA17). Neuroimage 62:1354-1366. CrossRef Medline
42. Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588:2291-2304. CrossRef Medline
43. Sarfeld AS, Diekhoff S, Wang LE, Liuzzi G, Uluda{eth} K, Eickhoff SB, Fink GR, Grefkes C (2012) Convergence of human brain mapping tools: neuronavigated TMS parameters and fMRI activity in the hand motor area. Hum Brain Mapp 33:1107-1123. CrossRef Medline
44. Satterthwaite TD, Elliott MA, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RC, Gur RE, Wolf DH (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240-256. CrossRef Medline
45. Sharma N, Baron JC, Rowe JB (2009) Motor imagery after stroke: relating outcome to motor network connectivity. Ann Neurol 66:604-616. CrossRef Medline
46. Siebner HR, Peller M, Willoch F, Minoshima S, Boecker H, Auer C, Drzezga A, Conrad B, Bartenstein P (2000) Lasting cortical activation after repetitive TMS of the motor cortex: a glucose metabolic study. Neurology 54:956-963. CrossRef Medline
47. Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21:1-10. CrossRef Medline
48. Soghomonian JJ, Martin DL (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19:500-505. CrossRef Medline
49. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, Bestmann S (2009) Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 101: 2872-2877. CrossRef Medline
50. Stefan K, Gentner R, Zeller D, Dang S, Classen J (2008) Theta burst stimulation: remote physiological and local behavioral aftereffects. Neuroimage 40:265-274. CrossRef Medline
51. Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330:238-271. CrossRef Medline
52. Suppa A, Ortu E, Zafar N, Deriu F, Paulus W, Berardelli A, Rothwell JC (2008) Theta burst stimulation induces aftereffects on contralateral primary motor cortex excitability in humans. J Physiol 586:4489-4500. CrossRef Medline
53. Teo JT, Swayne OB, Rothwell JC (2007) Further evidence for NMDA dependence of the aftereffects of human theta burst stimulation. Clin Neurophysiol 118:1649-1651. CrossRef Medline
54. Terao Y, Ugawa Y (2002) Basic mechanisms of TMS. J Clin Neurophysiol 19:322-343. CrossRef Medline
55. van der Werf YD, Sanz-Arigita EJ, Menning S, van den Heuvel OA (2011) Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation. BMC Neurosci 11:145. CrossRef Medline
56. Veniero D, Ponzo V, Koch G (2013) Paired associative stimulation enforces the communication between interconnected areas. J Neurosci 33:13773-13783. CrossRef Medline
57. Vercammen A, Knegtering H, Liemburg EJ, den Boer JA, Aleman A (2010) Functional connectivity of the temporo-parietal region in schizophrenia: effects of rTMS treatment of auditory hallucinations. J Psychiatr Res 44: 725-731. CrossRef Medline
58. Volz LJ, Benali A, Mix A, Neubacher U, FunkeK (2013) Dose dependence of changes in cortical protein expression induced with repeated transcranial magnetic theta burst stimulation in the rat. Brain Stimul 6:598-606. CrossRef Medline
59. Wassermann EM (1998) 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 108:1-16. CrossRef Medline
60. Watanabe T, Hanajima R, Shirota Y, Ohminami S, Tsutsumi R, Terao Y, Ugawa Y, Hirose S, Miyashita Y, Konishi S, Kunimatsu A, Ohtomo K (2014) Bidirectional effects on interhemispheric resting-state functional connectivity induced by excitatory and inhibitory repetitive transcranial magnetic stimulation. Hum Brain Mapp 35:1896-1905. CrossRef Medline
61. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus: a new landmark. Brain 120:141-157. CrossRef Medline
62. Zafar N, Paulus W, SommerM (2008) Comparative assessment of best conventional with best theta burst repetitive transcranial magnetic stimulation protocols on human motor cortex excitability. Clin Neurophysiol 119:1393-1399. CrossRef Medline
63. Zeller D, Dang SY, Weise D, Rieckmann P, Toyka KV, Classen J (2012) Excitability decreasing central motor plasticity is retained in multiple sclerosis patients. BMC Neurol 12:92. CrossRef Medline
64. Ziemann U, Siebner HR (2008) Modifying motor learning through gating and homeostatic metaplasticity. Brain Stimul 1:60-66. CrossRef Medline
65. zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60:162-169. CrossRef Medline