Bidirectional effects on interhemispheric resting-state functional connectivity induced by excitatory and inhibitory repetitive transcranial magnetic stimulation

Human Brain Mapping

Volumn 35, Issue 5, 2014, Pages 1896-1905

  Watanabe, Takamitsu ^a   Hanajima, Ritsuko ^b   Shirota, Yuichiro ^b,c   Ohminami, Shinya ^b   Tsutsumi, Ryosuke ^b   Terao, Yasuo ^b   Ugawa, Yoshikazu ^d,e   Hirose, Satoshi ^a   Miyashita, Yasushi ^a   Konishi, Seiki ^a   Kunimatsu, Akira ^a   Ohtomo, Kuni ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

FMRI; QPS; Rs fcMRI; RTMS; Transcallosal connection

Indexed keywords

ADULT; ARTICLE; ASSOCIATION CORTEX; CEREBELLUM; EVOKED MUSCLE RESPONSE; EXCITATORY REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INHIBITORY REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; INTERHEMISPHERIC TRANSFER; MALE; MIDDLE FRONTAL GYRUS; NERVE CELL EXCITABILITY; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PARIETAL CORTEX; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; QUADRIPULSE REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; RESTING STATE FUNCTIONAL CONNECTIVITY; SUPERIOR TEMPORAL GYRUS; TRANSCRANIAL MAGNETIC STIMULATION; BLOOD; BRAIN MAPPING; ELECTROMYOGRAPHY; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MOTOR CORTEX; PHYSIOLOGY; REST; VASCULARIZATION;

OXYGEN;

ADULT; BRAIN MAPPING; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MOTOR CORTEX; OXYGEN; REST; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84886697567     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22300     Document Type: Article

References (65)

1. Allen EA, Pasley BN, Duong T, Freeman RD (2007): Transcranial magnetic stimulation elicits coupled neural and hemodynamic consequences. Science 317:1918-1921.
2. Barker AT, Jalinous R, Freeston IL (1985): Non-invasive magnetic stimulation of human motor cortex. Lancet 1:1106-1107.
3. Beckmann CF, Deluca M, Devlin JT, Smith SM (2005): Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001-1013.
4. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
5. Biswal BB, Mennes M, Zuo X-N, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kotter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, Mcmahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SARB, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng GJ, Veijola J, Villringer A, Walter M, Wang L, Weng XC, Whitfield-Gabrieli S Williamson P, Windischberger C, Zang YF, Zhang HY, Castellanos FX, Milham MP (2010): Toward discovery science of human brain function. Proc Natl Acad Sci USA 107:4734-4739.
6. Chen W-H, Mima T, Siebner HR, Oga T, Hara H, Satow T, Begum T, Nagamine T, Shibasaki H (2003): Low-frequency rTMS over lateral premotor cortex induces lasting changes in regional activation and functional coupling of cortical motor areas. Clin Neurophysiol 114:1628-1637.
7. Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006):Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848-13853.
8. Drummond GB (2009): Reporting ethical matters in the Journal of Physiology: Standards and advice. J Physiol (Lond) 587:713-719.
9. Duann JR, Ide JS, Luo X, Li CSR (2009): Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. J Neurosci 29:10171-10179.
10. Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG (2005): Transcallosal inhibition in chronic subcortical stroke. NeuroImage 28:940-946.
11. 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 USA 108:21229-21234.
12. Fair DA, Schlaggar BL, Cohen AL, Miezin FM, Dosenbach NUF, Wenger KK, Fox MD, Snyder AZ, Raichle ME, Petersen SE (2007): A method for using blocked and event-related fMRI data to study "resting state" functional connectivity. NeuroImage 35:396-405.
13. Fox MD, Raichle ME (2007): Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711.
14. Fox MD, Snyder AZ, Vincent JL, Corbetta M, van Essen DC, Raichle ME (2005): The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673-9678.
15. Fox MD, Halko MA, Eldaief MC, Pascual-Leone A (2012): Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). NeuroImage 62:2232-2243.
16. Fuggetta G, Pavone EF, Fiaschi A, Manganotti P (2008): Acute modulation of cortical oscillatory activities during short trains of high-frequency repetitive transcranial magnetic stimulation of the human motor cortex: A combined EEG and TMS study. Hum Brain Mapp 29:1-13.
17. George MS, Lisanby SH, Sackeim HA (1999): Transcranial magnetic stimulation: Applications in neuropsychiatry. Arch Gen Psychiatry 56:300-311.
18. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Küst J, Karbe H, Fink GR (2008): Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann N Y Acad Sci 63:236-246.
19. 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.
20. Greicius MD, Krasnow B, Reiss AL, Menon V (2003): Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253-258.
21. Hamada M, Hanajima R, Terao Y, Arai N, Furubayashi T, Inomata-Terada S, Yugeta A, Matsumoto H, Shirota Y, Ugawa Y (2007): Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex. Clin Neurophysiol 118:2672-2682.
22. Hamada M, Terao Y, Hanajima R, Shirota Y, Nakatani-Enomoto S, Furubayashi T, Matsumoto H, Ugawa Y (2008): Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J Physiol (Lond) 586:3927-3947.
23. Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, Furubayashi T, Shiio Y, Uesugi H, Kanazawa I (2001): Interhemispheric facilitation of the hand motor area in humans. J Physiol (Lond) 531:849-859.
24. Honey CJ, Kötter R, Breakspear M, Sporns O (2007): Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA 104:10240-10245.
25. Horacek J, Brunovsky M, Novak T, Skrdlantova L, Klirova M, Bubenikova-Valesova V, Krajca V, Tislerova B, Kopecek M, Spaniel F, Mohr P, Höschl C (2007): Effect of low-frequency rTMS on electromagnetic tomography (LORETA) and regional brain metabolism (PET) in schizophrenia patients with auditory hallucinations. Neuropsychobiology 55:132-142.
26. Kanai R, Dong MY, Bahrami B, Rees G (2011): Distractibility in daily life is reflected in the structure and function of human parietal cortex. J Neurosci 31:6620-6626.
27. Kilpatrick LA, Zald DH, Pardo JV, Cahill LF (2006): Sex-related differences in amygdala functional connectivity during resting conditions. NeuroImage 30:452-461.
28. Koyama MS, Di Martino A, Zuo X-N, Kelly C, Mennes M, Jutagir DR, Castellanos FX, Milham MP (2011): Resting-state functional connectivity indexes reading competence in children and adults. J Neurosci 31:8617-8624.
29. Lee L, Siebner HR, Rowe JB, Rizzo V, Rothwell JC, Frackowiak RSJ, Friston KJ (2003): Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23:5308-5318.
30. Merton PA, Morton HB (1980): Stimulation of the cerebral cortex in the intact human subject. Nature 285:227.
31. Meyer-Lindenberg A (2010): From maps to mechanisms through neuroimaging of schizophrenia. Nature 468:194-202.
32. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR, Berman KF (2005): Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch Gen Psychiatry 62:379-386.
33. Moisa M, Pohmann R, Uludag K, Thielscher A (2010): Interleaved TMS/CASL: Comparison of different rTMS protocols. NeuroImage 49:612-620.
34. Murase N, Duque J, Mazzocchio R, Cohen LG (2004): Influence of interhemispheric interactions on motor function in chronic stroke. Ann N Y Acad Sci 55:400-409.
35. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009): The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? NeuroImage 44:893-905.
36. O'shea J, Johansen-Berg H, Trief D, Göbel S, Rushworth MFS (2007): Functionally specific reorganization in human premotor cortex. Neuron 54:479-490.
37. Oliviero A, Strens LHA, Di Lazzaro V, Tonali PA, Brown P (2003): Persistent effects of high frequency repetitive TMS on the coupling between motor areas in the human. Exp Brain Res 149:107-113.
38. Orosz A, Jann K, Wirth M, Wiest R, Dierks T, Federspiel A (2012): Theta burst TMS increases cerebral blood flow in the primary motor cortex during motor performance as assessed by arterial spin labeling (ASL). NeuroImage 61:599-605.
39. Parks NA, Maclin EL, Low KA, Beck DM, Fabiani M, Gratton G (2012): Examining cortical dynamics and connectivity with simultaneous single-pulse transcranial magnetic stimulation and fast optical imaging. NeuroImage 59:2504-2510.
40. Pascual-Leone A, Walsh V, Rothwell J (2000): Transcranial magnetic stimulation in cognitive neuroscience-Virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 10:232-237.
41. Paus T, Castro-Alamancos MA, Petrides M (2001): Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation. Eur J Neurosci 14:1405-1411.
42. Post RM, Kimbrell TA, Mccann UD, Dunn RT, Osuch EA, Speer AM, Weiss SR (1999): Repetitive transcranial magnetic stimulation as a neuropsychiatric tool: Present status and future potential. J Ect 15:39-59.
43. Pridmore S, Belmaker R (1999): Transcranial magnetic stimulation in the treatment of psychiatric disorders. Psychiatry Clin Neurosci 53:541-548.
44. Romei V, Driver J, Schyns PG, Thut G (2011): Rhythmic TMS over parietal cortex links distinct brain frequencies to global versus local visual processing. Curr Biol 21:334-337.
45. Shirota Y, Hamada M, Terao Y, Matsumoto H, Ohminami S, Furubayashi T, Nakatani-Enomoto S, Ugawa Y, Hanajima R (2010): Influence of short-interval intracortical inhibition on short-interval intracortical facilitation in human primary motor cortex. J Neurophysiol 104:1382-1391.
46. Siebner HR, Filipovic SR, Rowe JB, Cordivari C, Gerschlager W, Rothwell JC, Frackowiak RSJ, Bhatia KP (2003): Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126:2710-2725.
47. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009): Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040-13045.
48. Sparing R, Buelte D, Meister IG, Pauš T, Fink GR (2008): Transcranial magnetic stimulation and the challenge of coil placement: A comparison of conventional and stereotaxic neuronavigational strategies. Hum Brain Mapp 29:82-96.
49. Speer AM, Kimbrell TA, Wassermann EM, Repella JD, Willis MW, Herscovitch P, Post RM (2000): Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry 48:1133-1141.
50. Stark DE, Margulies DS, Shehzad ZE, Reiss P, Kelly AMC, Uddin LQ, Gee DG, Roy AK, Banich MT, Castellanos FX, Milham MP (2008). Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. J Neurosci 28:13754-13764.
51. Strafella AP, Paus T (2001): Cerebral blood-flow changes induced by paired-pulse transcranial magnetic stimulation of the primary motor cortex. J Neurophysiol 85:2624-2629.
52. Strens LHA, Oliviero A, Bloem BR, Gerschlager W, Rothwell JC, Brown P (2002): The effects of subthreshold 1 Hz repetitive TMS on cortico-cortical and interhemispheric coherence. Clin Neurophysiol 113:1279-1285.
53. Tian L, Ren J, Zang Y (2012): Regional homogeneity of resting state fMRI signals predicts stop signal task performance. NeuroImage 60:539-544.
54. Toro R, Fox PT, Pauš T (2008): Functional coactivation map of the human brain. Cereb Cortex 18:2553-2559.
55. Valero-Cabre A, Payne BR, Pascual-Leone A (2007): Opposite impact on 14C-2-deoxyglucose brain metabolism following patterns of high and low frequency repetitive transcranial magnetic stimulation in the posterior parietal cortex. Exp Brain Res 176:603-615.
56. van der Werf YD, Sanz-Arigita EJ, Menning S, van den Heuvel OA (2010): Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation. BMC Neurosci 11:145.
57. van Dijk KRA, Hedden T, Venkataraman A, Evans KC, Lazar SW, Buckner RL (2010): Intrinsic functional connectivity as a tool for human connectomics: Theory, properties, and optimization. J Neurophysiol 103:297-321.
58. van Kesteren MTR, Fernández G, Norris DG, Hermans EJ (2010): Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci USA 107:7550-7555.
59. van Schouwenburg MR, O'shea J, Mars RB, Rushworth MFS, Cools R (2012): Controlling human striatal cognitive function via the frontal cortex. J Neurosci 32:5631-5637.
60. Vercammen A, Knegtering H, Liemburg EJ, Boer den 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.
61. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006): Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517-3531.
62. 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.
63. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, Mccarley RW, Shenton ME, Green AI, Nieto-Castanon A, Laviolette P, Wojcik J, Gabrieli JDE, Seidman LJ (2009): Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci USA 106:1279-1284.
64. Zaretskaya N, Thielscher A, Logothetis NK, Bartels A (2010). Disrupting parietal function prolongs dominance durations in binocular rivalry. Curr Biol 20:2106-2111.
65. Zuo XN, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP (2010): Reliable intrinsic connectivity networks: Test-retest evaluation using ICA and dual regression approach. NeuroImage 49:2163-2177.