Mechanisms of human motor cortex facilitation induced by subthreshold 5-Hz repetitive transcranial magnetic stimulation

Journal of Neurophysiology

Volumn 109, Issue 12, 2013, Pages 3060-3066

  Sommer, Martin ^a   Rummel, Milena ^a   Norden, Christoph ^a   Rothkegel, Holger ^a,b   Lang, Nicolas ^a,b   Paulus, Walter ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Carbamazepine; Dextrometorphan; Lorazepam; Plasticity; Transcranial magnetic stimulation

Indexed keywords

CARBAMAZEPINE; DEXTROMETHORPHAN; LORAZEPAM; PLACEBO; SODIUM CHANNEL;

ABDUCTOR DIGITI MINIMI MUSCLE; ADULT; AMPLITUDE MODULATION; ARTICLE; CONDITIONING; EVOKED MUSCLE RESPONSE; EXTENSOR CARPI RADIALIS MUSCLE; FEMALE; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; LONG TERM POTENTIATION; MALE; MOLECULAR MECHANICS; MOTOR CORTEX; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NORMAL HUMAN; PERCEPTIVE THRESHOLD; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; SKELETAL MUSCLE; TRANSCRANIAL MAGNETIC STIMULATION;

CARBAMAZEPINE; DEXTROMETORPHAN; LORAZEPAM; PLASTICITY; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; CARBAMAZEPINE; EVOKED POTENTIALS, MOTOR; FEMALE; GABA MODULATORS; HUMANS; LONG-TERM POTENTIATION; LORAZEPAM; MALE; MOTOR CORTEX; MUSCLE, SKELETAL; PIRENZEPINE; REACTION TIME; RECEPTORS, N-METHYL-D-ASPARTATE; SENSORY THRESHOLDS; SODIUM CHANNEL BLOCKERS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84879136618     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01089.2012     Document Type: Article

References (60)

1. Beck S, Hallett M. Surround inhibition is modulated by task difficulty. Clin Neurophysiol 121: 98-103, 2010.
2. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci 19: 1950-1962, 2004.
3. Brown MW, Rose D, Ahlquist J. Amnesia-producing drugs affect hippocam-pal frequency potentiation. Neuroscience 10: 697-706, 1983.
4. Citri A, Malenka RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33: 18-41, 2008.
5. Conca A, Swoboda E, Konig P, Koppi S, Beraus W, Kunz A, Fritzsche H, Weiss P. Clinical impacts of single transcranial magnetic stimulation (sTMS) as an add-on therapy in severely depressed patients under SSRI treatment. Hum Psychopharmacol 15: 429-438, 2000.
6. Cruccu G, Leandri M, Iannetti GD, Mascia A, Romaniello A, Truini A, Galeotti F, Manfredi M. Small-fiber dysfunction in trigeminal neuralgia: carbamazepine effect on laser-evoked potentials. Neurology 56: 1722-1726, 2001.
7. Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, Insola A, Tonali PA, Rothwell JC. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115: 255-266, 2004.
8. Fitzgerald PB, Benitez J, Oxley T, Daskalakis JZ, de Castella AR, Kulkarni J. A study of the effects of lorazepam and dextromethorphan on the response to cortical 1 Hz repetitive transcranial magnetic stimulation. Neuroreport 16: 1525-1528, 2005.
9. Fox PT, Narayana S, Tandon N, Sandoval H, Fox SP, Kochunov P, Lancaster JL. Column-based model of electric field excitation of cerebral cortex. Hum Brain Mapp 22: 1-14, 2004.
10. Geradin AP, Abadie FV, Campestrini JA, Theobald W. Pharmacokinetics of carbamazepine in normal humans after single and repeated oral doses. J Pharmacokinet Biopharm 4: 521-535, 1976.
11. Greenblatt DJ, Shader RI, Franke K, MacLaughlin DS, Harmatz JS, Allen MD, Werner A, Woo E. Pharmacokinetics and bioavailability of intravenous, intramuscular, and oral lorazepam in humans. J Pharm Sci 68: 57-63, 1979.
12. Habets RL, Borst JG. An increase in calcium influx contributes to post-tetanic potentiation at the rat calyx of Held synapse. J Neurophysiol 96: 2868-2876, 2006.
13. Habets RL, Borst JG. Post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 564: 173-187, 2005.
14. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 45: 201-206, 2005.
15. Inghilleri M, Conte A, Frasca V, Curra A, Gilio F, Manfredi M, Berardelli A. Antiepileptic drugs and cortical excitability: a study with repetitive transcranial stimulation. Exp Brain Res 154: 488-493, 2004.
16. Jacobs KM, Donoghue JP. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251: 944-947, 1991.
17. Janicak PG, Nahas Z, Lisanby SH, Solvason HB, Sampson SM, McDonald WM, Marangell LB, Rosenquist P, McCall WV, Kimball J, O'Reardon JP, Loo C, Husain MH, Krystal A, Gilmer W, Dowd SM, Demitrack MA, Schatzberg AF. Durability of clinical benefit with transcranial magnetic stimulation (TMS) in the treatment of pharmacoresistant major depression: assessment of relapse during a 6-mo, multisite, open-label study. Brain Stimul 3: 187-199, 2010.
18. Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H. Motor threshold in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol 112: 250-258, 2001.
19. Kirkwood A, Dudek SM, Gold JT, Aizenman CD, Bear MF. Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 260: 1518-1521, 1993.
20. Lazar RM, Fitzsimmons BF, Marshall RS, Mohr JP, Berman MF. Mida-zolam challenge reinduces neurological deficits after transient ischemic attack. Stroke 34: 794-796, 2003.
21. Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125: 2238-2247, 2002.
22. Maccabee PJ, Nagaranjan SS, Amassian VE, Durand DM, Szabo AZ, Ahad AB, Cracco RQ, Lai KS, Eberle LP. Influence of pulse sequence, polarity and amplitude on magnetic stimulation of human and porcine periheral nerve. J Physiol 513: 571-585, 1998.
23. Melkerson MN. Food and Drug administration regulation on NeuroStar TMS Therapy System Food and Drug Administration (Online). http://www.accessdata.fda.gov/cdrh_docs/pdf8/K083538.pdf [8 Nov. 2009].
24. Netzer R, Pflimlin P, Trube G. Dextromethorphan blocks N-methyl-D-aspartate-induced currents and voltage-operated inward currents in cultured cortical neurons. Eur J Pharmacol 238: 209-216, 1993.
25. Nitsche MA, Fricke K, Henschke U, Schlitterlau A, Liebetanz D, Lang N, Henning S, Tergau F, Paulus W. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553: 293-301, 2003.
26. Nitsche MA, Liebetanz D, Schlitterlau A, Henschke U, Fricke K, From-mann K, Lang N, Henning S, Paulus W, Tergau F. GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur J Neurosci 19: 2720-2726, 2004.
27. O'Reardon JP, Solvason HB, Janicak PG, Sampson S, Isenberg KE, Nahas Z, McDonald WM, Avery D, Fitzgerald PB, Loo C, Demitrack MA, George MS, Sackeim HA. Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 62: 1208-1216, 2007.
28. Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117: 847-858, 1994.
29. Pasley BN, Allen EA, Freeman RD. State-dependent variability of neuronal responses to transcranial magnetic stimulation of the visual cortex. Neuron 62: 291-303, 2009.
30. Pell GS, Roth Y, Zangen A. Modulation of cortical excitability induced by repetitive transcranial magnetic stimulation: influence of timing and geometrical parameters and underlying mechanisms. Prog Neurobiol 93: 59-98, 2011.
31. Quartarone A, Bagnato S, Rizzo V, Morgante F, Sant'Angelo A, Battaglia F, Messina C, Siebner HR, Girlanda P. Distinct changes in cortical and spinal excitability following high-frequency repetitive TMS to the human motor cortex. Exp Brain Res 161: 114-124, 2005.
32. Ridding MC, Ziemann U. Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588: 2291-2304, 2010.
33. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120: 2008- 2039, 2009.
34. Rothkegel H, Sommer M, Paulus W. Breaks during 5 Hz rTMS are essential for facilitatory after effects. Clin Neurophysiol 121: 426-430, 2010.
35. Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W. Magnetic stimulation: motor evoked potentials. In: Recommendations for the Practice of Clinical Neurophysiology: Guidelines of the International Federation of Clinical Neurophysiology, edited by Deuschl G, and Eisen A. Amsterdam: Elsevier Science, 1999, p. 97-103.
36. Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD. Stimulation of the human motor cortex through the scalp. Exp Physiol 76: 159-200, 1991.
37. Salvador R, Silva S, Basser PJ, Miranda PC. Determining which mechanisms lead to activation in the motor cortex: a modeling study of transcranial magnetic stimulation using realistic stimulus waveforms and sulcal geometry. Clin Neurophysiol 122: 748-758, 2011.
38. Samii A, Chen R, Wassermann EM, Hallett M. Phenytoin does not influence postexercise facilitation of motor evoked potentials. Neurology 50: 291-293, 1998.
39. Samii A, Wassermann EM, Ikoma K, Mercuri B, Hallett M. Characterization of postexercise facilitation and depression of motor evoked potentials to transcranial magnetic stimulation. Neurology 46: 1376-1382, 1996.
40. Schulz PE, Fitzgibbons JC. Differing mechanisms of expression for short-and long-term potentiation. J Neurophysiol 78: 321-334, 1997.
41. Silvasti M, Karttunen P, Tukiainen H, Kokkonen P, Hanninen U, Ny-kanen S. Pharmacokinetics of dextromethorphan and dextrorphan: a single dose comparison of three preparations in human volunteers. Int J Clin Pharmacol Ther Toxicol 25: 493-497, 1987.
42. Sommer M, Alfaro A, Rummel M, Speck S, Lang N, Tings T, Paulus W. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin Neurophysiol 117: 838-844, 2006.
43. Sommer M, Norden C, Schmack L, Rothkegel H, Lang N, Paulus W. Opposite optimal current flow directions for induction of neuroplasticity and excitation threshold in the human motor cortex. Brain Stimul 6: 363-370, 2013.
44. Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J. Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543: 699-708, 2002.
45. Swandulla D, Hans M, Zipser K, Augustine GJ. Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signaling in nerve terminals. Neuron 7: 915-926, 1991.
46. Talwar D. Mechanisms of antiepileptic drug action. Pediatr Neurol 6: 289-295, 1990.
47. Tegenthoff M, Ragert P, Pleger B, Schwenkreis P, Forster AF, Nicolas V, Dinse HR. Improvement of tactile discrimination performance and enlargement of cortical somatosensory maps after 5 Hz rTMS. PLoS Biol 3: e362, 2005.
48. Teo JT, Terranova C, Swayne O, Greenwood RJ, Rothwell JC. Differing effects of intracortical circuits on plasticity. Exp Brain Res 193: 555-563, 2009.
49. Tings T, Lang N, Tergau F, Paulus W, Sommer M. Orientation-specific fast rTMS maximizes corticospinal inhibition and facilitation. Exp Brain Res 124: 323-333, 2005.
50. Treiman DM. GABAergic mechanisms in epilepsy. Epilepsia 42: 8-12, 2001.
51. Valls-Solé J, Hallett M. On technical features of neurophysiological equipment and their reliability. Clin Neurophysiol 117: 714-715, 2006.
52. Wan H, Warburton EC, Zhu XO, Koder TJ, Park Y, Aggleton JP, Cho K, Bashir ZI, Brown MW. Benzodiazepine impairment of perirhinal cortical plasticity and recognition memory. Eur J Neurosci 20: 2214-2224, 2004.
53. Werhahn KJ, Mortensen J, Kaelin-Lang A, Boroojerdi B, Cohen LG. Cortical excitability changes induced by deafferentation of the contralateral hemisphere. Brain 125: 1402-1413, 2002.
54. White HS. Clinical significance of animal seizure models and mechanism of action studies of potential antiepileptic drugs. Epilepsia 38: S9-S17, 1997.
55. Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J. A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol 89: 2339-2345, 2003.
56. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology 51: 1320-1324, 1998a.
57. Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18: 7000-7007, 1998b.
58. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109: 127-135, 1996a.
59. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40: 367-378, 1996b.
60. Ziemann U, Muellbacher W, Hallett M, Cohen LG. Modulation of practice-dependent plasticity in human motor cortex. Brain 124: 1171-1181, 2001.