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Published in: Experimental Brain Research 1/2005

01-02-2005 | Research Article

Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura

Authors: Filippo Brighina, Giuseppe Giglia, Simona Scalia, Margherita Francolini, Antonio Palermo, Brigida Fierro

Published in: Experimental Brain Research | Issue 1/2005

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Abstract

We previously showed paradoxical facilitatory effects of low-frequency repetitive transcranial magnetic stimulation (rTMS) on striate and extrastriate cortex of patients suffering migraine with aura. In this study we evaluated the effects of 1 Hz rTMS on the excitability of inhibitory and facilitatory circuits of motor cortex to explore whether the abnormal pattern of excitability extends beyond the sensory cortex also involving motor areas in migraine with aura. Nine patients affected by migraine with aura and eight healthy controls entered into the study. The hot spot for activation of the right abductor pollicis brevis (APB) was checked by means of a figure-of-eight coil and motor threshold (MT) recorded on this point. Nine hundred magnetic stimuli at 1 Hz frequency and 90% MT intensity were delivered at the hot spot. Before and after rTMS, intracortical inhibitory and facilitatory circuit excitability was assessed by means of a paired pulse paradigm (conditioning stimulus 80% MT and test stimulus 120% MT) with two different interstimulus intervals: 2 ms (inhibitory) and 10 ms (facilitatory). Amplitude of the responses was expressed as the percentage of motor evoked potential (MEP) to test stimulus alone. Results showed that in basal condition migraineurs present significantly reduced levels of intracortical inhibition (ICI) compared to controls. More importantly, opposite results were obtained in migraineurs with respect to controls when 1 Hz rTMS was applied. Specifically, whereas intracortical facilitation (ICF) significantly decreased in controls, it significantly increased in migraineurs. ICI levels were not significantly affected by low-frequency stimulation. Our results showed that motor as well as sensory cortex of migraine patients present an abnormal modulation of cortical excitability, where a relevant role is likely played by the inefficiency of inhibitory circuits.
Literature
go back to reference Afra J, Mascia A, Gèrard P, Maertens de Noordhout A, Schoenen J (1998) Interictal cortical excitability in migraine: a study using transcranial magnetic stimulation of motor and visual cortices. Ann Neurol 44:209–215 Afra J, Mascia A, Gèrard P, Maertens de Noordhout A, Schoenen J (1998) Interictal cortical excitability in migraine: a study using transcranial magnetic stimulation of motor and visual cortices. Ann Neurol 44:209–215
go back to reference Aurora SK, Ahmad BK, Welch KMA, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms the hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114 Aurora SK, Ahmad BK, Welch KMA, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms the hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114
go back to reference Aurora SK, al-Sayeed F, Welch KM (1999) The cortical silent period is shortened in migraine with aura. Cephalalgia 19:708–712CrossRefPubMed Aurora SK, al-Sayeed F, Welch KM (1999) The cortical silent period is shortened in migraine with aura. Cephalalgia 19:708–712CrossRefPubMed
go back to reference Boroojerdi B, Prager A., Muellbacher W, Cohen LG (2000) Reduction of human visual cortical excitability using low transcranial magnetic stimulation. Neurology 54:1529–1531PubMed Boroojerdi B, Prager A., Muellbacher W, Cohen LG (2000) Reduction of human visual cortical excitability using low transcranial magnetic stimulation. Neurology 54:1529–1531PubMed
go back to reference Brighina F, Piazza A, Daniele O, Fierro B (2002) Modulation of visual cortex excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp Brain Res 145:177–181CrossRefPubMed Brighina F, Piazza A, Daniele O, Fierro B (2002) Modulation of visual cortex excitability in migraine with aura: effects of 1 Hz repetitive transcranial magnetic stimulation. Exp Brain Res 145:177–181CrossRefPubMed
go back to reference Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMed Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMed
go back to reference Di Lazzaro V, Restuccia D, Olivero A, Proficue P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 119:265–268CrossRefPubMed Di Lazzaro V, Restuccia D, Olivero A, Proficue P, Ferrara L, Insola A, Mazzone P, Tonali P, Rothwell JC (1998) Magnetic transcranial stimulation at intensities below active motor threshold activates intracortical inhibitory circuits. Exp Brain Res 119:265–268CrossRefPubMed
go back to reference Fierro B, Ricci R, Piazza A, Scalia S, Giglia G, Vitello G, Brighina F (2003) 1 Hz rTMS enhances extrastriate cortex activity in migraine. Evidence of reduced inhibition? Neurology 61:1446–1448PubMed Fierro B, Ricci R, Piazza A, Scalia S, Giglia G, Vitello G, Brighina F (2003) 1 Hz rTMS enhances extrastriate cortex activity in migraine. Evidence of reduced inhibition? Neurology 61:1446–1448PubMed
go back to reference Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J (2002) Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol 113:1136–1141CrossRefPubMed Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J (2002) Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol 113:1136–1141CrossRefPubMed
go back to reference Headache Classification Subcommittee of the International Headache Society (2004) The International Classification of Headache Disorders, 2nd edn. Cephalalgia 24 [Suppl 1]:9–160 Headache Classification Subcommittee of the International Headache Society (2004) The International Classification of Headache Disorders, 2nd edn. Cephalalgia 24 [Suppl 1]:9–160
go back to reference Hess G, Donoghue JP (1994) Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J Neurophysiol 71:2543–2547PubMed Hess G, Donoghue JP (1994) Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J Neurophysiol 71:2543–2547PubMed
go back to reference 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 471:501–519PubMed 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 471:501–519PubMed
go back to reference Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133:425–430CrossRefPubMed Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133:425–430CrossRefPubMed
go back to reference McCormick DA (1989) GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62:1018–1027PubMed McCormick DA (1989) GABA as an inhibitory neurotransmitter in human cerebral cortex. J Neurophysiol 62:1018–1027PubMed
go back to reference Maertens de Noordhout A, Pepin JL, Schoenen J, Delwaide PJ (1992) Percutaneous magnetic stimulation of the motor cortex in migraine. Electroencephalogr Clin Neurophysiol 85:110–115CrossRefPubMed Maertens de Noordhout A, Pepin JL, Schoenen J, Delwaide PJ (1992) Percutaneous magnetic stimulation of the motor cortex in migraine. Electroencephalogr Clin Neurophysiol 85:110–115CrossRefPubMed
go back to reference Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001a) Visual cortex excitability in migraine with and without aura. Headache 41:565–572CrossRefPubMed Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001a) Visual cortex excitability in migraine with and without aura. Headache 41:565–572CrossRefPubMed
go back to reference Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001b) Suppression of perception in migraine: evidence for reduced inhibition in visual cortex. Neurology 56:178–183PubMed Mulleners WM, Chronicle EP, Palmer JE, Koehler PJ, Vredeveld JW (2001b) Suppression of perception in migraine: evidence for reduced inhibition in visual cortex. Neurology 56:178–183PubMed
go back to reference Palmer JE, Chronicle EP, Rolan P, Mulleners WM (2000) Cortical hyperexcitability is cortical under-inhibition: evidence from a novel functional test of migraine patients. Cephalalgia 20:525–532CrossRefPubMed Palmer JE, Chronicle EP, Rolan P, Mulleners WM (2000) Cortical hyperexcitability is cortical under-inhibition: evidence from a novel functional test of migraine patients. Cephalalgia 20:525–532CrossRefPubMed
go back to reference Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847–858PubMed Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847–858PubMed
go back to reference Romero JR, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol 113:101–107CrossRefPubMed Romero JR, Anschel D, Sparing R, Gangitano M, Pascual-Leone A (2002) Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex. Clin Neurophysiol 113:101–107CrossRefPubMed
go back to reference Rothwell JC (1996) The use of paired pulse stimulation to investigate the intrinsic circuitry of human motor cortex. In: Nilsson J, Panizza M, Grandori F (eds) Advances in magnetic stimulation. Mathematical modeling and clinical applications. Fondazione Salvatore Maugeri, Pavia, Italy, pp 99–104 Rothwell JC (1996) The use of paired pulse stimulation to investigate the intrinsic circuitry of human motor cortex. In: Nilsson J, Panizza M, Grandori F (eds) Advances in magnetic stimulation. Mathematical modeling and clinical applications. Fondazione Salvatore Maugeri, Pavia, Italy, pp 99–104
go back to reference Schwenkreis P, Liepert J, Witscher K, Fischer W, Weiller C, Malin JP, Tegenthoff M (2000) Riluzole suppresses motor cortex facilitation in correlation to its plasma level. A study using transcranial magnetic stimulation. Exp Brain Res 135:293–299CrossRefPubMed Schwenkreis P, Liepert J, Witscher K, Fischer W, Weiller C, Malin JP, Tegenthoff M (2000) Riluzole suppresses motor cortex facilitation in correlation to its plasma level. A study using transcranial magnetic stimulation. Exp Brain Res 135:293–299CrossRefPubMed
go back to reference Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A (1999) Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 52:529–537PubMed Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A (1999) Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 52:529–537PubMed
go back to reference Siebner HR, Mentschel C, Auer C, Lehner C, Conrad B (2000). Repetitive transcranial magnetic stimulation causes a short-term increase in the duration of the cortical silent period in patients with Parkinson’s disease. Neurosci Lett 284:147–150CrossRefPubMed Siebner HR, Mentschel C, Auer C, Lehner C, Conrad B (2000). Repetitive transcranial magnetic stimulation causes a short-term increase in the duration of the cortical silent period in patients with Parkinson’s disease. Neurosci Lett 284:147–150CrossRefPubMed
go back to reference Touge T, Gerschlager W, Brown P, Rothwell JC (2001) Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 112:2138–2145CrossRefPubMed Touge T, Gerschlager W, Brown P, Rothwell JC (2001) Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 112:2138–2145CrossRefPubMed
go back to reference van der Kamp W, Maassen Van Den Brink A, Ferrari MD, van Dijk JG (1996) Interictal cortical hyperexcitability in migraine patients demonstrated with transcranial magnetic stimulation. J Neurol Sci139:106–110 van der Kamp W, Maassen Van Den Brink A, Ferrari MD, van Dijk JG (1996) Interictal cortical hyperexcitability in migraine patients demonstrated with transcranial magnetic stimulation. J Neurol Sci139:106–110
go back to reference van der Kamp W, Maassen Van Den Brink A, Ferrari MD, van Dijk JG (1997) Interictal cortical excitability to magnetic stimulation in familial hemiplegic migraine. Neurology 48:1462–1464PubMed van der Kamp W, Maassen Van Den Brink A, Ferrari MD, van Dijk JG (1997) Interictal cortical excitability to magnetic stimulation in familial hemiplegic migraine. Neurology 48:1462–1464PubMed
go back to reference Ziemann U (1999) Intracortical inhibition and facilitation in the conventional paired TMS paradigm. Electroencephalogr Clin Neurophysiol 51 [Suppl]:127–136 Ziemann U (1999) Intracortical inhibition and facilitation in the conventional paired TMS paradigm. Electroencephalogr Clin Neurophysiol 51 [Suppl]:127–136
go back to reference Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123PubMed Ziemann U, Corwell B, Cohen LG (1998) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123PubMed
go back to reference Ziemann U, Lonnecker S, Paulus W (1995) Inhibition of human motor cortex by ethanol. A transcranial magnetic stimulation study. Brain 118:1437–1446PubMed Ziemann U, Lonnecker S, Paulus W (1995) Inhibition of human motor cortex by ethanol. A transcranial magnetic stimulation study. Brain 118:1437–1446PubMed
go back to reference Ziemann U, Rothwell JC, Ridding MC (1996) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496:873–881PubMed Ziemann U, Rothwell JC, Ridding MC (1996) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496:873–881PubMed
Metadata
Title
Facilitatory effects of 1 Hz rTMS in motor cortex of patients affected by migraine with aura
Authors
Filippo Brighina
Giuseppe Giglia
Simona Scalia
Margherita Francolini
Antonio Palermo
Brigida Fierro
Publication date
01-02-2005
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2005
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-004-2042-7

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