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Subcortical Hyperexcitability in Migraineurs: A High-Frequency Oscillation Study

Published online by Cambridge University Press:  02 December 2014

Kuan-Lin Lai
Affiliation:
Department of Neurology, Taipei Municipal Gandau Hospital Department of Neurology, Neurological Institute, Taipei Veterans General Hospital Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan
Kwong-Kum Liao
Affiliation:
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan
Jong-Ling Fuh
Affiliation:
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan
Shuu-Jiun Wang*
Affiliation:
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan
*
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital, No. 201, Shih-Pai Road, Section 2, Taipei, Taiwan, 112
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Abstract

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Objective:

An abnormal central nervous system excitability level was found in patients with migraine. Whether it is hyper- or hypo-excitable is still debated. This study aimed to compare the somatosensory high-frequency oscillations (HFOs), which reflected subcortical excitability (early phase) and intracortical inhibition (late phase), between patients with migraine and control subjects.

Methods:

HFOs were recorded from C3'-Fz, using a 500-1000 Hz frequency filter after stimulation at right median nerves at the wrists, and divided into early and late phases based on the N20 peak. Fifty-nine untreated patients (n=24 during ictal period; n=35, interictal) and 22 controls finished the study.

Results:

In early HFOs, patients both during ictal and interictal periods had higher maximal amplitudes (p =0.039) and area-under-curve (p =0.029) than those of the controls. Regarding the late HFOs, there were no significant differences among these groups.

Conclusion:

Our study suggests a hyper-excitable state in the subcortical regions in patients with migraine both during interictal and ictal periods.

Type
Original Article
Copyright
Copyright © The Canadian Journal of Neurological 2011

References

1Pietrobon, D, Striessnig, J.Neurobiology of migraine. Nat Rev Neurosci. 2003;4(5):38698.Google Scholar
2Somjen, GG.Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev. 2001;81(3):106596.Google Scholar
3Welch, KM, Barkley, GL, Tepley, N, et al.Central neurogenic mechanisms of migraine. Neurology. 1993;43(S3):S215.Google ScholarPubMed
4de Tommaso, M, Sciruicchio, V, Tota, P, et al.Somatosensory evoked potentials in migraine. Funct Neurol. 1997;12(2):7782.Google Scholar
5Firenze, C, Gatto, FD, Mazzotta, G, et al.Somatosensory-evoked potential study in headache patients. Cephalalgia. 1988;8(3): 15762.Google Scholar
6Afra, J, Cecchini, A, De Pasqua, V, et al.Visual evoked potentials during long periods of pattern-reversal stimulation in migraine. Brain. 1998;121(2):23341.Google Scholar
7Connolly, JF, Gawel, M, Rose, FC.Migraine patients exhibit abnormalities in the visual evoked potential. J Neurol Neurosurg Psychiatry. 1982;45(5):4647.Google Scholar
8Aurora, SK, Ahmad, BK, Welch, KM, et al.Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology. 1998;50(4):11114.Google Scholar
9Khedr, EM, Ahmed, MA, Mohamed, KA.Motor and visual cortical excitability in migraineurs patients with or without aura: transcranial magnetic stimulation. Neurophysiol Clin. 2006;36(1):138.CrossRefGoogle ScholarPubMed
10Goadsby, PJ.Recent advances in understanding migraine mechanisms, molecules and therapeutics. Trends Mol Med. 2007;13(1):3944.Google Scholar
11Dodick, D, Silberstein, S.Central sensitization theory of migraine: clinical implications. Headache. 2006;46(S4):S18291.CrossRefGoogle ScholarPubMed
12Haas, DC, Kent, PF, Friedman, DI.Headache caused by a single lesion of multiple sclerosis in the periaqueductal gray area. Headache. 1993;33(8):4525.Google Scholar
13Goadsby, P.Neurovascular headache and a midbrain vascular malformation: evidence for a role of the brainstem in chronic migraine. Cephalalgia. 2002;22(2):10711.Google Scholar
14Cracco, RQ, Cracco, JB.Somatosensory evoked potential in man: far field potentials. Electroencephalogr Clin Neurophysiol. 1976;41(5):4606.Google Scholar
15Nakano, S, Hashimoto, I.Comparison of somatosensory evoked high-frequency oscillations after posterior tibial and median nerve stimulation. Clin Neurophysiol. 1999;110(11):194852.Google Scholar
16Yamada, T, Kameyama, S, Fuchigami, Y, et al.Changes of short latency somatosensory evoked potential in sleep. Electroencephalogr Clin Neurophysiol. 1988;70(2):12636.CrossRefGoogle ScholarPubMed
17Gobbel’, R, Buchner, H, Curio, G.High-frequency (600 Hz) SEP activities originating in the subcortical and cortical human somatosensory system. Electroencephalogr Clin Neurophysiol. 1998;108(2):1829.Google Scholar
18Gobbel’, R, Buchner, H, Scherg, M, et al.Stability of high-frequency (600 Hz) components in human somatosensory evoked potentials under variation of stimulus rate-evidence for a thalamic origin. Clin Neurophysiol. 1999;110(9):165963.Google Scholar
19Gobbel’, R, Waberski, TD, Simon, H, et al.Different origins of low-and high-frequency components (600 Hz) of human somatosensory evoked potentials. Clin Neurophysiol. 2004;115(4):92737.Google Scholar
20Hashimoto, I, Mashiko, T, Imada, T.Somatic evoked high-frequency magnetic oscillations reflect activity of inhibitory interneurons in the human somatosensory cortex. Electroencephalogr Clin Neurophysiol. 1996;100(3):189203.Google Scholar
21Ozaki, I, Hashimoto, I.Neural mechanisms of the ultrafast activities. Clin EEG Neurosci. 2005;36(4):2717.Google Scholar
22Restuccia, D, Della Marca, G, Valeriani, M, et al.Influence of cholinergic circuitries in generation of high-frequency somatosensory evoked potentials. Clin Neurophysiol. 2003;114(8):153848.CrossRefGoogle ScholarPubMed
23Sakuma, K, Takeshima, T, Ishizaki, K, Nakashima, K.Somatosensory evoked high-frequency oscillations in migraine patients. Clin Neurophysiol. 2004;115(8):185762.Google Scholar
24Coppola, G, Vandenheede, M, Di Clemente, L, et al.Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. Brain. 2005;128(1):98103.Google Scholar
25Headache classification subcommittee of the international headache society. The international classification of headache disorders: 2nd ed. Cephalalgia. 2004;24(S1):S9160.Google Scholar
26Emerson, RG, Sgro, JA, Pedley, TA, et al.State-dependent changes in the N20 component of the median nerve somatosensory evoked potential. Neurology. 1988;38(1):648.Google Scholar
27Urasaki, E, Genmoto, T, Yokota, A, et al.Effects of general anesthesia on high-frequency oscillations in somato-sensory evoked potentials. J Clin Neurophysiol. 2006;23(5):42630.CrossRefGoogle Scholar
28Mochizuki, H, Ugawa, Y, Machii, K, et al.Somatosensory evoked high-frequency oscillation in Parkinson’s disease and myoclonus epilepsy. Clin Neurophysiol. 1999;110(1):18591.Google Scholar
29Hamada, M, Hanajima, R, Terao, Y, et al.Median nerve somatosensory evoked potentials and their high-frequency oscillations in amyotrophic lateral sclerosis. Clin Neurophysiol. 2007;118(4):87786.Google Scholar
30Nakano, S, Hashimoto, I.The later part of high-frequency oscillations in human somatosensory evoked potentials is enhanced in aged subjects. Neurosci Lett. 1999;276(2):836.Google Scholar
31Curio, G.Linking 600-Hz “spikelike” EEG/MEG wavelets (“sigmabursts”) to cellular substrates: concepts and caveats. J Clin Neurophysiol. 2000;17(4):37796.Google Scholar
32Burstein, R, Yarnitsky, D, Goor-Aryeh, I, et al.An association between migraine and cutaneous allodynia. Ann Neurol. 2000; 47(5):61424.Google Scholar
33Weissman-Fogel, I, Sprecher, E, Granovsky, Y, et al.Repeated noxious stimulation of the skin enhances cutaneous pain perception of migraine patients in-between attacks: clinical evidence for continuous sub-threshold increase in membrane excitability of central trigeminovascular neurons. Pain. 2003;104(3):693700.Google Scholar
34Zohsel, K, Hohmeister, J, Oelkers-Ax, R, et al.Quantitative sensory testing in children with migraine: preliminary evidence for enhanced sensitivity to painful stimuli especially in girls. Pain. 2006;123(1-2):108.CrossRefGoogle ScholarPubMed
35DaSilva, AF, Granziera, C, Tuch, DS, et al.Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport. 2007;18(4):3015.Google Scholar
36Inoue, K, Hashimoto, I, Nakamura, S.High-frequency oscillations in human posterior tibial somatosensory evoked potentials are enhanced in patients with Parkinson’s disease and multiple system atrophy. Neurosci Lett. 2001;297(2):8992.Google Scholar
37Inoue, K, Hashimoto, I, Shirai, T, et al.Disinhibition of the somatosensory cortex in cervical dystonia-decreased amplitudes of high-frequency oscillations. Clin Neurophysiol. 2004;115(7): 162430.Google Scholar
38Gobbel’, R, Waberski, TD, Kuelkens, S, et al.Thalamic and cortical high-frequency (600 Hz) somatosensory-evoked potential (SEP) components are modulated by slight arousal changes in awake subjects. Exp Brain Res. 2000;133(4):50613.Google Scholar
39Restuccia, D, Della Marca, G, Valeriani, M, et al.Brain-stem components of high-frequency somatosensory evoked potentials are modulated by arousal changes: nasopharyngeal recordings in healthy humans. Clin Neurophysiol. 2004;115(6):13928.Google Scholar
40Antal, A, Arlt, S, Nitsche, M, et al.Higher variability of phosphene thresholds in migraineurs than in controls: a consecutive transcranial magnetic stimulation study. Cephalalgia. 2006;26(7):86570.CrossRefGoogle ScholarPubMed
41Restuccia, D, Ulivelli, M, De Capua, A, et al.Modulation of high-frequency (600 Hz) somatosensory-evoked potentials after rTMS of the primary sensory cortex. Eur J Neurosci. 2007; 26(8):234958.CrossRefGoogle ScholarPubMed
42Allison, T, McCarthy, G, Wood, CC, et al.Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve: a review of scalp and intracranial recordings. Brain. 1991;114(6):2465503.Google Scholar