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Open Access 01-12-2016 | Research article

Quantitative neuromagnetic signatures of aberrant cortical excitability in pediatric chronic migraine

Authors: Kimberly A. Leiken, Jing Xiang, Emily Curry, Hisako Fujiwara, Douglas F. Rose, Janelle R. Allen, Joanne E. Kacperski, Hope L. O’Brien, Marielle A. Kabbouche, Scott W. Powers, Andrew D. Hershey

Published in: The Journal of Headache and Pain | Issue 1/2015

Abstract

Background

Reports have suggested that abnormal cortical excitability may be associated with acute migraines. The present study quantitatively assesses the degree of cortical excitability in chronic migraine as compared to acute migraine and healthy controls within the pediatric population.

Methods

We investigated 27 children suffering from chronic migraine, 27 children suffering from acute migraine, and 27 healthy controls using a magnetoencephalography (MEG) system, recording at a sampling rate of 6000 Hz. All groups were age-matched and gender-matched. Neuromagnetic brain activation was elicited by a finger-tapping motor task. The spatiotemporal and spectral signatures of MEG data within a 5–2884 Hz range were analyzed using Morlet wavelet transform and beamformer analyses.

Results

Compared with controls, the chronic migraine group showed (1) significantly prolonged latencies of movement-elicited magnetic fields (MEFs) between 5 and 100 Hz; (2) increased spectral power between 100 and 200 Hz, and between 2200 and 2800 Hz; and (3) a higher likelihood of neuromagnetic activation in the ipsilateral sensorimotor cortices, supplementary motor area, and occipital regions. Compared with acute migraine group, chronic migraine patients showed (1) significantly higher odds of having strong MEFs after 150 ms; and (2) significantly higher odds of having neuromagnetic activation from the deep brain areas.

Conclusions

Results demonstrated that chronic migraine subjects were not only different from the healthy controls, but also different from acute migraine subjects. The chronification of migraines may be associated with elevated cortical excitability, delayed and spread neural response, as well as aberrant activation from deep brain areas.

Stovner LJ, Andree C (2010) Prevalence of headache in Europe: a review for the Eurolight project. J Headache Pain 11(4):289–299. doi:10.1007/s10194-010-0217-0 CrossRefPubMedPubMedCentral

Lipton RB (2009) Tracing transformation: chronic migraine classification, progression, and epidemiology. Neurology 72(5 Suppl):S3–7. doi:10.1212/WNL.0b013e3181974b19 CrossRefPubMed

Bigal ME, Sheftell FD, Rapoport AM, Lipton RB, Tepper SJ (2002) Chronic daily headache in a tertiary care population: correlation between the International Headache Society diagnostic criteria and proposed revisions of criteria for chronic daily headache. Cephalalgia 22(6):432–438CrossRefPubMed

Koenig MA, Gladstein J, McCarter RJ, Hershey AD, Wasiewski W (2002) Chronic daily headache in children and adolescents presenting to tertiary headache clinics. Headache 42(6):491–500CrossRefPubMed

Seshia SS, Wang SJ, Abu-Arafeh I, Hershey AD, Guidetti V, Winner P, Wober-Bingol C (2010) Chronic daily headache in children and adolescents: a multi-faceted syndrome. Can J Neurol Sci 37(6):769–778PubMed

Bigal ME, Tepper SJ, Sheftell FD, Rapoport AM, Lipton RB (2004) Chronic daily headache: correlation between the 2004 and the 1988 International Headache Society diagnostic criteria. Headache 44(7):684–691. doi:10.1111/j.1526-4610.2004.04128.x CrossRefPubMed

Bigal ME, Sheftell FD, Rapoport AM, Tepper SJ, Lipton RB (2002) Chronic daily headache: identification of factors associated with induction and transformation. Headache 42(7):575–581CrossRefPubMed

Wheeler AH (1999) Chronic Daily Headache: Theory to Therapy. Curr Rev Pain 3(6):481–488CrossRefPubMed

Saper JR (2008) Chronic daily headache: transformational migraine, chronic migraine, and related disorders. Curr Neurol Neurosci Rep 8(2):100–107CrossRefPubMed

10.

Hershey AD (2003) Chronic daily headaches in children. Expert Opin Pharmacother 4(4):485–491. doi:10.1517/14656566.4.4.485 CrossRefPubMed

11.

Hershey AD, Kabbouche MA, Powers SW (2006) Chronic daily headaches in children. Curr Pain Headache Rep 10(5):370–376CrossRefPubMed

12.

Coppola G, Bracaglia M, Di Lenola D, Di Lorenzo C, Serrao M, Parisi V, Di Renzo A, Martelli F, Fadda A, Schoenen J, Pierelli F (2015) Visual evoked potentials in subgroups of migraine with aura patients. J Headache Pain 16:92. doi:10.1186/s10194-015-0577-6 CrossRefPubMedPubMedCentral

13.

Xiang J, deGrauw X, Korostenskaja M, Korman AM, O'Brien HL, Kabbouche MA, Powers SW, Hershey AD (2013) Altered cortical activation in adolescents with acute migraine: a magnetoencephalography study. J Pain 14(12):1553–1563. doi:10.1016/j.jpain.2013.04.009 CrossRefPubMed

14.

Xiang J, Degrauw X, Korman AM, Allen JR, O'Brien HL, Kabbouche MA, Powers SW, Hershey AD (2013) Neuromagnetic abnormality of motor cortical activation and phases of headache attacks in childhood migraine. PLoS One 8(12):e83669. doi:10.1371/journal.pone.0083669 CrossRefPubMedPubMedCentral

15.

Bowyer SM, Shvarts V, Moran JE, Mason KM, Barkley GL, Tepley N (2012) Slow brain activity (ISA/DC) detected by MEG. J Clin Neurophysiol 29(4):320–326. doi:10.1097/WNP.0b013e3182624342 CrossRefPubMedPubMedCentral

16.

Bowyer SM, Mason KM, Moran JE, Tepley N, Mitsias PD (2005) Cortical hyperexcitability in migraine patients before and after sodium valproate treatment. J Clin Neurophysiol 22(1):65–67CrossRefPubMed

17.

Huo X, Wang Y, Kotecha R, Kirtman EG, Fujiwara H, Hemasilpin N, Degrauw T, Rose DF, Xiang J (2011) High gamma oscillations of sensorimotor cortex during unilateral movement in the developing brain: a MEG study. Brain Topogr 23(4):375–384. doi:10.1007/s10548-010-0151-0 CrossRefPubMed

18.

Wang X, Xiang J, Wang Y, Pardos M, Meng L, Huo X, Korostenskaja M, Powers SW, Kabbouche MA, Hershey AD (2010) Identification of abnormal neuromagnetic signatures in the motor cortex of adolescent migraine. Headache 50(6):1005–1016. doi:10.1111/j.1526-4610.2010.01674.x CrossRefPubMed

19.

Liu H, Ge H, Xiang J, Miao A, Tang L, Wu T, Chen Q, Yang L, Wang X (2015) Resting state brain activity in patients with migraine: a magnetoencephalography study. J Headache Pain 16:525. doi:10.1186/s10194-015-0525-5 CrossRefPubMed

20.

Xiang J, Wang Y, Chen Y, Liu Y, Kotecha R, Huo X, Rose DF, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Jones B, DeGrauw T (2010) Noninvasive localization of epileptogenic zones with ictal high-frequency neuromagnetic signals. J Neurosurg Pediatr 5(1):113–122. doi:10.3171/2009.8.PEDS09345 CrossRefPubMed

21.

Xiang J, Liu Y, Wang Y, Kirtman EG, Kotecha R, Chen Y, Huo X, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Leach J, Jones B, DeGrauw T, Rose D (2009) Frequency and spatial characteristics of high-frequency neuromagnetic signals in childhood epilepsy. Epileptic Disord 11(2):113–125. doi:10.1684/epd.2009.0253 PubMed

22.

Leahy RM, Mosher JC, Spencer ME, Huang MX, Lewine JD (1998) A study of dipole localization accuracy for MEG and EEG using a human skull phantom. Electroencephalogr Clin Neurophysiol 107(2):159–173CrossRefPubMed

23.

Siniatchkin M, Sendacki M, Moeller F, Wolff S, Jansen O, Siebner H, Stephani U (2012) Abnormal changes of synaptic excitability in migraine with aura. Cereb Cortex 22(10):2207–2216. doi:10.1093/cercor/bhr248 CrossRefPubMed

24.

Antal A, Kriener N, Lang N, Boros K, Paulus W (2011) Cathodal transcranial direct current stimulation of the visual cortex in the prophylactic treatment of migraine. Cephalalgia 31(7):820–828. doi:10.1177/0333102411399349 CrossRefPubMed

25.

Ward TN (2010) Transcranial magnetic stimulation. Headache 50(10):1629. doi:10.1111/j.1526-4610.2010.01786.x CrossRefPubMed

26.

Teepker M, Hotzel J, Timmesfeld N, Reis J, Mylius V, Haag A, Oertel WH, Rosenow F, Schepelmann K (2010) Low-frequency rTMS of the vertex in the prophylactic treatment of migraine. Cephalalgia 30(2):137–144. doi:10.1111/j.1468-2982.2009.01911.x PubMed

27.

Lo YL (2010) Headache: migraine, magnetic stimulation and cortical excitability. Nat Rev Neurol 6(8):425–427. doi:10.1038/nrneurol.2010.109 CrossRefPubMed

28.

Headache Classification Committee of the International Headache Society (1988) Classification and diagnostic criteria for headache disorders, cranial neuralgias and facial pain. Cephalalgia 8(Suppl 7):1–96

29.

Hershey AD, Winner P, Kabbouche MA, Gladstein J, Yonker M, Lewis D, Pearlman E, Linder SL, Rothner AD, Powers SW (2005) Use of the ICHD-II criteria in the diagnosis of pediatric migraine. Headache 45(10):1288–1297. doi:10.1111/j.1526-4610.2005.00260.x CrossRefPubMed

30.

Hershey AD, Powers SW, Vockell AL, LeCates SL, Segers A, Kabbouche MA (2004) Development of a patient-based grading scale for PedMIDAS. Cephalalgia 24(10):844–849. doi:10.1111/j.1468-2982.2004.00757.x CrossRefPubMed

31.

Kotecha R, Xiang J, Wang Y, Huo X, Hemasilpin N, Fujiwara H, Rose D, deGrauw T (2009) Time, frequency and volumetric differences of high-frequency neuromagnetic oscillation between left and right somatosensory cortices. Int J Psychophysiol 72(2):102–110. doi:10.1016/j.ijpsycho.2008.10.009 CrossRefPubMed

32.

Xiang J, Korman A, Samarasinghe KM, Wang X, Zhang F, Qiao H, Sun B, Wang F, Fan HH, Thompson EA (2015) Volumetric imaging of brain activity with spatial-frequency decoding of neuromagnetic signals. J Neurosci Methods 239:114–128. doi:10.1016/j.jneumeth.2014.10.007 CrossRefPubMed

33.

Xiang J, Luo Q, Kotecha R, Korman A, Zhang F, Luo H, Fujiwara H, Hemasilpin N, Rose DF (2014) Accumulated source imaging of brain activity with both low and high-frequency neuromagnetic signals. Frontiers Neuroinformatics 8(57):57. doi:10.3389/fninf.2014.00057

34.

Thompson EA, Xiang J, Wang YY (2015) Frequency-spatial beamformer for MEG source localization. Biomed Signal Process Contr 18:263–273. doi:10.1016/j.bspc.2015.01.004 CrossRef

35.

Huo X, Xiang J, Wang Y, Kirtman EG, Kotecha R, Fujiwara H, Hemasilpin N, Rose DF, Degrauw T (2010) Gamma oscillations in the primary motor cortex studied with MEG. Brain Dev 32(8):619–624. doi:10.1016/j.braindev.2009.09.021 CrossRefPubMed

36.

Hershey AD (2010) Current approaches to the diagnosis and management of paediatric migraine. Lancet Neurol 9(2):190–204. doi:10.1016/S1474-4422(09)70303-5 CrossRefPubMed

37.

Guo X, Xiang J, Wang Y, O'Brien H, Kabbouche M, Horn P, Powers SW, Hershey AD (2012) Aberrant neuromagnetic activation in the motor cortex in children with acute migraine: a magnetoencephalography study. PLoS One 7(11):e50095. doi:10.1371/journal.pone.0050095 CrossRefPubMedPubMedCentral

38.

Rocca MA, Colombo B, Pagani E, Falini A, Codella M, Scotti G, Comi G, Filippi M (2003) Evidence for cortical functional changes in patients with migraine and white matter abnormalities on conventional and diffusion tensor magnetic resonance imaging. Stroke 34(3):665–670. doi:10.1161/01.STR.0000057977.06681.11 CrossRefPubMed

39.

Cheyne D, Bells S, Ferrari P, Gaetz W, Bostan AC (2008) Self-paced movements induce high-frequency gamma oscillations in primary motor cortex. NeuroImage 42(1):332–342. doi:10.1016/j.neuroimage.2008.04.178 CrossRefPubMed

40.

Ge HT, Liu HX, Xiang J, Miao AL, Tang L, Guan QS, Wu T, Chen QQ, Yang L, Wang XS (2015) Abnormal cortical activation in females with acute migraine: a magnetoencephalography study. Clin Neurophysiol 126(1):170–179. doi:10.1016/j.clinph.2014.03.033 CrossRefPubMed

41.

Bowyer SM, Fleming T, Greenwald ML, Moran JE, Mason KM, Weiland BJ, Smith BJ, Barkley GL, Tepley N (2005) Magnetoencephalographic localization of the basal temporal language area. Epilepsy Behav 6(2):229–234. doi:10.1016/j.yebeh.2004.12.003 CrossRefPubMed

42.

Gummadavelli A, Wang Y, Guo X, Pardos M, Chu H, Liu Y, Horn P, Zhang F, Xiang J (2013) Spatiotemporal and frequency signatures of word recognition in the developing brain: a magnetoencephalographic study. Brain Res 1498:20–32. doi:10.1016/j.brainres.2013.01.001 CrossRefPubMed

43.

Sakura Y, Terada K, Usui K, Baba K, Usui N, Umeoka S, Yamaguchi M, Matsuda K, Tottori T, Mihara T, Nakamura F, Inoue Y (2009) Very high-frequency oscillations (over 1000 Hz) of somatosensory-evoked potentials directly recorded from the human brain. J Clin Neurophysiol 26(6):414–421. doi:10.1097/WNP.0b013e3181c298c9 CrossRefPubMed

44.

Usui N, Terada K, Baba K, Matsuda K, Nakamura F, Usui K, Tottori T, Umeoka S, Fujitani S, Mihara T, Inoue Y (2010) Very high frequency oscillations (over 1000 Hz) in human epilepsy. Clin Neurophysiol 121(11):1825–1831. doi:10.1016/j.clinph.2010.04.018 CrossRefPubMed

45.

Conforto AB, Moraes MS, Amaro E Jr, Young WB, Lois LA, Goncalves AL, Peres MF (2012) Increased variability of motor cortical excitability to transcranial magnetic stimulation in migraine: a new clue to an old enigma. J Headache Pain 13(1):29–37. doi:10.1007/s10194-011-0379-4 CrossRefPubMedPubMedCentral

46.

Rapoport A (2011) New frontiers in headache therapy. Neurol Sci 32(Suppl 1):S105–109. doi:10.1007/s10072-011-0542-3 CrossRefPubMed

Title: Quantitative neuromagnetic signatures of aberrant cortical excitability in pediatric chronic migraine
Authors: Kimberly A. Leiken
Jing Xiang
Emily Curry
Hisako Fujiwara
Douglas F. Rose
Janelle R. Allen
Joanne E. Kacperski
Hope L. O’Brien
Marielle A. Kabbouche
Scott W. Powers
Andrew D. Hershey
Publication date: 01-12-2016
Publisher: Springer Milan
Published in: The Journal of Headache and Pain / Issue 1/2015
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI: https://doi.org/10.1186/s10194-016-0641-x

At a glance: The STEP trials

Springer Medicine

Quantitative neuromagnetic signatures of aberrant cortical excitability in pediatric chronic migraine

Abstract

Background

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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