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The Journal of Headache and Pain
Published in: The Journal of Headache and Pain 1/2017

Open Access 01-12-2017 | Research article

Interictal brain activity differs in migraine with and without aura: resting state fMRI study

Authors: Péter Faragó, Bernadett Tuka, Eszter Tóth, Nikoletta Szabó, András Király, Gergő Csete, Délia Szok, János Tajti, Árpád Párdutz, László Vécsei, Zsigmond Tamás Kincses

Published in: The Journal of Headache and Pain | Issue 1/2017

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Abstract

Background

Migraine is one of the most severe primary headache disorders. The nature of the headache and the associated symptoms during the attack suggest underlying functional alterations in the brain. In this study, we examined amplitude, the resting state fMRI fluctuation in migraineurs with and without aura (MWA, MWoA respectively) and healthy controls.

Methods

Resting state functional MRI images and T1 high-resolution images were acquired from all participants. For data analysis we compared the groups (MWA-Control, MWA-MWoA, MWoA-Control). The resting state networks were identified by MELODIC. The mean time courses of the networks were identified for each participant for all networks. The time-courses were decomposed into five frequency bands by discrete wavelet decomposition. The amplitude of the frequency-specific activity was compared between groups. Furthermore, the preprocessed resting state images were decomposed by wavelet analysis into five specific frequency bands voxel-wise. The voxel-wise amplitudes were compared between groups by non-parametric permutation test.

Results

In the MWA-Control comparison the discrete wavelet decomposition found alterations in the lateral visual network. Higher activity was measured in the MWA group in the highest frequency band (0.16–0.08 Hz).
In case of the MWA-MWoA comparison all networks showed higher activity in the 0.08–0.04 Hz frequency range in MWA, and the lateral visual network in in higher frequencies.
In MWoA-Control comparison only the default mode network revealed decreased activity in MWoA group in the 0.08–0.04 Hz band.
The voxel-wise frequency specific analysis of the amplitudes found higher amplitudes in MWA as compared to MWoA in the in fronto-parietal regions, anterior cingulate cortex and cerebellum.

Discussion

The amplitude of the resting state fMRI activity fluctuation is higher in MWA than in MWoA. These results are in concordance with former studies, which found cortical hyperexcitability in MWA.
Literature
1.
Lipton RB, Bigal ME, Steiner TJ, Silberstein SD, Olesen J (2004) Classification of primary headaches. Neurology 63:427–435CrossRefPubMed
2.
Headache Classification Committee of the International Headache (2013) The international classification of headache disorders, 3rd edition (beta version). Cephalalgia 33:629–808CrossRef
3.
Manzoni GC, Torelli P (2008) Migraine with and without aura: a single entity? Neurol sci 29(Suppl 1):S40–43CrossRefPubMed
4.
Ranson R, Igarashi H, MacGregor EA, Wilkinson M (1991) The similarities and differences of migraine with aura and migraine without aura: a preliminary study. Cephalalgia 11:189–192CrossRefPubMed
5.
Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 98:4687–4692CrossRefPubMedPubMedCentral
6.
Petrusic I, Zidverc-Trajkovic J (2014) Cortical spreading depression: origins and paths as inferred from the sequence of events during migraine aura. Funct Neurol 29:207–212PubMedPubMedCentral
7.
Antal A, Temme J, Nitsche MA, Varga ET, Lang N, Paulus W (2005) Altered motion perception in migraineurs: evidence for interictal cortical hyperexcitability. Cephalalgia 25:788–794CrossRefPubMed
8.
Pierelli F, Iacovelli E, Bracaglia M, Serrao M, Coppola G (2013) Abnormal sensorimotor plasticity in migraine without aura patients. Pain 154:1738–1742CrossRefPubMed
9.
Aurora SK, Ahmad BK, Welch KM, Bhardhwaj P, Ramadan NM (1998) Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50:1111–1114CrossRefPubMed
10.
Chadaide Z, Arlt S, Antal A, Nitsche MA, Lang N, Paulus W (2007) Transcranial direct current stimulation reveals inhibitory deficiency in migraine. Cephalalgia 27:833–839CrossRefPubMed
11.
Gawel M, Connolly JF, Rose FC (1983) Migraine patients exhibit abnormalities in the visual evoked potential. Headache 23:49–52CrossRefPubMed
12.
Afra J, Proietti Cecchini A, Sandor PS, Schoenen J (2000) Comparison of visual and auditory evoked cortical potentials in migraine patients between attacks. Clin Neurophysiol 111:1124–1129CrossRefPubMed
13.
Brigo F, Storti M, Nardone R, Fiaschi A, Bongiovanni LG, Tezzon F, Manganotti P (2012) Transcranial magnetic stimulation of visual cortex in migraine patients: a systematic review with meta-analysis. J Headache Pain 13:339–349CrossRefPubMedPubMedCentral
14.
Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci U S A 104:13170–13175CrossRefPubMedPubMedCentral
15.
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos T Roy Soc B 360:1001–1013CrossRef
16.
Xue T, Yuan K, Zhao L, Yu D, Zhao L, Dong T, Cheng P, von Deneen KM, Qin W, Tian J (2012) Intrinsic brain network abnormalities in migraines without aura revealed in resting-state fMRI. PloS One 7(12):e52927. doi:10.​1371/​journal.​pone.​0052927
17.
Tessitore A, Russo A, Giordano A, Conte F, Corbo D, De Stefano M, Cirillo S, Cirillo M, Esposito F, Tedeschi G (2013) Disrupted default mode network connectivity in migraine without aura. J Headache Pain 14:89. doi:10.​1186/​1129-2377-14-89
18.
Yuan K, Zhao L, Cheng P, Yu DH, Zhao LM, Dong T, Xing LH, Bi YZ, Yang XJ, von Deneen KM, Liang FR, Gong QY, Qin W, Tian J (2013) Altered structure and resting-state functional connectivity of the basal ganglia in migraine patients without aura. J Pain 14:836–844CrossRefPubMed
19.
Mainero C, Boshyan J, Hadjikhani N (2011) Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Ann Neurol 70:838–845CrossRefPubMedPubMedCentral
20.
Tedeschi G, Russo A, Conte F, Corbo D, Caiazzo G, Giordano A, Conforti R, Esposito F, Tessitore A (2015) Increased interictal visual network connectivity in patients with migraine with aura. Cephalalgia: an international journal of headache. doi:10.​1177/​0333102415584360​
21.
Hadjikhani N, Ward N, Boshyan J, Napadow V, Maeda Y, Truini A, Caramia F, Tinelli E, Mainero C (2013) The missing link: enhanced functional connectivity between amygdala and visceroceptive cortex in migraine. Cephalalgia 33:1264–1268CrossRefPubMedPubMedCentral
22.
Niddam DM, Lai KL, Fuh JL, Chuang CY, Chen WT, Wang SJ (2015) Reduced functional connectivity between salience and visual networks in migraine with aura. Cephalalgia: an international journal of headache. doi:10.​1177/​0333102415583144​
23.
Tessitore A, Russo A, Conte F, Giordano A, De Stefano M, Lavorgna L, Corbo D, Caiazzo G, Esposito F, Tedeschi G (2015) Abnormal connectivity within executive resting-state network in migraine with aura. Headache 55:794–805CrossRefPubMed
24.
Hougaard A, Amin FM, Magon S, Sprenger T, Rostrup E, Ashina M (2015) No abnormalities of intrinsic brain connectivity in the interictal phase of migraine with aura. Eur j neurol 22:702–e746CrossRefPubMed
25.
Hougaard A, Amin FM, Hoffmann MB, Larsson HB, Magon S, Sprenger T, Ashina M (2015) Structural gray matter abnormalities in migraine relate to headache lateralization, but not aura. Cephalalgia 35:3–9CrossRefPubMed
26.
Schwedt TJ, Schlaggar BL, Mar S, Nolan T, Coalson RS, Nardos B, Benzinger T, Larson-Prior LJ (2013) Atypical resting-state functional connectivity of affective pain regions in chronic migraine. Headache 53:737–751CrossRefPubMedPubMedCentral
27.
Jin CW, Yuan K, Zhao LM, Zhao L, Yu DH, von Deneen KM, Zhang M, Qin W, Sun WX, Tian J (2013) Structural and functional abnormalities in migraine patients without aura. NMR Biomed 26:58–64CrossRefPubMed
28.
29.
Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, Wang YF, Zang YF (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172:137–141CrossRefPubMedPubMedCentral
30.
Kim JY, Kim SH, Seo J, Kim SH, Han SW, Nam EJ, Kim SK, Lee HJ, Lee SJ, Kim YT, Chang Y (2013) Increased power spectral density in resting-state pain-related brain networks in fibromyalgia. Pain 154:1792–1797CrossRefPubMed
31.
32.
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefPubMed
33.
Beckmann CF, Smith SM (2005) Tensorial extensions of independent component analysis for multisubject FMRI analysis. Neuroimage 25:294–311CrossRefPubMed
34.
Oelkers R, Grosser K, Lang E, Geisslinger G, Kobal G, Brune K, Lotsch J (1999) Visual evoked potentials in migraine patients: alterations depend on pattern spatial frequency. Brain 122(Pt 6):1147–1155CrossRefPubMed
35.
Connolly JF, Gawel M, Rose FC (1982) Migraine patients exhibit abnormalities in the visual evoked potential. J Neurol Neurosurg Psychiatry 45:464–467CrossRefPubMedPubMedCentral
36.
Diener HC, Scholz E, Dichgans J, Gerber WD, Jack A, Bille A, Niederberger U (1989) Central effects of drugs used in migraine prophylaxis evaluated by visual evoked potentials. Ann Neurol 25:125–130CrossRefPubMed
37.
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 16:92CrossRefPubMedPubMedCentral
38.
Sand T, Zhitniy N, White LR, Stovner LJ (2008) Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin Neurophysiol 119:1020–1027CrossRefPubMed
39.
Brigo F, Storti M, Tezzon F, Manganotti P, Nardone R (2013) Primary visual cortex excitability in migraine: a systematic review with meta-analysis. Neurol Sci 34:819–830CrossRefPubMed
40.
Vincent M, Pedra E, Mourao-Miranda J, Bramati IE, Henrique AR, Moll J (2003) Enhanced interictal responsiveness of the migraineous visual cortex to incongruent bar stimulation: a functional MRI visual activation study. Cephalalgia 23:860–868CrossRefPubMed
41.
42.
Boulloche N, Denuelle M, Payoux P, Fabre N, Trotter Y, Geraud G (2010) Photophobia in migraine: an interictal PET study of cortical hyperexcitability and its modulation by pain. J Neurol Neurosurg Psychiatry 81:978–984CrossRefPubMed
43.
Datta R, Aguirre GK, Hu S, Detre JA, Cucchiara B (2013) Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura. Cephalalgia 33:365–374CrossRefPubMedPubMedCentral
44.
Cucchiara B, Datta R, Aguirre GK, Idoko KE, Detre J (2015) Measurement of visual sensitivity in migraine: validation of two scales and correlation with visual cortex activation. Cephalalgia 35:585–592CrossRefPubMed
45.
Gonzalez de la Aleja J, Ramos A, Mato-Abad V, Martinez-Salio A, Hernandez-Tamames JA, Molina JA, Hernandez-Gallego J, Alvarez-Linera J (2013) Higher glutamate to glutamine ratios in occipital regions in women with migraine during the interictal state. Headache 53:365–375CrossRefPubMed
46.
Bridge H, Stagg CJ, Near J, Lau CI, Zisner A, Cader MZ (2015) Altered neurochemical coupling in the occipital cortex in migraine with visual aura. Cephalalgia 35:1025–1030CrossRefPubMed
47.
Sarchielli P, Tarducci R, Presciutti O, Gobbi G, Pelliccioli GP, Stipa G, Alberti A, Capocchi G (2005) Functional 1H-MRS findings in migraine patients with and without aura assessed interictally. Neuroimage 24:1025–1031CrossRefPubMed
48.
Hougaard A, Amin FM, Hoffmann MB, Rostrup E, Larsson HB, Asghar MS, Larsen VA, Olesen J, Ashina M (2014) Interhemispheric differences of fMRI responses to visual stimuli in patients with side-fixed migraine aura. Hum Brain Mapp 35:2714–2723CrossRefPubMed
49.
Russo A, Tessitore A, Giordano A, Corbo D, Marcuccio L, De Stefano M, Salemi F, Conforti R, Esposito F, Tedeschi G (2012) Executive resting-state network connectivity in migraine without aura. Cephalalgia 32:1041–1048CrossRefPubMed
50.
Ma X, Li S, Tian J, Jiang G, Wen H, Wang T, Fang J, Zhan W, Xu Y (2015) Altered brain spontaneous activity and connectivity network in irritable bowel syndrome patients: a resting-state fMRI study. Clin Neurophysiol 126:1190–1197CrossRefPubMed
51.
Baliki MN, Mansour AR, Baria AT, Apkarian AV (2014) Functional reorganization of the default mode network across chronic pain conditions. PLoS One 9:e106133CrossRefPubMedPubMedCentral
52.
Wang JJ, Chen X, Sah SK, Zeng C, Li YM, Li N, Liu MQ, Du SL (2016) Amplitude of low-frequency fluctuation (ALFF) and fractional ALFF in migraine patients: a resting-state functional MRI study. Clin Radiol 71:558–564CrossRefPubMed
53.
Gao L, Bai L, Zhang Y, Dai XJ, Netra R, Min Y, Zhou F, Niu C, Dun W, Gong H, Zhang M (2015) Frequency-dependent changes of local resting oscillations in sleep-deprived brain. PLoS One 10:e0120323CrossRefPubMedPubMedCentral
54.
Otti A, Guendel H, Wohlschlager A, Zimmer C, Noll-Hussong M (2013) Frequency shifts in the anterior default mode network and the salience network in chronic pain disorder. BMC Psychiatry 13:84CrossRefPubMedPubMedCentral
55.
Salvador R, Martinez A, Pomarol-Clotet E, Gomar J, Vila F, Sarro S, Capdevila A, Bullmore E (2008) A simple view of the brain through a frequency-specific functional connectivity measure. Neuroimage 39:279–289CrossRefPubMed
56.
Malinen S, Vartiainen N, Hlushchuk Y, Koskinen M, Ramkumar P, Forss N, Kalso E, Hari R (2010) Aberrant temporal and spatial brain activity during rest in patients with chronic pain. Proc Natl Acad Sci U S A 107:6493–6497CrossRefPubMedPubMedCentral
57.
Boyacioglu R, Beckmann CF, Barth M (2013) An investigation of RSN frequency spectra using ultra-fast generalized inverse imaging. Front Hum Neurosci 7:156CrossRefPubMedPubMedCentral
58.
59.
Davis KD, Moayedi M (2013) Central mechanisms of pain revealed through functional and structural MRI. J Neuroimmune Pharmacol 8:518–534CrossRefPubMed
60.
Bliss TV, Collingridge GL, Kaang B-K, Zhuo M (2016) Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nature Reviews Neuroscience
61.
Cohen S, Mao J (2014) Neuropathic Pain: Mechanisms & Clinical Implications + MP3. Br Med J 348:f7656CrossRef
62.
Treede R-D, Kenshalo DR, Gracely RH, Jones AK (1999) The cortical representation of pain. Pain 79:105–111CrossRefPubMed
63.
Denk F, McMahon SB, Tracey I (2014) Pain vulnerability: a neurobiological perspective. Nat Neurosci 17:192–200CrossRefPubMed
64.
Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422:556–578CrossRefPubMed
65.
Spisak T, Pozsgay Z, Aranyi C, David S, Kocsis P, Nyitrai G, Gajari D, Emri M, Czurko A, Kincses ZT, Central sensitization related changes of effective and functional connectivity in the rat inflammatory trigeminal pain model. Neuroscience (in press)
66.
67.
Sandor PS, Mascia A, Seidel L, de Pasqua V, Schoenen J (2001) Subclinical cerebellar impairment in the common types of migraine: a three-dimensional analysis of reaching movements. Ann Neurol 49:668–672CrossRefPubMed
68.
Harno H, Hirvonen T, Kaunisto MA, Aalto H, Levo H, Isotalo E, Kallela M, Kaprio J, Palotie A, Wessman M, Farkkila M (2003) Subclinical vestibulocerebellar dysfunction in migraine with and without aura. Neurology 61:1748–1752CrossRefPubMed
69.
Granziera C, Romascano D, Daducci A, Roche A, Vincent M, Krueger G, Hadjikhani N (2013) Migraineurs without aura show microstructural abnormalities in the cerebellum and frontal lobe. Cerebellum 12:812–818CrossRefPubMed
70.
Jin C, Yuan K, Zhao L, Zhao L, Yu D, von Deneen KM, Zhang M, Qin W, Sun W, Tian J (2013) Structural and functional abnormalities in migraine patients without aura. NMR Biomed 26:58–64CrossRefPubMed
71.
Arkink EB, Bleeker EJ, Schmitz N, Schoonman GG, Wu O, Ferrari MD, van Buchem MA, van Osch MJ, Kruit MC (2012) Cerebral perfusion changes in migraineurs: a voxelwise comparison of interictal dynamic susceptibility contrast MRI measurements. Cephalalgia 32:279–288CrossRefPubMedPubMedCentral
72.
O’Bryant SE, Marcus DA, Rains JC, Penzien DB (2005) Neuropsychology of migraine: present status and future directions. Expert Rev Neurother 5:363–370CrossRefPubMed
73.
Camarda C, Monastero R, Pipia C, Recca D, Camarda R (2007) Interictal executive dysfunction in migraineurs without aura: relationship with duration and intensity of attacks. Cephalalgia 27:1094–1100CrossRefPubMed
Metadata
Title
Interictal brain activity differs in migraine with and without aura: resting state fMRI study
Authors
Péter Faragó
Bernadett Tuka
Eszter Tóth
Nikoletta Szabó
András Király
Gergő Csete
Délia Szok
János Tajti
Árpád Párdutz
László Vécsei
Zsigmond Tamás Kincses
Publication date
01-12-2017
Publisher
Springer Milan
Published in
The Journal of Headache and Pain / Issue 1/2017
Print ISSN: 1129-2369
Electronic ISSN: 1129-2377
DOI
https://doi.org/10.1186/s10194-016-0716-8

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