Altered Resting State Functional Activity and Microstructure of the White Matter in Migraine With Aura
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
31632336
PubMed Central
PMC6779833
DOI
10.3389/fneur.2019.01039
Knihovny.cz E-resources
- Keywords
- ALFF, diffusion, fMRI, migraine, resting state, white matter,
- Publication type
- Journal Article MeSH
Introduction: Brain structure and function were reported to be altered in migraine. Importantly our earlier results showed that white matter diffusion abnormalities and resting state functional activity were affected differently in the two subtypes of the disease, migraine with and without aura. Resting fluctuation of the BOLD signal in the white matter was reported recently. The question arising whether the white matter activity, that is strongly coupled with gray matter activity is also perturbed differentially in the two subtypes of the disease and if so, is it related to the microstructural alterations of the white matter. Methods: Resting state fMRI, 60 directional DTI images and high-resolution T1 images were obtained from 51 migraine patients and 32 healthy volunteers. The images were pre-processed and the white matter was extracted. Independent component analysis was performed to obtain white matter functional networks. The differential expression of the white matter functional networks in the two subtypes of the disease was investigated with dual-regression approach. The Fourier spectrum of the resting fMRI fluctuations were compared between groups. Voxel-wise correlation was calculated between the resting state functional activity fluctuations and white matter microstructural measures. Results: Three white matter networks were identified that were expressed differently in migraine with and without aura. Migraineurs with aura showed increased functional connectivity and amplitude of BOLD fluctuation. Fractional anisotropy and radial diffusivity showed strong correlation with the expression of the frontal white matter network in patients with aura. Discussion: Our study is the first to describe changes in white matter resting state functional activity in migraine with aura, showing correlation with the underlying microstructure. Functional and structural differences between disease subtypes suggest at least partially different pathomechanism, which may necessitate handling of these subtypes as separate entities in further studies.
Central European Institute of Technology Brno Czechia
Department of Radiology Faculty of Medicine University of Szeged Szeged Hungary
See more in PubMed
Lipton RB, Stewart WF, Von Korff M. Burden of migraine: societal costs and therapeutic opportunities. Neurology. (1997) 48:S4–9. 10.1212/WNL.48.3_Suppl_3.4S PubMed DOI
Pellegrino ABW, Davis-Martin RE, Houle TT, Turner DP, Smitherman TA. Perceived triggers of primary headache disorders: a meta-analysis. Cephalalgia. (2018) 38:1188–98. 10.1177/0333102417727535 PubMed DOI PMC
Charles AC, Baca SM. Cortical spreading depression and migraine. Nat Rev Neurol. (2013) 9:637–44. 10.1038/nrneurol.2013.192 PubMed DOI
Pietrobon D, Moskowitz MA. Pathophysiology of migraine. Annu Rev Physiol. (2013) 75:365–91. 10.1146/annurev-physiol-030212-183717 PubMed DOI
Sand T, Zhitniy N, White LR, Stovner LJ. Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin Neurophysiol. (2008) 119:1020–7. 10.1016/j.clinph.2008.01.009 PubMed DOI
Coppola G, Bracaglia M, Di Lenola D, Di Lorenzo C, Serrao M, Parisi V, et al. . Visual evoked potentials in subgroups of migraine with aura patients. J Headache Pain. (2015) 16:92. 10.1186/s10194-015-0577-6 PubMed DOI PMC
Antal A, Temme J, Nitsche MA, Varga ET, Lang N, Paulus W. Altered motion perception in migraineurs: evidence for interictal cortical hyperexcitability. Cephalalgia. (2005) 25:788–94. 10.1111/j.1468-2982.2005.00949.x PubMed DOI
Vincent M, Pedra E, Mourao-Miranda J, Bramati IE, Henrique AR, Moll J. Enhanced interictal responsiveness of the migraineous visual cortex to incongruent bar stimulation: a functional MRI visual activation study. Cephalalgia. (2003) 23:860–8. 10.1046/j.1468-2982.2003.00609.x PubMed DOI
Datta R, Aguirre GK, Hu SY, Detre JA, Cucchiara B. Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura. Cephalalgia. (2013) 33:365–74. 10.1177/0333102412474503 PubMed DOI PMC
Leao AA. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol. (1947) 10:409–14. 10.1152/jn.1947.10.6.409 PubMed DOI
Ren J, Xiang J, Chen Y, Li F, Wu T, Shi J. Abnormal functional connectivity under somatosensory stimulation in migraine: a multi-frequency magnetoencephalography study. J Headache Pain. (2019) 20:3. 10.1186/s10194-019-0958-3 PubMed DOI PMC
Beese LC, Putzer D, Osada N, Evers S, Marziniak M. Contact heat evoked potentials and habituation measured interictally in migraineurs. J Headache Pain. (2015) 16:1. 10.1186/1129-2377-16-1 PubMed DOI PMC
Russo A, Esposito F, Conte F, Fratello M, Caiazzo G, Marcuccio L, et al. . Functional interictal changes of pain processing in migraine with ictal cutaneous allodynia. Cephalalgia. (2017) 37:305–14. 10.1177/0333102416644969 PubMed DOI
Kisler LB, Granovsky Y, Coghill RC, Sprecher E, Manor D, Yarnitsky D, et al. . Do patients with interictal migraine modulate pain differently from healthy controls? A psychophysical and brain imaging study. Pain. (2018) 159:2667–77. 10.1097/j.pain.0000000000001380 PubMed DOI
Tedeschi G, Russo A, Conte F, Corbo D, Caiazzo G, Giordano A, et al. . Increased interictal visual network connectivity in patients with migraine with aura. Cephalalgia. (2016) 36:139–47. 10.1177/0333102415584360 PubMed DOI
Niddam DM, Lai KL, Fuh JL, Chuang CYN, Chen WT, Wang SJ. Reduced functional connectivity between salience and visual networks in migraine with aura. Cephalalgia. (2016) 36:53–66. 10.1177/0333102415583144 PubMed DOI
Farago P, Tuka B, Toth E, Szabo N, Kiraly A, Csete G, et al. . Interictal brain activity differs in migraine with and without aura: resting state fMRI study. J Headache Pain. (2017) 18:8. 10.1186/s10194-016-0716-8 PubMed DOI PMC
Gawryluk JR, D'arcy RC, Mazerolle EL, Brewer KD, Beyea SD. Functional mapping in the corpus callosum: a 4T fMRI study of white matter. Neuroimage. (2011) 54:10–5. 10.1016/j.neuroimage.2010.07.028 PubMed DOI
Gawryluk JR, Mazerolle EL, D'arcy RC. Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions. Front Neurosci. (2014) 8:239. 10.3389/fnins.2014.00239 PubMed DOI PMC
Marussich L, Lu KH, Wen HG, Liu ZM. Mapping white-matter functional organization at rest and during naturalistic visual perception. Neuroimage. (2017) 146:1128–41. 10.1016/j.neuroimage.2016.10.005 PubMed DOI PMC
Peer M, Nitzan M, Bick AS, Levin N, Arzyt S. Evidence for functional networks within the human brain's white matter. J Neurosci. (2017) 37:6394–407. 10.1523/JNEUROSCI.3872-16.2017 PubMed DOI PMC
Ding ZH, Huang YL, Bailey SK, Gao YR, Cutting LE, Rogers BP, et al. . Detection of synchronous brain activity in white matter tracts at rest and under functional loading. Proc Natl Acad Sci USA. (2018) 115:595–600. 10.1073/pnas.1711567115 PubMed DOI PMC
Huang YL, Bailey SK, Wang PG, Cutting LE, Gore JC, Ding ZH. Voxel-wise detection of functional networks in white matter. Neuroimage. (2018) 183:544–52. 10.1016/j.neuroimage.2018.08.049 PubMed DOI PMC
Zhang Z, Liao M, Yao ZJ, Hu B, Xie YW, Zheng WH, et al. . Frequency-specific functional connectivity density as an effective biomarker for adolescent generalized anxiety disorder. Front Human Neurosci. (2017) 11:549. 10.3389/fnhum.2017.00549 PubMed DOI PMC
Cocozza S, Pontillo G, Quarantelli M, Sacca F, Riccio E, Costabile T, et al. . Default mode network modifications in Fabry disease: a resting-state fMRI study with structural correlations. Hum Brain Mapp. (2018) 39:1755–64. 10.1002/hbm.23949 PubMed DOI PMC
Jiang Y, Luo C, Li X, Li Y, Yang H, Li J, et al. . White-matter functional networks changes in patients with schizophrenia. Neuroimage. (2018) 190:172–81. 10.1016/j.neuroimage.2018.04.018 PubMed DOI
Szabo N, Kincses ZT, Pardutz A, Tajti J, Szok D, Tuka B, et al. . White matter microstructural alterations in migraine: a diffusion-weighted MRI study. Pain. (2012) 153:651–6. 10.1016/j.pain.2011.11.029 PubMed DOI
Szabo N, Farago P, Kiraly A, Vereb D, Csete G, Toth E, et al. . Evidence for plastic processes in migraine with aura: a diffusion weighted MRI study. Front Neuroanat. (2017) 11:138. 10.3389/fnana.2017.00138 PubMed DOI PMC
Gohel SR, Biswal BB. Functional integration between brain regions at rest occurs in multiple-frequency bands. Brain Connect. (2015) 5:23–34. 10.1089/brain.2013.0210 PubMed DOI PMC
Zhang Z, Liao W, Chen H, Mantini D, Ding JR, Xu Q, et al. . Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain. (2011) 134:2912–28. 10.1093/brain/awr223 PubMed DOI
Qi SL, Gao QJ, Shen J, Teng Y, Xie X, Sun YJ, et al. . Multiple frequency bands analysis of large scale intrinsic brain networks and its application in schizotypal personality disorder. Front Comput Neurosci. (2018) 12:64. 10.3389/fncom.2018.00064 PubMed DOI PMC
Shen YT, Li JY, Yuan YS, Wang XX, Wang M, Wang JW, et al. . Disrupted amplitude of low-frequency fluctuations and causal connectivity in Parkinson's disease with apathy. Neurosci Lett. (2018) 683:75–81. 10.1016/j.neulet.2018.06.043 PubMed DOI
Xiao F, Wang T, Gao L, Fang J, Sun Z, Xu H, et al. . Frequency-dependent changes of the resting BOLD signals predicts cognitive deficits in asymptomatic carotid artery stenosis. Front Neurosci. (2018) 12:416. 10.3389/fnins.2018.00416 PubMed DOI PMC
Smith SM. Fast robust automated brain extraction. Human Brain Mapping. (2002) 17:143–55. 10.1002/hbm.10062 PubMed DOI PMC
Beckmann CF, Deluca M, Devlin JT, Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Transac R Soc B Biol Sci. (2005) 360:1001–13. 10.1098/rstb.2005.1634 PubMed DOI PMC
Niazy RK, Xie JY, Miller K, Beckmann CF, Smith SM. Spectral characteristics of resting state networks. Slow Brain Oscillations Sleep Resting State Vigilance. (2011) 193:259–76. 10.1016/B978-0-444-53839-0.00017-X PubMed DOI
Ding ZH, Newton AT, Xu R, Anderson AW, Morgan VL, Gore JC. Spatio-temporal correlation tensors reveal functional structure in human brain. PLoS ONE. (2013) 8:82107. 10.1371/journal.pone.0082107 PubMed DOI PMC
Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. (2009) 44:83–98. 10.1016/j.neuroimage.2008.03.061 PubMed DOI
Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. (2002) 15:1–25. 10.1002/hbm.1058 PubMed DOI PMC
Gawryluk JR, Mazerolle EL, Beyea SD, D'arcy RC. Functional MRI activation in white matter during the Symbol Digit Modalities Test. Front Hum Neurosci. (2014) 8:589. 10.3389/fnhum.2014.00589 PubMed DOI PMC
Mazerolle EL, Beyea SD, Gawryluk JR, Brewer KD, Bowen CV, D'arcy RCN. Confirming white matter fMRI activation in the corpus callosum: co-localization with DTI tractography. Neuroimage. (2010) 50:616–21. 10.1016/j.neuroimage.2009.12.102 PubMed DOI
Rostrup E, Law I, Blinkenberg M, Larsson HBW, Born AP, Holm S, et al. . Regional differences in the CBF and BOLD responses to hypercapnia: a combined PET and fMRI study. Neuroimage. (2000) 11:87–97. 10.1006/nimg.1999.0526 PubMed DOI
Wu TL, Wang F, Anderson AW, Chen LM, Ding ZH, Gore JC. Effects of anesthesia on resting state BOLD signals in white matter of non-human primates. Magnetic Resonance Imag. (2016) 34:1235–41. 10.1016/j.mri.2016.07.001 PubMed DOI PMC
Fraser LM, Stevens MT, Beyea SD, D'arcy RCN. White versus gray matter: fMRI hemodynamic responses show similar characteristics, but differ in peak amplitude. BMC Neurosci. (2012) 13:91. 10.1186/1471-2202-13-91 PubMed DOI PMC
Courtemanche MJ, Sparrey CJ, Song XW, Mackay A, D'arcy RCN. Detecting white matter activity using conventional 3 Tesla fMRI: an evaluation of standard field strength and hemodynamic response function. Neuroimage. (2018) 169:145–50. 10.1016/j.neuroimage.2017.12.008 PubMed DOI
Li MW, Newton AT, Anderson AW, Ding ZH, Gore JC. Characterization of the hemodynamic response function in white matter tracts for event-related fMRI. Nat Commun. (2019) 10:1140. 10.1038/s41467-019-09076-2 PubMed DOI PMC
Nonaka H, Akima M, Hatori T, Nagayama T, Zhang Z, Ihara F. Microvasculature of the human cerebral white matter: arteries of the deep white matter. Neuropathology. (2003) 23:111–8. 10.1046/j.1440-1789.2003.00486.x PubMed DOI
Mozumder M, Pozo JM, Coelho S, Costantini M, Simpson J, Highley JR, et al. . Quantitative histomorphometry of capillary microstructure in deep white matter. Neuroimage Clin. (2019) 23:101839. 10.1016/j.nicl.2019.101839 PubMed DOI PMC
Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. (2001) 412:150–7. 10.1038/35084005 PubMed DOI
Helenius J, Perkio J, Soinne L, Ostergaard L, Carano RA, Salonen O, et al. . Cerebral hemodynamics in a healthy population measured by dynamic susceptibility contrast MR imaging. Acta Radiol. (2003) 44:538–46. 10.1034/j.1600-0455.2003.00104.x PubMed DOI
Brigo F, Storti M, Tezzon F, Manganotti P, Nardone R. Primary visual cortex excitability in migraine: a systematic review with meta-analysis. Neurol Sci. (2013) 34:819–30. 10.1007/s10072-012-1274-8 PubMed DOI
Bridge H, Stagg CJ, Near J, Lau CI, Zisner A, Cader MZ. Altered neurochemical coupling in the occipital cortex in migraine with visual aura. Cephalalgia. (2015) 35:1025–30. 10.1177/0333102414566860 PubMed DOI
Gonzalez De La Aleja J, Ramos A, Mato-Abad V, Martinez-Salio A, Hernandez-Tamames JA, Molina JA, et al. Higher glutamate to glutamine ratios in occipital regions in women with migraine during the interictal state. Headache. (2013) 53:365–75. 10.1111/head.12030 PubMed DOI
Tracey I. Imaging pain. Br J Anaesth. (2008) 101:32–9. 10.1093/bja/aen102 PubMed DOI
Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. . Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. (2005) 26:132–40. 10.1016/j.neuroimage.2005.01.028 PubMed DOI
Warbrick T, Rosenberg J, Shah NJ. The relationship between BOLD fMRI response and the underlying white matter as measured by fractional anisotropy (FA): a systematic review. Neuroimage. (2017) 153:369–81. 10.1016/j.neuroimage.2016.12.075 PubMed DOI