Evidence for Plastic Processes in Migraine with Aura: A Diffusion Weighted MRI Study

. 2017 ; 11 () : 138. [epub] 20180117

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29387002

Background: Formerly white matter abnormalities in a mixed group of migraine patients with and without aura were shown. Here, we aimed to explore white matter alterations in a homogeneous group of migraineurs with aura and to delineate possible relationships between white matter changes and clinical variables. Methods: Eighteen patients with aura, 25 migraine patients without aura and 28 controls were scanned on a 1.5T MRI scanner. Diffusivity parameters of the white matter were estimated and compared between patients' groups and controls using whole-brain tract-based spatial statistics. Results: Decreased radial diffusivity (p < 0.036) was found bilaterally in the parieto-occipital white matter, the corpus callosum, and the cingular white matter of migraine with aura (MwA) patients compared to controls. Migraine without aura (MwoA) patients showed no alteration compared to controls. MwA compared to MwoA showed increased fractional anisotropy (p < 0.048) in the left parieto-occipital white matter. In MwA a negative correlation was found between axial diffusivity and disease duration in the left superior longitudinal fascicle (left parieto-occipital region) and in the left corticospinal tract (p < 0.036) and with the number of the attacks in the right superior longitudinal fascicle (p < 0.048). Conclusion: We showed for the first time that there are white matter microstructural differences between these two subgroups of migraine and hence it is important to handle the two groups separately in further researches. We propose that degenerative and maladaptive plastic changes coexist in the disease and the diffusion profile is a result of these processes.

Zobrazit více v PubMed

Afra J., Proietti Cecchini A., Sandor P. S., Schoenen J. (2000). Comparison of visual and auditory evoked cortical potentials in migraine patients between attacks. Clin. Neurophysiol. 111 1124–1129. 10.1016/S1388-2457(00)00271-6 PubMed DOI

Akhtari M., Salamon N., Duncan R., Fried I., Mathern G. W. (2006). Electrical conductivities of the freshly excised cerebral cortex in epilepsy surgery patients; correlation with pathology, seizure duration, and diffusion tensor imaging. Brain Topogr. 18 281–290. 10.1007/s10548-006-0006-x PubMed DOI

Antal A., Temme J., Nitsche M. A., Varga E. T., Lang N., Paulus W. (2005). Altered motion perception in migraineurs: evidence for interictal cortical hyperexcitability. Cephalalgia 25 788–794. 10.1111/j.1468-2982.2005.00949.x PubMed DOI

Aurora S. K., Ahmad B. K., Welch K. M., Bhardhwaj P., Ramadan N. M. (1998). Transcranial magnetic stimulation confirms hyperexcitability of occipital cortex in migraine. Neurology 50 1111–1114. 10.1212/WNL.50.4.1111 PubMed DOI

Ayata C. (2010). Cortical spreading depression triggers migraine attack: pro. Headache 50 725–730. 10.1111/j.1526-4610.2010.01647.x PubMed DOI

Ayata C., Lauritzen M. (2015). Spreading depression, spreading depolarizations, and the cerebral vasculature. Physiol. Rev. 95 953–993. 10.1152/physrev.00027.2014 PubMed DOI PMC

Barrio-Arranz G., de Luis-Garcia R., Tristan-Vega A., Martin-Fernandez M., Aja-Fernandez S. (2015). Impact of MR acquisition parameters on DTI scalar indexes: a tractography based approach. PLOS ONE 10:e0137905. 10.1371/journal.pone.0137905 PubMed DOI PMC

Benitez A., Fieremans E., Jensen J. H., Falangola M. F., Tabesh A., Ferris S. H., et al. (2014). White matter tract integrity metrics reflect the vulnerability of late-myelinating tracts in Alzheimer’s disease. Neuroimage Clin. 4 64–71. 10.1016/j.nicl.2013.11.001 PubMed DOI PMC

Blumenfeld-Katzir T., Pasternak O., Dagan M., Assaf Y. (2011). Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLOS ONE 6:e20678. 10.1371/journal.pone.0020678 PubMed DOI PMC

Boyke J., Driemeyer J., Gaser C., Buchel C., May A. (2008). Training-induced brain structure changes in the elderly. J. Neurosci. 28 7031–7035. 10.1523/JNEUROSCI.0742-08.2008 PubMed DOI PMC

Brienza M., Pujia F., Colaiacomo M. C., Anastasio M. G., Pierelli F., Di Biasi C., et al. (2014). 3T diffusion tensor imaging and electroneurography of peripheral nerve: a morphofunctional analysis in carpal tunnel syndrome. J. Neuroradiol. 41 124–130. 10.1016/j.neurad.2013.06.001 PubMed DOI

Brighina F., Bolognini N., Cosentino G., Maccora S., Paladino P., Baschi R., et al. (2015). Visual cortex hyperexcitability in migraine in response to sound-induced flash illusions. Neurology 84 2057–2061. 10.1212/WNL.0000000000001584 PubMed DOI

Brigo F., Storti M., Nardone R., Fiaschi A., Bongiovanni L. G., Tezzon F., et al. (2012). Transcranial magnetic stimulation of visual cortex in migraine patients: a systematic review with meta-analysis. J. Headache Pain 13 339–349. 10.1007/s10194-012-0445-6 PubMed DOI PMC

Chadaide Z., Arlt S., Antal A., Nitsche M. A., Lang N., Paulus W. (2007). Transcranial direct current stimulation reveals inhibitory deficiency in migraine. Cephalalgia 27 833–839. 10.1111/j.1468-2982.2007.01337.x PubMed DOI

Charles A., Brennan K. (2009). Cortical spreading depression-new insights and persistent questions. Cephalalgia 29 1115–1124. 10.1111/j.1468-2982.2009.01983.x PubMed DOI PMC

Chong C. D., Schwedt T. J. (2015). Migraine affects white-matter tract integrity: A diffusion-tensor imaging study. Cephalalgia 35 1162–1171. 10.1177/0333102415573513 PubMed DOI

Coppola G., Bracaglia M., Di Lenola D., Di Lorenzo C., Serrao M., Parisi V., et al. (2015). Visual evoked potentials in subgroups of migraine with aura patients. J. Headache Pain 16:92. 10.1186/s10194-015-0577-6 PubMed DOI PMC

Cosentino G., Fierro B., Brighina F. (2014). From different neurophysiological methods to conflicting pathophysiological views in migraine: a critical review of literature. Clin. Neurophysiol. 125 1721–1730. 10.1016/j.clinph.2014.05.005 PubMed DOI

Dai Z., Zhong J., Xiao P., Zhu Y., Chen F., Pan P., et al. (2015). Gray matter correlates of migraine and gender effect: a meta-analysis of voxel-based morphometry studies. Neuroscience 299 88–96. 10.1016/j.neuroscience.2015.04.066 PubMed DOI

DaSilva A. F., Granziera C., Tuch D. S., Snyder J., Vincent M., Hadjikhani N. (2007). Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 18 301–305. 10.1097/WNR.0b013e32801776bb PubMed DOI PMC

Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., May A. (2004). Neuroplasticity: changes in grey matter induced by training. Nature 427 311–312. 10.1038/427311a PubMed DOI

Farago P., Tuka B., Toth E., Szabo N., Kiraly A., Csete G., et al. (2017). Interictal brain activity differs in migraine with and without aura: resting state fMRI study. J Headache Pain 18:8. 10.1186/s10194-016-0716-8 PubMed DOI PMC

Gawel M., Connolly J. F., Rose F. C. (1983). Migraine patients exhibit abnormalities in the visual evoked potential. Headache 23 49–52. 10.1111/j.1526-4610.1983.hed2302049.x PubMed DOI

Granziera C., DaSilva A. F., Snyder J., Tuch D. S., Hadjikhani N. (2006). Anatomical alterations of the visual motion processing network in migraine with and without aura. PLOS Med. 3:e402. 10.1371/journal.pmed.0030402 PubMed DOI PMC

Granziera C., Romascano D., Daducci A., Roche A., Vincent M., Krueger G., et al. (2013). Migraineurs without aura show microstructural abnormalities in the cerebellum and frontal lobe. Cerebellum 12 812–818. 10.1007/s12311-013-0491-x PubMed DOI

Gregory S., Cole J. H., Farmer R. E., Rees E. M., Roos R. A., Sprengelmeyer R., et al. (2015). Longitudinal diffusion tensor imaging shows progressive changes in white matter in Huntington’s disease. J. Huntingtons Dis. 4 333–346. 10.3233/JHD-150173 PubMed DOI

Hadjikhani N., Sanchez Del Rio M., Wu O., Schwartz D., Bakker D., Fischl B., et al. (2001). Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. U.S.A. 98 4687–4692. 10.1073/pnas.071582498 PubMed DOI PMC

Hamilton M. (1960). A rating scale for depression. J. Neurol. Neurosurg. Psychiatry 23 56–62. 10.1136/jnnp.23.1.56 PubMed DOI PMC

Headache Classification Committee of the International Headache Society (2013). The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 33 629–808. 10.1177/0333102413485658 PubMed DOI

Heckel A., Weiler M., Xia A., Ruetters M., Pham M., Bendszus M., et al. (2015). Peripheral nerve diffusion tensor imaging: assessment of axon and myelin sheath integrity. PLOS ONE 10:e0130833. 10.1371/journal.pone.0130833 PubMed DOI PMC

Jenkinson M., Smith S. (2001). A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5 143–156. 10.1016/S1361-8415(01)00036-6 PubMed DOI

Kim J. H., Budde M. D., Liang H. F., Klein R. S., Russell J. H., Cross A. H., et al. (2006). Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol. Dis. 21 626–632. 10.1016/j.nbd.2005.09.009 PubMed DOI

Kim J. H., Suh S. I., Seol H. Y., Oh K., Seo W. K., Yu S. W., et al. (2008). Regional grey matter changes in patients with migraine: a voxel-based morphometry study. Cephalalgia 28 598–604. 10.1111/j.1468-2982.2008.01550.x PubMed DOI

Kincses Z. T., Szabo N., Toth E., Zadori D., Farago P., Nemeth D., et al. (2013). Diffusion MRI measured white matter microstructure as a biomarker of neurodegeneration in preclinical Huntington’s disease. Ideggyogy. Sz 66 399–405. PubMed

Landman B. A., Farrell J. A., Jones C. K., Smith S. A., Prince J. L., Mori S. (2007). Effects of diffusion weighting schemes on the reproducibility of DTI-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T. Neuroimage 36 1123–1138. 10.1016/j.neuroimage.2007.02.056 PubMed DOI

Lauritzen M. (1987). Cerebral blood flow in migraine and cortical spreading depression. Acta Neurol. Scand. Suppl. 113 1–40. 10.1111/j.1600-0404.1987.tb07881.x PubMed DOI

Lauritzen M. (1994). Pathophysiology of the migraine aura. The spreading depression theory. Brain 117(Pt 1) 199–210. 10.1093/brain/117.1.199 PubMed DOI

Lerch J. P., Yiu A. P., Martinez-Canabal A., Pekar T., Bohbot V. D., Frankland P. W., et al. (2011). Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning. Neuroimage 54 2086–2095. 10.1016/j.neuroimage.2010.09.086 PubMed DOI

Longoni M., Ferrarese C. (2006). Inflammation and excitotoxicity: role in migraine pathogenesis. Neurol. Sci. 27(Suppl. 2) S107–S110. 10.1007/s10072-006-0582-2 PubMed DOI

Manzoni G. C., Torelli P. (2008). Migraine with and without aura: a single entity? Neurol. Sci. 29(Suppl. 1) S40–S43. 10.1007/s10072-008-0884-7 PubMed DOI

May A. (2009). Morphing voxels: the hype around structural imaging of headache patients. Brain 132(Pt 6) 1419–1425. 10.1093/brain/awp116 PubMed DOI

Messina R., Rocca M. A., Colombo B., Pagani E., Falini A., Comi G., et al. (2015). White matter microstructure abnormalities in pediatric migraine patients. Cephalalgia 35 1278–1286. 10.1177/0333102415578428 PubMed DOI

Moskowitz M. A. (2007). Pathophysiology of headache–past and present. Headache 47(Suppl. 1) S58–S63. 10.1111/j.1526-4610.2007.00678.x PubMed DOI

Neeb L., Bastian K., Villringer K., Gits H. C., Israel H., Reuter U., et al. (2015). No microstructural white matter alterations in chronic and episodic migraineurs: a case-control diffusion tensor magnetic resonance imaging study. Headache 55 241–251. 10.1111/head.12496 PubMed DOI

Nichols T. E., Holmes A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 15 1–25. 10.1002/hbm.1058 PubMed DOI PMC

Petrusic I., Zidverc-Trajkovic J. (2014). Cortical spreading depression: origins and paths as inferred from the sequence of events during migraine aura. Funct. Neurol. 29 207–212. PubMed PMC

Pierelli F., Iacovelli E., Bracaglia M., Serrao M., Coppola G. (2013). Abnormal sensorimotor plasticity in migraine without aura patients. Pain 154 1738–1742. 10.1016/j.pain.2013.05.023 PubMed DOI

Pierpaoli C., Barnett A., Pajevic S., Chen R., Penix L. R., Virta A., et al. (2001). Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 13(6 Pt. 1) 1174–1185. 10.1006/nimg.2001.0765S1053811901907657 PubMed DOI

Ranson R., Igarashi H., MacGregor E. A., Wilkinson M. (1991). The similarities and differences of migraine with aura and migraine without aura: a preliminary study. Cephalalgia 11 189–192. 10.1046/j.1468-2982.1991.1104189.x PubMed DOI

Rocca M. A., Ceccarelli A., Falini A., Tortorella P., Colombo B., Pagani E., et al. (2006). Diffusion tensor magnetic resonance imaging at 3.0 tesla shows subtle cerebral grey matter abnormalities in patients with migraine. J. Neurol. Neurosurg. Psychiatry 77 686–689. 10.1136/jnnp.2005.080002 PubMed DOI PMC

Rocca M. A., Colombo B., Inglese M., Codella M., Comi G., Filippi M. (2003). A diffusion tensor magnetic resonance imaging study of brain tissue from patients with migraine. J. Neurol. Neurosurg. Psychiatry 74 501–503. 10.1136/jnnp.74.4.501 PubMed DOI PMC

Rocca M. A., Messina R., Colombo B., Falini A., Comi G., Filippi M. (2014). Structural brain MRI abnormalities in pediatric patients with migraine. J. Neurol. 261 350–357. 10.1007/s00415-013-7201-y PubMed DOI

Rocca M. A., Pagani E., Colombo B., Tortorella P., Falini A., Comi G., et al. (2008). Selective diffusion changes of the visual pathways in patients with migraine: a 3-T tractography study. Cephalalgia 28 1061–1068. 10.1111/j.1468-2982.2008.01655.x PubMed DOI

Sampaio-Baptista C., Khrapitchev A. A., Foxley S., Schlagheck T., Scholz J., Jbabdi S., et al. (2013). Motor skill learning induces changes in white matter microstructure and myelination. J. Neurosci. 33 19499–19503. 10.1523/JNEUROSCI.3048-13.2013 PubMed DOI PMC

Sand T., Zhitniy N., White L. R., Stovner L. J. (2008). Visual evoked potential latency, amplitude and habituation in migraine: a longitudinal study. Clin. Neurophysiol. 119 1020–1027. 10.1016/j.clinph.2008.01.009 PubMed DOI

Sas K., Pardutz A., Toldi J., Vecsei L. (2010). Dementia, stroke and migraine–some common pathological mechanisms. J. Neurol. Sci. 299 55–65. 10.1016/j.jns.2010.08.001 PubMed DOI

Schmidt-Wilcke T., Ganssbauer S., Neuner T., Bogdahn U., May A. (2008). Subtle grey matter changes between migraine patients and healthy controls. Cephalalgia 28 1–4. 10.1111/j.1468-2982.2007.01428.x PubMed DOI

Schmitz N., Admiraal-Behloul F., Arkink E. B., Kruit M. C., Schoonman G. G., Ferrari M. D., et al. (2008). Attack frequency and disease duration as indicators for brain damage in migraine. Headache 48 1044–1055. 10.1111/j.1526-4610.2008.01133.x PubMed DOI

Scholz J., Klein M. C., Behrens T. E., Johansen-Berg H. (2009). Training induces changes in white-matter architecture. Nat. Neurosci. 12 1370–1371. 10.1038/nn.2412 PubMed DOI PMC

Shatillo A., Koroleva K., Giniatullina R., Naumenko N., Slastnikova A. A., Aliev R. R., et al. (2013). Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system. Neuroscience 253 341–349. 10.1016/j.neuroscience.2013.09.002 PubMed DOI

Smith S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17 143–155. 10.1002/hbm.10062 PubMed DOI PMC

Smith S. M., Jenkinson M., Woolrich M. W., Beckmann C. F., Behrens T. E., Johansen-Berg H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl. 1) S208–S219. 10.1016/j.neuroimage.2004.07.051 PubMed DOI

Smith S. M., Johansen-Berg H., Jenkinson M., Rueckert D., Nichols T. E., Miller K. L., et al. (2007). Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat. Protoc. 2 499–503. 10.1038/nprot.2007.45 PubMed DOI

Smith S. M., Nichols T. E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44 83–98. 10.1016/j.neuroimage.2008.03.061 PubMed DOI

Sun S. W., Liang H. F., Trinkaus K., Cross A. H., Armstrong R. C., Song S. K. (2006). Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 55 302–308. 10.1002/mrm.20774 PubMed DOI

Szabo N., Kincses Z. T., Pardutz A., Tajti J., Szok D., Tuka B., et al. (2012). White matter microstructural alterations in migraine: a diffusion-weighted MRI study. Pain 153 651–656. 10.1016/j.pain.2011.11.029 PubMed DOI

Tedeschi G., Russo A., Conte F., Corbo D., Caiazzo G., Giordano A., et al. (2016). Increased interictal visual network connectivity in patients with migraine with aura. Cephalalgia 36 139–147. 10.1177/0333102415584360 PubMed DOI

Teepker M., Munk K., Mylius V., Haag A., Moller J. C., Oertel W. H., et al. (2009). Serum concentrations of s100b and NSE in migraine. Headache 49 245–252. 10.1111/j.1526-4610.2008.01228.x PubMed DOI

Teutsch S., Herken W., Bingel U., Schoell E., May A. (2008). Changes in brain gray matter due to repetitive painful stimulation. Neuroimage 42 845–849. 10.1016/j.neuroimage.2008.05.044 PubMed DOI

Valfre W., Rainero I., Bergui M., Pinessi L. (2008). Voxel-based morphometry reveals gray matter abnormalities in migraine. Headache 48 109–117. 10.1111/j.1526-4610.2007.00723.x PubMed DOI

Wang C., Paling D., Chen L., Hatton S. N., Lagopoulos J., Aw S. T., et al. (2015). Axonal conduction in multiple sclerosis: a combined magnetic resonance imaging and electrophysiological study of the medial longitudinal fasciculus. Mult. Scler. 21 905–915. 10.1177/1352458514556301 PubMed DOI

Wedeen V. J., Hagmann P., Tseng W. Y., Reese T. G., Weisskoff R. M. (2005). Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 54 1377–1386. 10.1002/mrm.20642 PubMed DOI

Yilmaz N., Karaali K., Ozdem S., Turkay M., Unal A., Dora B. (2011). Elevated S100B and neuron specific enolase levels in patients with migraine-without aura: evidence for neurodegeneration? Cell Mol. Neurobiol. 31 579–585. 10.1007/s10571-011-9651-z PubMed DOI PMC

Yu D., Yuan K., Qin W., Zhao L., Dong M., Liu P., et al. (2013). Axonal loss of white matter in migraine without aura: a tract-based spatial statistics study. Cephalalgia 33 34–42. 10.1177/0333102412466964 PubMed DOI

Yuan K., Qin W., Liu P., Zhao L., Yu D., Zhao L., et al. (2012). Reduced fractional anisotropy of corpus callosum modulates inter-hemispheric resting state functional connectivity in migraine patients without aura. PLOS ONE 7:e45476. 10.1371/journal.pone.0045476 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...