Abstract
We aimed to explore whether a migraine with aura (MA) is associated with structural changes in tracts of a white matter and to compare parameters of diffusivity between subgroups in migraineurs. Forty-three MA and 20 healthy subjects (HS), balanced by sex and age, were selected for this study. Analysis of diffusion tensor parameters was used to identify differences between MA patients and HS, and then between MA subgroups. A diffusion tensor probabilistic tractography analysis showed that there is no difference between MA patients and HS. However, using more-liberal uncorrected statistical threshold, we noted a trend in MA patients toward lower diffusivity indices of selected white matter tracts located in the forceps minor and right anterior thalamic radiation (ATR), superior longitudinal fasciculus (temporal part) (SLFT), cingulum-cingulate tract, and left uncinate fasciculus. Migraineurs who experienced somatosensory and dysphasic aura, besides visual symptoms, had tendency toward lower diffusivity indices, relative to migraineurs who experienced only visual symptoms, in the right inferior longitudinal fasciculus, forceps minor, and right superior longitudinal fasciculus (parietal part), SLFT, and cingulum-angular bundle. Aura frequency were negatively correlated with axial diffusivity and mean diffusivity of the right ATR (partial correlation = − 0.474; p = 0.002; partial correlation = − 0.460; p = 0.002), respectively. There were no significant differences between MA patients and HS, neither between MA subgroups. Migraineurs with abundant symptoms during the aura possibly have more myelinated fibers relative to those who experience only visual symptoms. Lower diffusivity indices of the right ATR are linked to more frequent migraine with aura attacks.
Similar content being viewed by others
References
Headache Classification Committee of the International Headache Society (IHS) (2018) The international classification of headache disorders, 3rd ed. Cephalalgia 38:1–211
Noseda R, Burstein R (2013) Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain. Pain 154:S44–S53
Hadjikhani N, Sanchez Del Rio M, Wu O et al (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci USA 98:4687–4692
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
Spreafico C, Frigerio R, Santoro P (2004) Visual evoked potentials in migraine. Neurol Sci 24:S288–S290
Rocca MA, Pagani E, Colombo B, Tortorella P, Falini A, Comi G, Filippi M (2008) Selective diffusion changes of the visual pathways in patients with migraine: a 3-T tractography study. Cephalalgia 28:1061–1068
DaSilva AF, Granziera C, Tuch DS, Snyder J, Vincent M, Hadjikhani N (2007) Interictal alterations of the trigeminal somatosensory pathway and periaqueductal gray matter in migraine. Neuroreport 18:301–305
Rocca MA, 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
Szabo N, Kincses ZT, Pardutz A et al (2012) White matter microstructural alterations in migraine: a diffusion weighted MRI study. Pain 153:651–656
Chong CD, Schwedt TJ (2015) Migraine affects white-matter tract integrity: a diffusion-tensor imaging study. Cephalalgia 35:1162–1171
Messina R, Rocca MA, Colombo B, Pagani E, Falini A, Comi G, Filippi M (2015) White matter microstructure abnormalities in pediatric migraine patients. Cephalalgia 35:1278–1286
Yendiki A, Panneck P, Srinivasan P et al (2011) Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinform 5:23
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis I: segmentation and surface reconstruction. Neuroimage 9:179–194
Behrens TEJ, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088
Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505
Jbabdi S, Woolrich MW, Andersson JL, Behrens TEJ (2007) A Bayesian framework for global tractography. NeuroImage 37:116–129
Yan J, Yonggang S, Liang Z et al (2014) Automatic clustering of white matter fibers in brain diffusion MRI with an application to genetics. Neuroimage 100:75–90
Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34:51–61
Magalhães R, Bourgin J, Boumezbeur F et al (2017) White matter changes in microstructure associated with a maladaptive response to stress in rats. Transl Psychiatry 7:e1009
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
Ding AY, Li Q, Zhou IY, Ma SJ, Tong G, McAlonan GM, Wu EX (2013) MR diffusion tensor imaging detects rapid microstructural changes in amygdala and hippocampus following fear conditioning in mice. PLoS One 8:e51704
Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15:528–536
Sampaio-Baptista C, Khrapitchev AA, Foxley S et al (2013) Motor skill learning induces changes in white matter microstructure and myelination. J Neurosci 33:19499–19503
Hofstetter S, Tavor I, Tzur Moryosef S, Assaf Y (2013) Short-term learning induces white matter plasticity in the fornix. J Neurosci 33:12844–12850
Petrusic I, Podgorac A, Zidverc-Trajkovic J, Radojicic A, Jovanovic Z, Sternic N (2016) Do interictal microembolic signals play a role in higher cortical dysfunction during migraine aura? Cephalalgia 36:561–567
Schain AJ, Melo-Carrillo A, Strassman AM, Burstein R (2017) Cortical spreading depression closes paravascular space and impairs glymphatic flow: implications for migraine headache. J Neurosci 37:2904–2915
Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex 44:953–961
Granziera C, Daducci A, Romascano D, Roche A, Helms G, Krueger G, Hadjikhani N (2014) Structural abnormalities in the thalamus of migraineurs with aura: a multiparametric study at 3 T. Hum Brain Mapp 35:1461–1468
Mamah D, Conturo TE, Harms MP et al (2010) Anterior thalamic radiation integrity in schizophrenia: a diffusion tensor imaging study. Psychiatry Res 183:144–150
Erpelding N, Davis KD (2013) Neural underpinnings of behavioural strategies that prioritize either cognitive task performance or pain. Pain 154:2060–2071
Charles AC, Baca SM (2013) Cortical spreading depression and migraine. Nat Rev Neurol 9:637–644
Gustin SM, Peck CC, Wilcox SL, Nash PG, Murray GM, Henderson LA (2011) Different pain, different brain: thalamic anatomy in neuropathic and non-neuropathic chronic pain syndromes. J Neurosci 31:5956–5964
Heilbronner SR, Haber SN (2014) Frontal cortical and subcortical projections provide a basis for segmenting the cingulum bundle: implications for neuroimaging and psychiatric disorders. J Neurosci 34:10041–10054
Adnan A, Barnett A, Moayedi M, McCormick C, Cohn M, McAndrews MP (2016) Distinct hippocampal functional networks revealed by tractography-based parcellation. Brain Struct Funct 221:2999–3012
Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6:533–544
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15:435–455
Acknowledgements
We thank Snezana Dikic for excellent technical MR scanning skills.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: IP and MD received research grant support from the Ministry of Education and Science, Republic of Serbia (project no. III 41005), and JZT received research grant support from the Ministry of Education and Science, Republic of Serbia (project no. 175022).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Rights and permissions
About this article
Cite this article
Petrušić, I., Daković, M., Kačar, K. et al. Migraine with aura and white matter tract changes. Acta Neurol Belg 118, 485–491 (2018). https://doi.org/10.1007/s13760-018-0984-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13760-018-0984-y