Advertisement

Acta Neurologica Belgica

, Volume 118, Issue 3, pp 485–491 | Cite as

Migraine with aura and white matter tract changes

  • Igor Petrušić
  • Marko Daković
  • Katarina Kačar
  • Olivera Mićić
  • Jasna Zidverc-Trajković
Original Article

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.

Keywords

Migraine aura Dysphasia Probabilistic tractography analysis 

Notes

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).

Compliance with ethical standards

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.

References

  1. 1.
    Headache Classification Committee of the International Headache Society (IHS) (2018) The international classification of headache disorders, 3rd ed. Cephalalgia 38:1–211CrossRefGoogle Scholar
  2. 2.
    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–S53CrossRefPubMedGoogle Scholar
  3. 3.
    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 98:4687–4692CrossRefPubMedGoogle Scholar
  4. 4.
    Petrusic I, Zidverc-Trajkovic J (2014) Cortical spreading depression: origins and paths as inferred from the sequence of events during migraine aura. Funct Neurol 29:207–212PubMedPubMedCentralGoogle Scholar
  5. 5.
    Spreafico C, Frigerio R, Santoro P (2004) Visual evoked potentials in migraine. Neurol Sci 24:S288–S290CrossRefGoogle Scholar
  6. 6.
    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 28:1061–1068CrossRefPubMedGoogle Scholar
  7. 7.
    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 18:301–305CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Rocca MA, Messina R, Colombo B, Falini A, Comi G, Filippi M (2014) Structural brain MRI abnormalities in pediatric patients with migraine. J Neurol 261:350–357CrossRefPubMedGoogle Scholar
  9. 9.
    Szabo N, Kincses ZT, Pardutz A et al (2012) White matter microstructural alterations in migraine: a diffusion weighted MRI study. Pain 153:651–656CrossRefPubMedGoogle Scholar
  10. 10.
    Chong CD, Schwedt TJ (2015) Migraine affects white-matter tract integrity: a diffusion-tensor imaging study. Cephalalgia 35:1162–1171CrossRefPubMedGoogle Scholar
  11. 11.
    Messina R, Rocca MA, Colombo B, Pagani E, Falini A, Comi G, Filippi M (2015) White matter microstructure abnormalities in pediatric migraine patients. Cephalalgia 35:1278–1286CrossRefPubMedGoogle Scholar
  12. 12.
    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 5:23CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis I: segmentation and surface reconstruction. Neuroimage 9:179–194CrossRefPubMedGoogle Scholar
  14. 14.
    Behrens TEJ, Woolrich MW, Jenkinson M et al (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077–1088CrossRefPubMedGoogle Scholar
  15. 15.
    Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505CrossRefPubMedGoogle Scholar
  16. 16.
    Jbabdi S, Woolrich MW, Andersson JL, Behrens TEJ (2007) A Bayesian framework for global tractography. NeuroImage 37:116–129CrossRefPubMedGoogle Scholar
  17. 17.
    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 100:75–90CrossRefGoogle Scholar
  18. 18.
    Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34:51–61CrossRefPubMedGoogle Scholar
  19. 19.
    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:e1009CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    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:e20678CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    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:e51704CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15:528–536CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Sampaio-Baptista C, Khrapitchev AA, Foxley S et al (2013) Motor skill learning induces changes in white matter microstructure and myelination. J Neurosci 33:19499–19503CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Hofstetter S, Tavor I, Tzur Moryosef S, Assaf Y (2013) Short-term learning induces white matter plasticity in the fornix. J Neurosci 33:12844–12850CrossRefPubMedGoogle Scholar
  25. 25.
    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 36:561–567CrossRefPubMedGoogle Scholar
  26. 26.
    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 37:2904–2915CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex 44:953–961CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    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 35:1461–1468CrossRefPubMedGoogle Scholar
  29. 29.
    Mamah D, Conturo TE, Harms MP et al (2010) Anterior thalamic radiation integrity in schizophrenia: a diffusion tensor imaging study. Psychiatry Res 183:144–150CrossRefPubMedGoogle Scholar
  30. 30.
    Erpelding N, Davis KD (2013) Neural underpinnings of behavioural strategies that prioritize either cognitive task performance or pain. Pain 154:2060–2071CrossRefPubMedGoogle Scholar
  31. 31.
    Charles AC, Baca SM (2013) Cortical spreading depression and migraine. Nat Rev Neurol 9:637–644CrossRefPubMedGoogle Scholar
  32. 32.
    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 31:5956–5964CrossRefPubMedGoogle Scholar
  33. 33.
    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 34:10041–10054CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    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 221:2999–3012CrossRefPubMedGoogle Scholar
  35. 35.
    Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6:533–544CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15:435–455CrossRefPubMedGoogle Scholar

Copyright information

© Belgian Neurological Society 2018

Authors and Affiliations

  • Igor Petrušić
    • 1
    • 2
  • Marko Daković
    • 2
  • Katarina Kačar
    • 3
  • Olivera Mićić
    • 2
  • Jasna Zidverc-Trajković
    • 1
    • 4
  1. 1.Faculty of MedicineUniversity of BelgradeBelgradeSerbia
  2. 2.Faculty of Physical ChemistryUniversity of BelgradeBelgradeSerbia
  3. 3.Department of RadiologySpecial hospital for prevention and Treatment of Cerebrovascular Diseases “Sveti Sava”BelgradeSerbia
  4. 4.Center for headaches, Neurology ClinicClinical Center of SerbiaBelgradeSerbia

Personalised recommendations