Shedding light on migraine with aura: the clarifying role of advanced neuroimaging investigations

References

• Noseda R, Burstein R. Migraine pathophysiology: anatomy of the trigeminovascular pathway and associated neurological symptoms, cortical spreading depression, sensitization, and modulation of pain. Pain. 2013;154(Suppl. 1):S44–S53.
   PubMed Web of Science ®Google Scholar
• Viana M, Sances G, Linde M, et al. Clinical features of migraine aura: results from a prospective diary-aided study. Cephalalgia. 2017;37(10):979–989.
   PubMed Web of Science ®Google Scholar
• Becker WJ. The premonitory phase of migraine and migraine management. Cephalalgia. 2013;33:1117–1121.
   PubMed Web of Science ®Google Scholar
• Viana M, Linde M, Sances G, et al. Migraine aura symptoms: duration, succession and temporal relationship to headache. Cephalalgia. 2016;36(5):413–421.
   PubMed Web of Science ®Google Scholar
• Hansen JM, Goadsby PJ, Charles AC. Variability of clinical features in attacks of migraine with aura. Cephalalgia. 2016;36(3):216–224.
   PubMed Web of Science ®Google Scholar
• Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain. 1994;117(Pt 1):199–210.
   PubMed Web of Science ®Google Scholar
• Leão AA. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–390.
   Google Scholar
• Leão AA, Morison RS. Propagation of spreading cortical depression. J Neurophysiol. 1945;8:33–45.
   Web of Science ®Google Scholar
• Hansen AJ, Zeuthen T. Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol Scand. 1981;113:437–445.
   PubMedGoogle Scholar
• Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med. 2011;17:439–447.
   PubMed Web of Science ®Google Scholar
• Ramadan NM. Glutamate and migraine: from Ikeda to the 21st century. Cephalalgia. 2014;34:86–89.
   PubMed Web of Science ®Google Scholar
• Sarrouilhe D, Dejean C, Mesnil M. Involvement of gap junction channels in the pathophysiology of migraine with aura. Front Physiol. 2014;5:78.
   PubMed Web of Science ®Google Scholar
• Ayata C, Shin HK, Salomone S, et al. Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab. 2004;24:1172–1182.
   PubMed Web of Science ®Google Scholar
• Pietrobon D, Moskowitz MA. Pathophysiology of migraine. Annu Rev Physiol. 2013;75:365–391.
   PubMed Web of Science ®Google Scholar
• Borgdorff P. Arguments against the role of cortical spreading depression in migraine. Neurol Res. 2018;40(3):173–181.
   PubMed Web of Science ®Google Scholar
• Yokota C, Kuge Y, Hasegawa Y, et al. Unique profile of spreading depression in a primate model. J Cereb Blood Flow Metab. 2002;22:835–842.
   PubMed Web of Science ®Google Scholar
• Anttila V, Winsvold BS, Gormley P, et al. Genome-wide meta-analysis identifies new susceptibility loci for migraine. Nat Genet. 2013;45(8):912–991.
   PubMed Web of Science ®Google Scholar
• Ulrich V, Gervil M, Kyvik KO, et al. Evidence of a genetic factor in migraine with aura: a population-based Danish twin study. Ann Neurol. 1999;45(2):242–246.
   PubMed Web of Science ®Google Scholar
• Puledda F, Messina R, Goadsby PJ. An update on migraine: current understanding and future directions. J Neurol. 2017;264(9):2031–2039.
   PubMed Web of Science ®Google Scholar
• Charles A, Brennan K. Cortical spreading depression-new insights and persistent questions. Cephalalgia. 2009;29(10):1115–1124.
   PubMed Web of Science ®Google Scholar
• Karatas H, Erdener SE, Gursoy-Ozdemir Y, et al. Spreading depression triggers headache by activating neuronal Panx1 channels. Science. 2013;339(6123):1092–1095.
   PubMed Web of Science ®Google Scholar
• Olesen J, Larsen B, Lauritzen M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann Neurol. 1981;9(4):344–352.
   PubMed Web of Science ®Google Scholar
• Cutrer FM, Sorensen AG, Weisskoff RM, et al. Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann Neurol. 1998;43(1):25–31.
   PubMed Web of Science ®Google Scholar
• Goadsby PJ. The vascular theory of migraine–a great story wrecked by the facts. Brain. 2009;132(Pt 1):6–7.
   PubMedGoogle Scholar
• Headache Classification Committee of the International Headache Society (IHS). The international classification of headache disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629–808.
   PubMed Web of Science ®Google Scholar
• Aurora SK, Cao Y, Bowyer SM, et al. The occipital cortex is hyperexcitable in migraine: experimental evidence. Headache. 1999;39(7):469–476.
   PubMed Web of Science ®Google Scholar
• Coppola G, Pierelli F, Schoenen J. Is the cerebral cortex hyperexcitable or hyperresponsive in migraine? Cephalalgia. 2007;27:1427–1439.
   PubMed Web of Science ®Google Scholar
• Ambrosini A, Schoenen J. Electrophysiological response patterns of primary sensory cortices in migraine. J Headache Pain. 2006;7:377–388.
   PubMedGoogle Scholar
• DeLange JM, Cutrer FM. Our evolving understanding of migraine with aura. Curr Pain Headache Rep. 2014;18(10):453.
   PubMed Web of Science ®Google Scholar
• Hadjikhani N, Sanchez Del Rio M, Wu O. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A. 2001 10;98(8):4687–4692.
   PubMed Web of Science ®Google Scholar
• Cao Y, Welch KM, Aurora S, et al. Functional MRI-BOLD of visually triggered headache in patients with migraine. Arch Neurol. 1999;56(5):548–554.
   PubMed Web of Science ®Google Scholar
• Arngrim N, Hougaard A, Ahmadi K, et al. Heterogenous migraine aura symptoms correlate with visual cortex functional magnetic resonance imaging responses. Ann Neurol. 2017;82(6):925–939.
   PubMed Web of Science ®Google Scholar
• Martín H. Sánchez del Río M, de Silanes CL et al. Photoreactivity of the occipital cortex measured by functional magnetic resonance imaging-blood oxygenation level dependent in migraine patients and healthy volunteers: pathophysiological implications. Headache. 2011;51(10):1520–1528.
   PubMed Web of Science ®Google Scholar
• Montagna P, Pierangeli G, Cortelli P. The primary headaches as a reflection of genetic darwinian adaptive behavioral responses. Headache. 2010;50(2):273–289.
   PubMed Web of Science ®Google Scholar
• Cortelli P, Pierangeli G, Montagna P. Is migraine a disease? Neurol Sci. 2010;31(Suppl 1):S29–31.
   PubMedGoogle Scholar
• Datta R, Aguirre GK, Hu S, et al. Interictal cortical hyperresponsiveness in migraine is directly related to the presence of aura. Cephalalgia. 2013;33(6):365–374.
   PubMed Web of Science ®Google Scholar
• Sarchielli P, Tarducci R, Presciutti O, et al. Functional 1H-MRS findings in migraine patients with and without aura assessed interictally. Neuroimage. 2005 15;24(4):1025–1031.
   PubMed Web of Science ®Google Scholar
• Huang J, Cooper TG, Satana B, et al. Visual distortion provoked by a stimulus in migraine associated with hyperneuronal activity. Headache. 2003;43:664–671.
   PubMed Web of Science ®Google Scholar
• Huang J, Zong X, Wilkins A, et al. fMRI evidence that precision ophthalmic tints reduce cortical hyperactivation in migraine. Cephalalgia. 2011;31:925–936.
   PubMed Web of Science ®Google Scholar
• Arngrim N, Hougaard A, Schytz HW, et al. Effect of hypoxia on BOLD fMRI response and total cerebral blood flow in migraine with aura patients. J Cereb Blood Flow Metab. 2017;1. doi:10.1177/0271678X17719430.
   Google Scholar
• Hougaard A, Amin FM, Hoffmann MB, et al. Interhemispheric differences of fMRI responses to visual stimuli in patients with side-fixed migraine aura. Hum Brain Mapp. 2014;35(6):2714–2723.
   PubMed Web of Science ®Google Scholar
• Tedeschi G, Russo A, Conte F, et al. Increased interictal visual network connectivity in patients with migraine with aura. Cephalalgia. 2016;36(2):139–147.
   PubMed Web of Science ®Google Scholar
• Vinogradova LV. Initiation of spreading depression by synaptic and network hyperactivity: insights into trigger mechanisms of migraine aura. Cephalalgia. 2018;38(6):1177–1187.
   PubMed Web of Science ®Google Scholar
• Granziera C, DaSilva AF, Snyder J, et al. Anatomical alterations of the visual motion processing network in migraine with and without aura. PLoS Med. 2006;3(10):e402.
   PubMed Web of Science ®Google Scholar
• Gaist D, Hougaard A, Garde E, et al. Migraine with visual aura associated with thicker visual cortex. Brain. 2018;141:776–785.
   PubMed Web of Science ®Google Scholar
• Russo A, Silvestro M, Tessitore A, et al. The conundrum of relationship between pain and visual pathway in migraine with aura. Neurol Sci. 2018;39(Suppl 1):75–76.
   PubMedGoogle Scholar
• Hougaard A, Amin FM, Christensen CE, et al. Increased brainstem perfusion, but no blood-brain barrier disruption, during attacks of migraine with aura. Brain. 2017 1;140(6):1633–1642.
   PubMed Web of Science ®Google Scholar
• Hougaard A, Amin FM, Larsson HB, et al. Increased intrinsic brain connectivity between pons and somatosensory cortex during attacks of migraine with aura. Hum Brain Mapp. 2017;38(5):2635–2642.
   PubMed Web of Science ®Google Scholar
• Hadjikhani N, Ward N, Boshyan J, et al. The missing link: enhanced functional connectivity between amygdala and visceroceptive cortex in migraine. Cephalalgia. 2013;33(15):1264–1268.
   PubMed Web of Science ®Google Scholar
• Stankewitz A, May A. Increased limbic and brainstem activity during migraine attacks following olfactory stimulation. Neurology. 2011;77(2011):476–482.
   PubMedGoogle Scholar
• Afridi SK, Matharu MS, Lee L, et al. A PET study exploring the laterality of brainstem activation in migraine using glyceryl trinitrate. Brain. 2005;128(2005):932–939.
   PubMedGoogle Scholar
• Prescot A, Becerra L, Pendse G, et al. Excitatory neurotransmitters in brain regions in interictal migraine patients. Mol Pain. 2009;5(2009):34.
   PubMedGoogle Scholar
• Gehrmann J, Mies G, Bonnekoh P, et al. Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol. 1993;3(1):11–17.
   PubMed Web of Science ®Google Scholar
• Albrecht D, Mainero C, Ichijo E, et al. Imaging of neuroinflammation in migraine with aura - a [11C] PBR28 PET/MR study. Neurology. Forthcoming 2019;92:e2038-e2050.
   PubMed Web of Science ®Google Scholar
• Granziera C, Daducci A, Romascano D, et al. Structural abnormalities in the thalamus of migraineurs with aura: a multiparametric study at 3 T. Cerebellum. 2013;12(6):812–818.
   PubMedGoogle Scholar
• DaSilva AF, Granziera C, Snyder J, et al. Thickening in the somatosensory cortex of patients with migraine. Neurology. 2007 20;69(21):1990–1995.
   PubMed Web of Science ®Google Scholar
• Messina R, Rocca MA, Colombo B, et al. Cortical abnormalities in patients with migraine: a surface-based analysis. Radiology. 2013;268(1):170–180.
   PubMed Web of Science ®Google Scholar
• Hougaard A, Amin FM, Arngrim N, et al. Sensory migraine aura is not associated with structural grey matter abnormalities. Neuroimage Clin. 2016;17(11):322–327.
   Google Scholar
• Hougaard A, Amin FM, Hoffmann MB, et al. Structural gray matter abnormalities in migraine relate to headache lateralization, but not aura. Cephalalgia. 2015;35(1):3–9.
   PubMed Web of Science ®Google Scholar
• Datta R, Detre JA, Aguirre GK, et al. Absence of changes in cortical thickness in patients with migraine. Cephalalgia. 2011;31(14):1452–1458.
   PubMed Web of Science ®Google Scholar
• Russo A, Tessitore A, Silvestro M, et al. Advanced visual network hyperresponsiveness to trigeminal nociception in migraine with aura. J Headache Pain. 2019 3;20(1): 46.
   PubMedGoogle Scholar
• Petrusic I, Pavlovski V, Savkovic Z, et al. Addenbrooke’s cognitive examination test for brief cognitive assessment of adolescents suffering from migraine with aura. Acta Neurol Belg. 2017;117(1):97–102.
   PubMed Web of Science ®Google Scholar
• Lo Buono V, Bonanno L, Corallo F, et al. Cognitive functions and psychological symptoms in migraine: a study on patients with and without aura. Int J Neurosci. 2019;129(6):588–592.
   PubMed Web of Science ®Google Scholar
• Russo A, Tessitore A, Giordano A, et al. Executive resting-state network connectivity in migraine without aura. Cephalalgia. 2012;32(14):1041–1048.
   PubMed Web of Science ®Google Scholar
• Tessitore A, Russo A, Conte F, et al. Abnormal connectivity within executive resting-state network in migraine with aura. Headache. 2015;55(6):794–805.
   PubMed Web of Science ®Google Scholar
• Borsook D, Maleki N, Becerra L, et al. Understanding migraine through the lens of maladaptive stress responses: a model disease of allostatic load. Neuron. 2012;73(2):219–234.
   PubMed Web of Science ®Google Scholar
• Niddam DM, Lai KL, Fuh JL, et al. Reduced functional connectivity between salience and visual networks in migraine with aura. Cephalalgia. 2016;36(1):53–66.
   PubMed Web of Science ®Google Scholar
• Schankin CJ, Maniyar FH, Sprenger T, et al. The relation between migraine, typical migraine aura and “visual snow”. Headache. 2014;54(6):957–966.
   PubMed Web of Science ®Google Scholar
• Petrusic I, Viana M, Dakovic M, et al. Proposal for a migraine aura complexity score. Cephalalgia. 2019;39(6):732–741.
   PubMed Web of Science ®Google Scholar
• Yang H, Zhang J, Liu Q, et al. Multimodal MRI-based classification of migraine: using deep learning convolutional neural network. Biomed Eng Online. 2018 11;17(1):138.
   PubMedGoogle Scholar