Adult; Humans; Brain; Cerebrovascular Circulation; Perfusion; Migraine Disorders/diagnostic imaging; Migraine Disorders/therapy; Transcranial Direct Current Stimulation; Migraine Disorders; Multidisciplinary
Abstract :
[en] Cerebral blood flow differs between migraine patients and healthy controls during attack and the interictal period. This study compares the brain perfusion of episodic migraine patients and healthy controls and investigates the influence of anodal transcranial direct current stimulation (tDCS) over the occipital cortex. We included healthy adult controls and episodic migraineurs. After a 28-day baseline period and the baseline visit, migraine patients received daily active or sham anodal tDCS over the occipital lobe for 28 days. All participants underwent a MRI scan at baseline; migraineurs were also scanned shortly after the stimulation period and about five months later. At baseline, brain perfusion of migraine patients and controls differed in several areas; among the stimulated areas, perfusion was increased in the cuneus of healthy controls. At the first visit, the active tDCS group had an increased blood flow in regions processing visual stimuli and a decreased perfusion in other areas. Perfusion did not differ at the second follow-up visit. The lower perfusion level in migraineurs in the cuneus indicates a lower preactivation level. Anodal tDCS over the occipital cortex increases perfusion of several areas shortly after the stimulation period, but not 5 months later. An increase in the cortical preactivation level could mediate the transient reduction of the migraine frequency.Trial registration: NCT03237754 (registered at clincicaltrials.gov; full date of first trial registration: 03/08/2017).
Disciplines :
Neurology
Author, co-author :
Pohl, Heiko ; Department of Neurology, University Hospital Zurich, Zurich, Switzerland
Sandor, Peter S ; Department of Neurology, University Hospital Zurich, Zurich, Switzerland ; Department of Neurology and Neurorehabilitation, ZURZACH Care, Bad Zurzach, Switzerland
Moisa, Marius; Zurich Center for Neuroeconomics (ZNE), Department of Economics, University of Zurich, Zurich, Switzerland
Ruff, Christian C; Zurich Center for Neuroeconomics (ZNE), Department of Economics, University of Zurich, Zurich, Switzerland
Schoenen, Jean ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Luechinger, Roger ; Institute for Biomedical Engineering, ETH Zurich and University of Zurich, Zurich, Switzerland
O'Gorman, Ruth ; Center for MR-Research, University Children's Hospital, Zurich, Switzerland ; Children's Research Center, University Children's Hospital, Zurich, Switzerland
Riederer, Franz ; Department of Neurology, University Hospital Zurich, Zurich, Switzerland ; Department of Neurology, Clinic Hietzing, Vienna, Austria ; Karl Landsteiner Institute for Epilepsy Research and Cognitive Neurology, Vienna, Austria
Gantenbein, Andreas R ; Department of Neurology, University Hospital Zurich, Zurich, Switzerland ; Department of Neurology and Neurorehabilitation, ZURZACH Care, Bad Zurzach, Switzerland
Michels, Lars ; Department of Neuroradiology, Clinical Neuroscience Center, University Hospital Zurich, 8091, Zurich, Switzerland. Lars.michels@usz.ch ; Clinical Neuroscience Center, University Hospital Zurich, Zurich, Switzerland. Lars.michels@usz.ch ; Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology Zurich, Zurich, Switzerland. Lars.michels@usz.ch
Language :
English
Title :
Occipital transcranial direct current stimulation in episodic migraine patients: effect on cerebral perfusion.
HP was funded by the Werner Dessauer Stiftung. The funding source had no role in the design of this study, its execution, analyses, interpretation of the data, or decision to submit results.
Gil-Gouveia, R. & Martins, I. P. Clinical description of attack-related cognitive symptoms in migraine: A systematic review. Cephalalgia 38(7), 1335–1350. 10.1177/0333102417728250 (2018). DOI: 10.1177/0333102417728250
Borogovac, A. & Asllani, I. Arterial Spin Labeling (ASL) fMRI: Advantages, theoretical constrains, and experimental challenges in neurosciences. Int. J. Biomed. Imaging. 2012, 818456. 10.1155/2012/818456 (2012). DOI: 10.1155/2012/818456
Maniyar, F. H., Sprenger, T., Monteith, T., Schankin, C. & Goadsby, P. J. Brain activations in the premonitory phase of nitroglycerin-triggered migraine attacks. Brain 137(Pt 1), 232–241. 10.1093/brain/awt320 (2014). DOI: 10.1093/brain/awt320
Pollock, J. M. et al. Migraine associated cerebral hyperperfusion with arterial spin-labeled MR imaging. AJNR Am. J. Neuroradiol. 29(8), 1494–1497. 10.3174/ajnr.A1115 (2008). DOI: 10.3174/ajnr.A1115
Sanchez del Rio, M. et al. Perfusion weighted imaging during migraine: spontaneous visual aura and headache. Cephalalgia Int. J. Headache. 19(8), 701–707 (1999). DOI: 10.1046/j.1468-2982.1999.019008701.x
Cutrer, F. M. et al. Perfusion-weighted imaging defects during spontaneous migrainous aura. Ann. Neurol. 43(1), 25–31. 10.1002/ana.410430108 (1998). DOI: 10.1002/ana.410430108
Cutrer, F. M., O’Donnell, A. & Sanchez del Rio, M. Functional neuroimaging: Enhanced understanding of migraine pathophysiology. Neurology 55(9 Suppl 2), S36-45 (2000).
Hodkinson, D. J. et al. Primary somatosensory cortices contain altered patterns of regional cerebral blood flow in the interictal phase of migraine. PLoS ONE 10(9), e0137971. 10.1371/journal.pone.0137971 (2015). DOI: 10.1371/journal.pone.0137971
Michels, L. et al. Interictal hyperperfusion in the higher visual cortex in patients with episodic migraine. Headache 59(10), 1808–1820. 10.1111/head.13646 (2019). DOI: 10.1111/head.13646
Youssef, A. M. et al. In child and adult migraineurs the somatosensory cortex stands out … again: An arterial spin labeling investigation. Hum. Brain Mapp. 38(8), 4078–4087. 10.1002/hbm.23649 (2017). DOI: 10.1002/hbm.23649
Zhang, D. et al. Assessment of normalized cerebral blood flow and its connectivity with migraines without aura during interictal periods by arterial spin labeling. J. Headache Pain. 22(1), 72. 10.1186/s10194-021-01282-y (2021). DOI: 10.1186/s10194-021-01282-y
Aurora, S. K., Welch, K. M. & Al-Sayed, F. The threshold for phosphenes is lower in migraine. Cephalalgia 23(4), 258–263. 10.1046/j.1468-2982.2003.00471.x (2003). DOI: 10.1046/j.1468-2982.2003.00471.x
Battelli, L., Black, K. R. & Wray, S. H. Transcranial magnetic stimulation of visual area V5 in migraine. Neurology 58(7), 1066–1069 (2002). DOI: 10.1212/WNL.58.7.1066
Welch, K. M. Contemporary concepts of migraine pathogenesis. Neurology 61(8 Suppl 4), S2-8 (2003). DOI: 10.1212/WNL.61.8_suppl_4.S2
Jamil, A. et al. Current intensity- and polarity-specific online and aftereffects of transcranial direct current stimulation: An fMRI study. Hum. Brain Mapp. 41(6), 1644–1666. 10.1002/hbm.24901 (2020). DOI: 10.1002/hbm.24901
Ambrosini, A. et al. Correlation between habituation of visual-evoked potentials and magnetophosphene thresholds in migraine: A case-control study. Cephalalgia 36(3), 258–264. 10.1177/0333102415590241 (2016). DOI: 10.1177/0333102415590241
Coppola, G. et al. Pathophysiological targets for non-pharmacological treatment of migraine. Cephalalgia 36(12), 1103–1111. 10.1177/0333102415620908 (2016). DOI: 10.1177/0333102415620908
Pohl, H. et al. Long-term effects of self-administered transcranial direct current stimulation in episodic migraine prevention: Results of a randomized controlled trial. Neuromodul. Technol. Neural Interface. 10.1111/ner.13292 (2020). DOI: 10.1111/ner.13292
Vigano, A. et al. Transcranial direct current stimulation (tDCS) of the visual cortex: A proof-of-concept study based on interictal electrophysiological abnormalities in migraine. J. Headache Pain. 14, 23. 10.1186/1129-2377-14-23 (2013). DOI: 10.1186/1129-2377-14-23
Antal, A., Kriener, N., Lang, N., Boros, K. & Paulus, W. Cathodal transcranial direct current stimulation of the visual cortex in the prophylactic treatment of migraine. Cephalalgia 31(7), 820–828. 10.1177/0333102411399349 (2011). DOI: 10.1177/0333102411399349
Baschi, R. et al. EHMTI-0317. Transcranial direct current stimulation in chronic migraine: a pilot trial combining cathodal visual and anodal dlpfc stimulation. J. Headache Pain. 10.1186/1129-2377-15-s1-g4 (2014). DOI: 10.1186/1129-2377-15-s1-g4
Auvichayapat, P. et al. Transcranial direct current stimulation on prophylactic treatment in migraine patients, an open-label pilot study. Srinagarind Med. J. 27(1), 49–57 (2012).
Rocha, S. et al. Transcranial direct current stimulation in the prophylactic treatment of migraine based on interictal visual cortex excitability abnormalities: A pilot randomized controlled trial. J. Neurol. Sci. 349(1–2), 33–39. 10.1016/j.jns.2014.12.018 (2015). DOI: 10.1016/j.jns.2014.12.018
Ahdab, R. et al. Cathodal transcranial direct current stimulation of the occipital cortex in episodic migraine: A randomized sham-controlled crossover study. J. Clin. Med. 10.3390/jcm9010060 (2019). DOI: 10.3390/jcm9010060
Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edn. Cephalalgia. 38(1), 1–211 (2018). https://doi.org/10.1177/0333102417738202.
Stern, A. F. The hospital anxiety and depression scale. Occup. Med. (Lond). 64, 393–394 (2014). DOI: 10.1093/occmed/kqu024
Stewart, W. F. et al. Validity of the Migraine Disability Assessment (MIDAS) score in comparison to a diary-based measure in a population sample of migraine sufferers. Pain 88(1), 41–52 (2000). DOI: 10.1016/S0304-3959(00)00305-5
Nitsche, M. A. et al. Shaping the effects of transcranial direct current stimulation of the human motor cortex. J. Neurophysiol. 97(4), 3109–3117. 10.1152/jn.01312.2006 (2007). DOI: 10.1152/jn.01312.2006
Dai, W., Garcia, D., de Bazelaire, C. & Alsop, D. C. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn. Reson. Med. 60(6), 1488–1497. 10.1002/mrm.21790 (2008). DOI: 10.1002/mrm.21790
Weiger, M. et al. Sensitivity-encoded single-shot spiral imaging for reduced susceptibility artifacts in BOLD fMRI. Magn. Reson. Med. 48(5), 860–866. 10.1002/mrm.10286 (2002). DOI: 10.1002/mrm.10286
Wang, Z. et al. Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn. Reson. Imaging. 26(2), 261–269. 10.1016/j.mri.2007.07.003 (2008). DOI: 10.1016/j.mri.2007.07.003
Herscovitch, P. & Raichle, M. E. What is the correct value for the brain–blood partition coefficient for water?. J. Cereb. Blood Flow Metab. 5(1), 65–69. 10.1038/jcbfm.1985.9 (1985). DOI: 10.1038/jcbfm.1985.9
Lu, H., Clingman, C., Golay, X. & van Zijl, P. C. Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla. Magn. Reson. Med. 52(3), 679–682. 10.1002/mrm.20178 (2004). DOI: 10.1002/mrm.20178
Slotnick, S. D., Moo, L. R., Segal, J. B. & Hart, J. Jr. Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Res. Cogn. Brain Res. 17(1), 75–82 (2003). DOI: 10.1016/S0926-6410(03)00082-X
Slotnick, S. D. Cluster success: fMRI inferences for spatial extent have acceptable false-positive rates. Cogn. Neurosci. 8(3), 150–155. 10.1080/17588928.2017.1319350 (2017). DOI: 10.1080/17588928.2017.1319350
Olesen, J., Larsen, B. & Lauritzen, M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine. Ann. Neurol. 9(4), 344–352. 10.1002/ana.410090406 (1981). DOI: 10.1002/ana.410090406
Friberg, L., Olesen, J., Lassen, N. A., Olsen, T. S. & Karle, A. Cerebral oxygen extraction, oxygen consumption, and regional cerebral blood flow during the aura phase of migraine. Stroke 25(5), 974–979. 10.1161/01.str.25.5.974 (1994). DOI: 10.1161/01.str.25.5.974
Wolf, M. E. et al. Arterial spin labeling cerebral perfusion magnetic resonance imaging in migraine aura: An observational study. J. Stroke Cerebrovasc. Dis. 27(5), 1262–1266. 10.1016/j.jstrokecerebrovasdis.2017.12.002 (2018). DOI: 10.1016/j.jstrokecerebrovasdis.2017.12.002
Fu, T. et al. Cerebral blood flow alterations in migraine patients with and without aura: An arterial spin labeling study. J. Headache Pain. 23(1), 131. 10.1186/s10194-022-01501-0 (2022). DOI: 10.1186/s10194-022-01501-0
Corno, S. et al. The brain effect of the migraine attack: An ASL MRI study of the cerebral perfusion during a migraine attack. Neurol. Sci. 39(Suppl 1), 73–74. 10.1007/s10072-018-3346-x (2018). DOI: 10.1007/s10072-018-3346-x
Kato, Y., Araki, N., Matsuda, H., Ito, Y. & Suzuki, C. Arterial spin-labeled MRI study of migraine attacks treated with rizatriptan. J. Headache Pain. 11(3), 255–258. 10.1007/s10194-010-0215-2 (2010). DOI: 10.1007/s10194-010-0215-2
Giani, L. et al. Cerebral blood flow in migraine without aura: ASL-MRI case control study. Neurol. Sci. 40(Suppl 1), 183–184. 10.1007/s10072-019-03806-6 (2019). DOI: 10.1007/s10072-019-03806-6
de Tommaso, M. et al. Altered processing of sensory stimuli in patients with migraine. Nat. Rev. Neurol. 10(3), 144–155. 10.1038/nrneurol.2014.14 (2014). DOI: 10.1038/nrneurol.2014.14
Raichle, M. E. et al. A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98(2), 676–682. 10.1073/pnas.98.2.676 (2001). DOI: 10.1073/pnas.98.2.676
Masson, R. et al. Is migraine associated to brain anatomical alterations? New data and coordinate-based meta-analysis. Brain Topogr. 34(3), 384–401. 10.1007/s10548-021-00824-6 (2021). DOI: 10.1007/s10548-021-00824-6
Atasoy, S., Donnelly, I. & Pearson, J. Human brain networks function in connectome-specific harmonic waves. Nat. Commun. 7, 10340. 10.1038/ncomms10340 (2016). DOI: 10.1038/ncomms10340
Atasoy, S. et al. Connectome-harmonic decomposition of human brain activity reveals dynamical repertoire re-organization under LSD. Sci. Rep. 7(1), 17661. 10.1038/s41598-017-17546-0 (2017). DOI: 10.1038/s41598-017-17546-0
Weiller, C. et al. Brain stem activation in spontaneous human migraine attacks. Nat. Med. 1(7), 658–660. 10.1038/nm0795-658 (1995). DOI: 10.1038/nm0795-658
Afridi, S. K. et al. A positron emission tomographic study in spontaneous migraine. Arch. Neurol. 62(8), 1270–1275. 10.1001/archneur.62.8.1270 (2005). DOI: 10.1001/archneur.62.8.1270
Zheng, X., Alsop, D. C. & Schlaug, G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage 58(1), 26–33. 10.1016/j.neuroimage.2011.06.018 (2011). DOI: 10.1016/j.neuroimage.2011.06.018
Yang, Y. L., Deng, H. X., Xing, G. Y., Xia, X. L. & Li, H. F. Brain functional network connectivity based on a visual task: Visual information processing-related brain regions are significantly activated in the task state. Neural Regen. Res. 10(2), 298–307. 10.4103/1673-5374.152386 (2015). DOI: 10.4103/1673-5374.152386
