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      Migraine Aura: Retracting Particle-Like Waves in Weakly Susceptible Cortex

      research-article
      1 , 2 , 3 , * , 4 , 5
      PLoS ONE
      Public Library of Science

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          Abstract

          Cortical spreading depression (SD) has been suggested to underlie migraine aura. Despite a precise match in speed, the spatio-temporal patterns of SD observed in animal cortex and aura symptoms mapped to the cortical surface ordinarily differ in aspects of size and shape. We show that this mismatch is reconciled by utilizing that both pattern types bifurcate from an instability point of generic reaction-diffusion models. To classify these spatio-temporal pattern we suggest a susceptibility scale having the value σ = 1 at the instability point. We predict that human cortex is only weakly susceptible to SD (σ<1), and support this prediction by directly matching visual aura symptoms with anatomical landmarks using fMRI retinotopic mapping. Moreover, we use retinal SD to give a proof of concept of the existence of this instability point and describe how cortical susceptibility to SD must be adjusted for migraine drug testing. Close to the instability point at σ = 1 the dynamical repertoire of cortical tissue is increased. As a consequence, the picture of an engulfing SD that became paradigmatic for migraine with aura needs to be modified in most cases towards a more spatially confined pattern that remains within the originating major gyrus or sulcus. Furthermore, we discuss the resulting implications on migraine pharmacology that is hitherto tested in the regime (σ>1), and potentially silent aura occurring below a second bifurcation point at σ = 0 on the susceptible scale.

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          Most cited references62

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          Mechanisms of spreading depression and hypoxic spreading depression-like depolarization.

          G Somjen (2001)
          Spreading depression (SD) and the related hypoxic SD-like depolarization (HSD) are characterized by rapid and nearly complete depolarization of a sizable population of brain cells with massive redistribution of ions between intracellular and extracellular compartments, that evolves as a regenerative, "all-or-none" type process, and propagates slowly as a wave in brain tissue. This article reviews the characteristics of SD and HSD and the main hypotheses that have been proposed to explain them. Both SD and HSD are composites of concurrent processes. Antagonists of N-methyl-D-aspartate (NMDA) channels or voltage-gated Na(+) or certain types of Ca(2+) channels can postpone or mitigate SD or HSD, but it takes a combination of drugs blocking all known major inward currents to effectively prevent HSD. Recent computer simulation confirmed that SD can be produced by positive feedback achieved by increase of extracellular K(+) concentration that activates persistent inward currents which then activate K(+) channels and release more K(+). Any slowly inactivating voltage and/or K(+)-dependent inward current could generate SD-like depolarization, but ordinarily, it is brought about by the cooperative action of the persistent Na(+) current I(Na,P) plus NMDA receptor-controlled current. SD is ignited when the sum of persistent inward currents exceeds persistent outward currents so that total membrane current turns inward. The degree of depolarization is not determined by the number of channels available, but by the feedback that governs the SD process. Short bouts of SD and HSD are well tolerated, but prolonged depolarization results in lasting loss of neuron function. Irreversible damage can, however, be avoided if Ca(2+) influx into neurons is prevented.
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            Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging.

            The borders of human visual areas V1, V2, VP, V3, and V4 were precisely and noninvasively determined. Functional magnetic resonance images were recorded during phase-encoded retinal stimulation. This volume data set was then sampled with a cortical surface reconstruction, making it possible to calculate the local visual field sign (mirror image versus non-mirror image representation). This method automatically and objectively outlines area borders because adjacent areas often have the opposite field sign. Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys. Retinotopically organized visual areas in humans extend anteriorly to overlap several areas previously shown to be activated by written words.
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              SPREADING DEPRESSION OF ACTIVITY IN THE CEREBRAL CORTEX

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2009
                1 April 2009
                : 4
                : 4
                : e5007
                Affiliations
                [1 ]Institut für Theoretische Physik, Technische Universität Berlin, Berlin, Germany
                [2 ]Klinik für Neurologie II, Otto-von-Guericke-Universität Magdeburg, Magdeburg, Germany
                [3 ]Leibniz Institute für Neurobiologie, Magdeburg, Germany
                [4 ]Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts, United States of America
                [5 ]Brain Mind Institute, EPFL, Lausanne, Switzerland
                Tel Aviv University, Israel
                Author notes

                Conceived and designed the experiments: MAD NH. Performed the experiments: MAD NH. Analyzed the data: MAD. Contributed reagents/materials/analysis tools: MAD NH. Wrote the paper: MAD NH.

                Article
                08-PONE-RA-05594R1
                10.1371/journal.pone.0005007
                2659426
                19337363
                6ee53003-85f0-460e-aadd-ac086109b77f
                Dahlem et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 21 July 2008
                : 6 February 2009
                Page count
                Pages: 9
                Categories
                Research Article
                Biophysics/Theory and Simulation
                Mathematics/Nonlinear Dynamics
                Neuroscience/Theoretical Neuroscience
                Physiology/Pattern Formation
                Neurological Disorders/Headache
                Neurological Disorders/Neuroimaging
                Pathology/Pathophysiology
                Pharmacology/Drug Development
                Radiology and Medical Imaging/Magnetic Resonance Imaging

                Uncategorized
                Uncategorized

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