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Direct electrophysiological evidence that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura and a review of the spreading depolarization continuum of acute neuronal mass injury.
Geroscience. 2020 02; 42(1):57-80.G

Abstract

Spreading depolarization is observed as a large negative shift of the direct current potential, swelling of neuronal somas, and dendritic beading in the brain's gray matter and represents a state of a potentially reversible mass injury. Its hallmark is the abrupt, massive ion translocation between intraneuronal and extracellular compartment that causes water uptake (= cytotoxic edema) and massive glutamate release. Dependent on the tissue's energy status, spreading depolarization can co-occur with different depression or silencing patterns of spontaneous activity. In adequately supplied tissue, spreading depolarization induces spreading depression of activity. In severely ischemic tissue, nonspreading depression of activity precedes spreading depolarization. The depression pattern determines the neurological deficit which is either spreading such as in migraine aura or migraine stroke or nonspreading such as in transient ischemic attack or typical stroke. Although a clinical distinction between spreading and nonspreading focal neurological deficits is useful because they are associated with different probabilities of permanent damage, it is important to note that spreading depolarization, the neuronal injury potential, occurs in all of these conditions. Here, we first review the scientific basis of the continuum of spreading depolarizations. Second, we highlight the transition zone of the continuum from reversibility to irreversibility using clinical cases of aneurysmal subarachnoid hemorrhage and cerebral amyloid angiopathy. These illustrate how modern neuroimaging and neuromonitoring technologies increasingly bridge the gap between basic sciences and clinic. For example, we provide direct electrophysiological evidence for the first time that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura.

Authors+Show Affiliations

Center for Stroke Research, Campus Charité Mitte, Charité University Medicine Berlin, Charitéplatz 1, 10117, Berlin, Germany. Department of Experimental Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. Department of Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.Center for Stroke Research, Campus Charité Mitte, Charité University Medicine Berlin, Charitéplatz 1, 10117, Berlin, Germany. Department of Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.Center for Stroke Research, Campus Charité Mitte, Charité University Medicine Berlin, Charitéplatz 1, 10117, Berlin, Germany. Department of Experimental Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.Department of Neuroradiology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.Solution Centre for Image Guided Local Therapies (STIMULATE), Otto-von-Guericke-University, Magdeburg, Germany.Evangelisches Krankenhaus Oldenburg, University of Oldenburg, Oldenburg, Germany.Center for Stroke Research, Campus Charité Mitte, Charité University Medicine Berlin, Charitéplatz 1, 10117, Berlin, Germany. Department of Experimental Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. Department of Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.Center for Stroke Research, Campus Charité Mitte, Charité University Medicine Berlin, Charitéplatz 1, 10117, Berlin, Germany. jens.dreier@charite.de. Department of Experimental Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. jens.dreier@charite.de. Department of Neurology, Charité-Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. jens.dreier@charite.de. Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany. jens.dreier@charite.de. Einstein Center for Neurosciences Berlin, Berlin, Germany. jens.dreier@charite.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Review

Language

eng

PubMed ID

31820363

Citation

Major, Sebastian, et al. "Direct Electrophysiological Evidence That Spreading Depolarization-induced Spreading Depression Is the Pathophysiological Correlate of the Migraine Aura and a Review of the Spreading Depolarization Continuum of Acute Neuronal Mass Injury." GeroScience, vol. 42, no. 1, 2020, pp. 57-80.
Major S, Huo S, Lemale CL, et al. Direct electrophysiological evidence that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura and a review of the spreading depolarization continuum of acute neuronal mass injury. Geroscience. 2020;42(1):57-80.
Major, S., Huo, S., Lemale, C. L., Siebert, E., Milakara, D., Woitzik, J., Gertz, K., & Dreier, J. P. (2020). Direct electrophysiological evidence that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura and a review of the spreading depolarization continuum of acute neuronal mass injury. GeroScience, 42(1), 57-80. https://doi.org/10.1007/s11357-019-00142-7
Major S, et al. Direct Electrophysiological Evidence That Spreading Depolarization-induced Spreading Depression Is the Pathophysiological Correlate of the Migraine Aura and a Review of the Spreading Depolarization Continuum of Acute Neuronal Mass Injury. Geroscience. 2020;42(1):57-80. PubMed PMID: 31820363.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Direct electrophysiological evidence that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura and a review of the spreading depolarization continuum of acute neuronal mass injury. AU - Major,Sebastian, AU - Huo,Shufan, AU - Lemale,Coline L, AU - Siebert,Eberhard, AU - Milakara,Denny, AU - Woitzik,Johannes, AU - Gertz,Karen, AU - Dreier,Jens P, Y1 - 2019/12/09/ PY - 2019/10/28/received PY - 2019/11/20/accepted PY - 2019/12/11/pubmed PY - 2021/4/28/medline PY - 2019/12/11/entrez KW - Cerebral amyloid angiopathy KW - Delayed cerebral ischemia KW - Migraine aura KW - Spreading depression KW - Subarachnoid hemorrhage SP - 57 EP - 80 JF - GeroScience JO - Geroscience VL - 42 IS - 1 N2 - Spreading depolarization is observed as a large negative shift of the direct current potential, swelling of neuronal somas, and dendritic beading in the brain's gray matter and represents a state of a potentially reversible mass injury. Its hallmark is the abrupt, massive ion translocation between intraneuronal and extracellular compartment that causes water uptake (= cytotoxic edema) and massive glutamate release. Dependent on the tissue's energy status, spreading depolarization can co-occur with different depression or silencing patterns of spontaneous activity. In adequately supplied tissue, spreading depolarization induces spreading depression of activity. In severely ischemic tissue, nonspreading depression of activity precedes spreading depolarization. The depression pattern determines the neurological deficit which is either spreading such as in migraine aura or migraine stroke or nonspreading such as in transient ischemic attack or typical stroke. Although a clinical distinction between spreading and nonspreading focal neurological deficits is useful because they are associated with different probabilities of permanent damage, it is important to note that spreading depolarization, the neuronal injury potential, occurs in all of these conditions. Here, we first review the scientific basis of the continuum of spreading depolarizations. Second, we highlight the transition zone of the continuum from reversibility to irreversibility using clinical cases of aneurysmal subarachnoid hemorrhage and cerebral amyloid angiopathy. These illustrate how modern neuroimaging and neuromonitoring technologies increasingly bridge the gap between basic sciences and clinic. For example, we provide direct electrophysiological evidence for the first time that spreading depolarization-induced spreading depression is the pathophysiological correlate of the migraine aura. SN - 2509-2723 UR - https://www.unboundmedicine.com/medline/citation/31820363/Direct_electrophysiological_evidence_that_spreading_depolarization-induced_spreading_depression_is_the_pathophysiological_correlate_of_the_migraine_aura_and_a_review_of_the_spreading_depolarization_continuum_of_acute_neuronal_mass_injury. L2 - https://doi.org/10.1007/s11357-019-00142-7 DB - PRIME DP - Unbound Medicine ER -