Cortical Spreading Depression and Migraine: Critical Review of a Neurophysiological Principle in the Third Millennium
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Abstract
Cortical spreading depression (CSD) is implicated in a diverse set of intracranial neurologic diseases and, in the early 21st Century, is generally believed to be the pathogenetic mechanism that underlies migraine. Except for malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury in humans, CSD has been recorded only in experimental animals. Primary “selfcycling” onset and spontaneous offset, as well as the other characteristic protean features or heterogeneity of migraine phenotype, are inexplicable through CSD. The magnesium-CSD-migraine nexus is untenable. CSD does not generate pain in experimental animals. CSD-induced in dural vasodilatation or neuro-inflammation is highly unlikely to generate lateralizing head or neck pain of migraine (unilateral, bilateral, side-shifting, or side-fixed) confined to the ophthalmic division of the trigeminal nerve (V1). Stress, missing a meal, alcohol consumption, or insufficient sleep are the most common precipitants of migraine but have no link to CSD. Post-stress migraine remains enigmatic with no link to CSD. Migraine selectively involves V1 rather than all three divisions of the trigeminal nerve, a feature inconsistent with generation or propagation, or both, of CSD. Precise and / or circadian onset of migraine attacks is indeterminate, clinically inaccessible, and unlinked to CSD. An initially adaptive, autonomic ocular storm is the apparent pathogenetic mechanism involving systemic and intrinsic brain vasopressinergic-serotonergic-noradrenergic nexus activation. This nexus possibly offers a “protective” effect that significantly delays migraine attacks. Vasopressin (AVP) surges rather than CSD generate early nausea/vomiting in migraineurs. Nausea/vomiting both characteristically release AVP and can, in turn, remit migraine. Photophobia is greater on the side of headache and CSD is unlikely to have a major role in its genesis. Neuroimaging has expanded the radiologic phenotype, but the cause-effect puzzle persists. Migraine with aura (MwA) is not associated with lateralizing abnormalities of cortical grey matter structure or function. Scintillating scotomata (SS) of migraine are not distributed homonymously and do not expand into the nasal visual fields. Eye cover, digital displacement of SS, synchronous movements of SS with the eyes, and determination of selective distribution in visual fields (temporal versus nasal, central versus peripheral) are important tests to determine its source. Displaceable non-homonymous eye movement synchronous nasal-field sparing SS absolutely cannot be cortical in origin or linked to CSD. Typical migraine headache and SS have not been reported after enucleation of eyes in a cohort of migraine patients with prior migraine attacks. Sightlessness markedly attenuates migrainous SS as well as photophobia. Atenolol and nadolol are first-line pharmacologic agents that prevent migraine but do not readily cross the blood-brain barrier (BBB) or affect CSD. Autonomic signs and symptoms are common in migraine but have no link with CSD. CSD has evolved into a landmark CNS physiological experimental phenomenon but has retarded meaningful progress in migraine research. A significant role for retinal spreading depression in SS cannot be excluded. A CNS adaptive or protective role for CSD is distinctly likely in experimental animals as well as in humans.
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