The Glial Spike Theory. I. On an Active Role of Neuroglia in Spreading Depression and Migraine

The propagation mechanism of spreading depression (SD), which has been implicated in the pathophysiology of the neurological auras of migraine, remains enigmatic but is widely believed to depend primarily upon the behaviour of assemblies of neurons. It is proposed here, based upon a program of theor...

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Bibliographic Details
Published in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 1992-12, Vol.250 (1329), p.287-295
Main Author: Leibowitz, David H.
Format: Article
Language:English
Subjects:
Animals
Biological and medical sciences
Brain - physiology
Brain - physiopathology
Calcium
Cortical Spreading Depression
Depolarization
Depressive disorders
Humans
Medical sciences
Migraine
Migraine Disorders - physiopathology
Models, Neurological
Nerve tissue
Neuroglia
Neuroglia - physiology
Neurology
Neurons
Neurons - physiology
Phase velocity
Retina
Vascular diseases and vascular malformations of the nervous system
Wave propagation
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Summary:The propagation mechanism of spreading depression (SD), which has been implicated in the pathophysiology of the neurological auras of migraine, remains enigmatic but is widely believed to depend primarily upon the behaviour of assemblies of neurons. It is proposed here, based upon a program of theoretical research, that the most essential constituent of SD is a slowly propagating, regenerative event in the neuroglial compartment. By altering the neuronal microenvironment, this glial spike helps trigger and coordinate the neuronal depolarization of SD; the glial spike is in turn facilitated by neuronally released agents acting at the neuroglial plasma membrane. The conduction velocity-determining propagation mechanism of SD is further proposed to be a wave of intracellular Ca2+ -induced Ca2+ release (cytocal wave) that travels through the glial compartment of nervous tissue. Some implications for the improved understanding and clinical management of migraine are suggested. Excitability of glial cells of vertebrates has until now been demonstrated only in vitro, and its physiological significance has remained unknown. This work identifies a macroscopic reaction of neural tissue, known from the in vivo vertebrate brain for over 45 years, as a manifestation of neuroglial excitability.
ISSN:0962-8452
1471-2954
DOI:10.1098/rspb.1992.0161