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Activation of Peripheral and Central Trigeminovascular Neurons by Seizure: Implications for Ictal and Postictal Headache.

Authors :
Melo-Carrillo A
Schain AJ
Strassman AM
Burstein R
Source :
The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2020 Jul 01; Vol. 40 (27), pp. 5314-5326. Date of Electronic Publication: 2020 Jun 11.
Publication Year :
2020

Abstract

An epileptic seizure can trigger a headache during (ictal) or after (postictal) the termination of the event. Little is known about the pathophysiology of seizure-induced headaches. In the current study, we determined whether a seizure can activate nociceptive pathways that carry pain signals from the meninges to the spinal cord, and if so, to what extent and through which classes of peripheral and central neurons. To achieve these goals, we used single-unit recording techniques and an established animal model of seizure (picrotoxin) to determine the effects of epileptic seizure on the activity of trigeminovascular Aδ-, C-, wide-dynamic range, and high-threshold neurons in male and female rats. Occurrence of seizure activated 54%, 50%, 68%, and 39% of the Aδ-, C-, wide-dynamic range, and high-threshold neurons, respectively. Regardless of their class, activated neurons exhibited a twofold to fourfold increase in their firing, which started immediately (1 min) or up to 90 min after seizure initiation, and lasted as short as 10 min or as long as 120 min. Administration of lidocaine to the dura prevented activation of all neuronal classes but not the initiation or maintenance of the seizure. These findings suggest that all neuronal classes may be involved in the initiation and maintenance of seizure-induced headache, and that their activation patterns can provide a neural substrate for explaining the timing and duration of ictal and possibly postictal headaches. By using seizure, which is evident in humans, this study bypasses controversies associated with cortical spreading depression, which is less readily observed in humans. SIGNIFICANCE STATEMENT This preclinical study provides a neural substrate for ictal and postictal headache. By studying seizure effects on the activity of peripheral (C and Aδ) and central (wide dynamic range and high-threshold) trigeminovascular neurons in intact and anesthetized dura, the findings help resolve two outstanding questions about the pathophysiology of headaches of intracranial origin. The first is that abnormal brain activity (i.e., seizure) that is evident in human (unlike cortical spreading depression) gives rise to specific and selective activation of the different components of the trigeminovascular system, and the second is that the activation of all components of the trigeminovascular pathway (i.e., peripheral and central neurons) depends on activation of the meningeal nociceptors from their receptors in the dura.<br /> (Copyright © 2020 the authors.)

Details

Language :
English
ISSN :
1529-2401
Volume :
40
Issue :
27
Database :
MEDLINE
Journal :
The Journal of neuroscience : the official journal of the Society for Neuroscience
Publication Type :
Academic Journal
Accession number :
32527981
Full Text :
https://doi.org/10.1523/JNEUROSCI.0283-20.2020