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Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain. | LitMetric

Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain.

Neuropharmacology

A.I. Virtanen Institute for Molecular Sciences, University of Eastern Finland, 70211, Kuopio, Finland; Laboratory of Neurobiology, Kazan Federal University, 420008, Kazan, Russia. Electronic address:

Published: April 2017

AI Article Synopsis

  • Serotonin (5-HT) significantly influences migraine pain by affecting the excitability of trigeminal afferents, which are crucial for pain signaling.
  • The study found that 5-HT can induce various firing patterns in nociceptive fibers, with different receptor antagonists either reducing or completely blocking its pro-nociceptive effects.
  • 5-HT shows both peripheral excitatory actions, such as increasing nociceptive firing and releasing CGRP, and central inhibitory effects that can mitigate pain signaling in the brainstem.

Article Abstract

Serotonergic mechanisms play a central role in migraine pathology. However, the region-specific effects of serotonin (5-HT) mediated via multiple types of receptors in the nociceptive system are poorly understood. Using extracellular and patch-clamp recordings, we studied the action of 5-HT on the excitability of peripheral and central terminals of trigeminal afferents. 5-HT evoked long-lasting TTX-sensitive firing in the peripheral terminals of meningeal afferents, the origin site of migraine pain. Cluster analysis revealed that in majority of nociceptive fibers 5-HT induced either transient or persistent spiking activity with prevailing delta and theta rhythms. The 5-HT3-receptor antagonist MDL-72222 or 5-HT1B/D-receptor antagonist GR127935 largely reduced, but their combination completely prevented the excitatory pro-nociceptive action of 5-HT. The 5-HT3 agonist mCPBG activated spikes in MDL-72222-dependent manner but the 5HT-1 receptor agonist sumatriptan did not affect the nociceptive firing. 5-HT also triggered peripheral CGRP release in meninges, which was blocked by MDL-72222.5-HT evoked fast membrane currents and Ca transients in a fraction of trigeminal neurons. Immunohistochemistry showed expression of 5-HT3A receptors in fibers innervating meninges. Endogenous release of 5-HT from degranulated mast cells increased nociceptive firing. Low pH but not histamine strongly activated firing. 5-HT reduced monosynaptic inputs from trigeminal Aδ- and C-afferents to the upper cervical lamina I neurons and this effect was blocked by MDL-72222. Consistent with central inhibitory effect, 5-HT reduced CGRP release in the brainstem slices. In conclusion, 5-HT evokes powerful pro-nociceptive peripheral and anti-nociceptive central effects in trigeminal system transmitting migraine pain.

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Source
http://dx.doi.org/10.1016/j.neuropharm.2016.12.024DOI Listing

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