Oxygen inhibits neuronal activation in the trigeminocervical complex after stimulation of trigeminal autonomic reflex, but not during direct dural activation of trigeminal afferents

Headache. 2009 Sep;49(8):1131-43. doi: 10.1111/j.1526-4610.2009.01501.x.

Abstract

Objective: To understand the mechanism of action of oxygen treatment in cluster headache.

Background: Trigeminal autonomic cephalalgias, including cluster headache, are characterized by unilateral head pain in association with ipsilateral cranial autonomic features. They are believed to involve activation of the trigeminovascular system and the parasympathetic outflow to the cranial vasculature from the superior salivatory nucleus (SuS) projections through the sphenopalatine ganglion, via the greater petrosal nerve of the VIIth (facial) cranial nerve. Cluster headache is remarkably responsive to treatment with oxygen, and yet our understanding of its mode of action is unknown.

Methods: Combining models of trigeminovascular nociception and a novel approach that activates the trigeminal-autonomic reflex, using SuS/facial nerve stimulation, we explored the effect of oxygen on trigeminal nerve activation as well as on autonomic responses through blood flow observations of the lacrimal duct/sac.

Results: Meningeal vasodilation and neuronal firing in the trigeminocervical complex (TCC), in response to dural electrical stimulation, was unaffected by treatment with 100% oxygen. Stimulation of the SuS via the facial nerve caused only marginal changes in dural blood vessel diameter, but did result in evoked firing in the TCC. Two populations of neurons were characterized, those responsive to 100% oxygen treatment, with a maximal inhibition of 33%, 20 minutes after the start of oxygen treatment (t(15) = 4.4, P < .0001). A second population of neurons were not inhibited by oxygen and tended to have shorter latency. Oxygen also inhibited evoked blood flow changes in the lacrimal sac/duct caused by SuS stimulation.

Conclusions: The data provide the first systematic, experimental evidence for a mechanism of action of oxygen in cluster headache. The data show oxygen has no direct effect on trigeminal afferents, acting specifically on the parasympathetic/facial nerve projections to the cranial vasculature to inhibit both evoked trigeminovascular activation and activation of the autonomic pathway during cluster headache attacks. Moreover, the studies begin to characterize a novel laboratory model for the most painful primary headache syndrome known--cluster headache.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Cerebral Arteries / innervation
  • Cerebral Arteries / physiopathology*
  • Cerebrovascular Circulation / physiology
  • Cluster Headache / drug therapy*
  • Cluster Headache / metabolism
  • Cluster Headache / physiopathology
  • Disease Models, Animal
  • Dura Mater / physiopathology
  • Electric Stimulation / adverse effects
  • Facial Nerve / anatomy & histology
  • Facial Nerve / physiopathology
  • Male
  • Oxygen / pharmacology*
  • Oxygen / therapeutic use
  • Parasympathetic Nervous System / anatomy & histology
  • Parasympathetic Nervous System / physiopathology
  • Rats
  • Rats, Sprague-Dawley
  • Reflex, Abnormal / drug effects*
  • Reflex, Abnormal / physiology
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / physiology
  • Trigeminal Caudal Nucleus / drug effects*
  • Trigeminal Caudal Nucleus / physiopathology
  • Trigeminal Nerve / drug effects*
  • Trigeminal Nerve / physiopathology
  • Vasodilation / drug effects
  • Vasodilation / physiology

Substances

  • Oxygen