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The Journal of Neuroscience, November 26, 2003, 23(34):10988-10997

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Behavioral/Systems/Cognitive
Peptidergic Nociceptors of Both Trigeminal and Dorsal Root Ganglia Express Serotonin 1D Receptors: Implications for the Selective Antimigraine Action of Triptans

Sonja Potrebic,^1,4 * Andrew H. Ahn,^1,2,4 * Kate Skinner,^2,4 Howard L. Fields,^1,3,4 and Allan I. Basbaum^2,3,4

Departments of ¹Neurology, ²Anatomy, and ³Physiology and ⁴W. M. Keck Foundation Center for Integrative Neurosciences, University of California, San Francisco, San Francisco, California 94143

Agonists at serotonin 1D (5-HT_1D) receptors relieve migraine headache but are not clinically used as general analgesics. One possible explanation for this difference is that 5-HT_1D receptors are preferentially expressed by cranial afferents of the trigeminal system. We compared the distribution of 5-HT_1D receptor-immunoreactive (5-HT_1D-IR) peripheral afferents within the trigeminal ganglion (TRG) and lumbar dorsal root ganglion (DRG) of the rat. We also examined the neurochemical identity of 5-HT_1D-IR neurons with markers of primary afferent nociceptors, peripherin, isolectin B4, and substance P, and markers of myelinated afferents, N52 and SSEA3. We observed a striking similarity in the size, distribution, and neurochemical identity of 5-HT_1D-IR neurons in TRG and lumbar DRG afferents. Furthermore, the vast majority of 5-HT_1D-IR neurons are unmyelinated peptidergic afferents that distribute peripherally, including the dura, cornea, and the sciatic nerve. In the central projections of these afferents within the trigeminal nucleus caudalis and the spinal cord dorsal horn, 5-HT_1D-IR fibers are concentrated in laminas I and outer II; a few axons penetrate to lamina V. At the ultrastructural level, 5-HT_1D receptors in the spinal cord dorsal horn are localized exclusively within dense core vesicles of synaptic terminals. We observed scattered 5-HT_1D-IR neurons in the nodose ganglia, and there was sparse terminal immunoreactivity in the solitary nucleus. The visceral efferents of the superior cervical ganglia did not contain 5-HT_1D immunoreactivity. Our finding, that 5-HT_1D receptors are distributed in nociceptors throughout the body, raises the possibility that triptans can regulate not only headache-associated pain but also nociceptive responses in extracranial tissues.

Key words: serotonin receptor; substance P; migraine pain; trigeminal; dorsal root ganglion; ultrastructure

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Received June 30, 2003; revised September 26, 2003; accepted September 29, 2003.

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