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Volume 17, Number 15, Issue of August 1, 1997 pp. 5921-5927
Copyright ©1997 Society for Neuroscience

Noxious Cutaneous Thermal Stimuli Induce a Graded Release of Endogenous Substance P in the Spinal Cord: Imaging Peptide Action In Vivo

Received Feb. 4, 1997; revised May 12, 1997; accepted May 15, 1997.

Brian J. Allen^{1, 3}, Scott D. Rogers^{1, 3}, Joseph R. Ghilardi^{1, 3}, Patrick M. Menning^{1, 3}, Michael A. Kuskowski², Allan I. Basbaum⁴, Donald A. Simone³, and Patrick W. Mantyh^{1, 3}

¹ Molecular Neurobiology Laboratory and ² Geriatric Research, Education and Clinical Center, Veterans Affairs Medical Center, Minneapolis, Minnesota 55417, ³ Department of Psychiatry, University of Minnesota, Minneapolis, Minnesota 55455, and ⁴ Department of Anatomy and Physiology, University of California, San Francisco, San Francisco, California 94143

Dorsal root ganglia (DRG) neurons synthesize and transport substance P (SP) to the spinal cord where it is released in response to intense noxious somatosensory stimuli. We have shown previously that SP release in vivo causes a rapid and reversible internalization of SP receptors (SPRs) in dorsal horn neurons, which may provide a pharmacologically specific image of neurons activated by SP. Here, we report that noxious heat (43°, 48°, and 55°C) and cold (10°, 0°, 10°, and 20°C) stimuli, but not innocuous warm (38°C) and cold (20°C) stimuli, applied to the hindpaw of anesthetized rats induce SPR internalization in spinal cord neurons that is graded with respect to the intensity of the thermal stimulus. Thus, with increasing stimulus intensities, both the total number of SPR+ lamina I neurons showing SPR internalization and the number of internalized SPR+ endosomes within each SPR immunoreactive neuron showed a significant increase. These data suggest that thermal stimuli induce a graded release of SP from primary afferent terminals and that agonist dependent receptor endocytosis provides evidence of a spatially and pharmacologically unique "neurochemical signature" after specific somatosensory stimuli.

Key words: substance P receptor; tachykinin; neurokinin-1; nociception; pain; sensory neuron

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