Abstract
Primary afferent terminals in the dorsal horn of the spinal cord release excitatory amino acid and peptide transmitters that initiate the central processing of nociceptive information1. The postsynaptic actions of amino acid transmitters on spinal neurons have been well characterized2, but the cellular basis of peptide actions remains unclear3. Substance P is the best characterized of the peptides present in sensory neurons and has been shown to depolarize dorsal horn neurons and to facilitate nociceptive reflexes4–7. To determine the mechanisms by which substance P contributes to afferent synaptic transmission, we have monitored the levels of intracellular calcium in single isolated rat dorsal horn neurons and report that substance P can produce a prolonged elevation in calcium concentration by mobilizing its release from intracellular stores. This elevation may contribute to the long-term changes in the excitable properties of dorsal horn neurons that occur following afferent fibre stimulation6. We have also found that L-glutamate elevates intracellular calcium in substance P-sensitive dorsal horn neurons by increasing calcium influx8,9. These results provide a direct demonstration of intracellular calcium changes in response to neuropeptides in mammalian central neurons. They also indicate that there is convergent regulation of intracellular calcium in dorsal horn neurons by two different classes of sensory transmitters that are co-released from the same afferent terminals.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Jahr, C. E. & Jessell, T. M. Adv. Pain Res. Therapy 9, 31–39 (1985).
Mayer, M. L. & Westbrook, G. L. Prog. Neurobiol 28, 197–276 (1987).
Jessell, T. M. & Womack, M. D. Trends Neurosci. 8, 43–45 (1985).
Murase, K. & Randic, M. J. Physiol., Lond. 346, 203–217 (1984).
Nowak, L. M. & MacDonald, R. L. J. Neurosci. 2, 1119–1128 (1982).
Woolf, C. & Wiesenfeld-Hallin, Z. Neurosci. Lett. 66, 226–230 (1986).
Cridland, R. A. & Henry, J. L. Brain Res. 381, 93–99 (1986).
MacDermott, A. B., Mayer, M. L., Westbrook, G. L., Smith, S. J. & Barker, J. L. Nature 321, 519–522 (1986).
Murphy, S. N., Thayer, S. A. & Miller, R. J. J. Neurosci. 7, 4145–4158 (1987).
Connor, J. A. & Hockberger, P. E. J. Neurosci. 7, 1384–1400 (1987).
Tsien, R. Y. & Rink, T. J. Curr. Meth. cell. Neurobiol. 3, 249–312 (1983).
Scanlon, M., Williams, D. A. & Fay, F. S. J. biol. Chem. 262, 6308–6312 1987).
Almers, W. & Neher, E. FEBS Lett. 192, 15–18 (1985).
Lee, C-M., Campbell, N. J., Williams, B. J. & Iversen, L. L. Eur. J. Pharmac. 130, 209–217 (1986).
Womack, M. D., Hanley, M. R. & Jessell, T. M. J. Neurosci. 5, 3370–3378 (1986).
Payan, D. G. Biochem. biophys. Res. Commun. 130, 104–109 (1985).
Masu, Y. et al. Nature 329, 834–836 (1987).
DeBiasi, S., VanEyck, S. L., Petruz, P. & Rustioni, A. Am. Soc. Neurosci. Abstr. 13, 1563 (1987).
Hanley, M. R., Lee, C. M., Jones, L. M. & Michell, R. H. Molec. Pharmac. 18, 78–83 (1980).
Mantyh, P. W., Pinnock, R. D., Downes, C. P., Goedert, M. & Hunt, S. P. Nature 309, 795–797 (1984).
Worley, P. F., Baraban, J. M., Colvin, J. S. & Snyder, S. H. Nature 325, 159–161 (1987).
Mayer, M. L., MacDermott, A. B., Westbrook, G. L., Smith, S. J. & Barker, J. L. J. Neurosci. 7, 3230–3244 (1987).
Schwindt, P. C. & Crill, W. E. J. Neurophysiol. 46, 1–16 (1981).
Owen, D. G., Segal, M. & Barker, J. L. Nature 311, 567–570 (1984).
Yoshimura, M., Polosa, C. & Nishi, S. J. Neurophysiology 55, 1234–1246 (1986).
Blair, L. E. & Dionne, V. E. Nature 315, 329–331 (1985).
Hunt, S. P., Pini, A. & Evan, G. Nature 328, 632–634 (1987).
Morgan, J. I. & Curran, T. Nature 322, 552–555 (1986).
Wall, P. D. & Fitzgerald, M. CIBA Fdn Symp. 91, 249–260 (1982).
Kay, A. R. & Wong, R. K. S. J. Neurosci. Meth. 16, 227–238 (1986).
Romijn, H. J., Habets, A. M. M. C., Mud, M. T. & Wolters, P. S. Devl Brain Res. 2, 583–589 (1982).
Grynkiewicz, G., Poenie, M. & Tsien, R. Y. J. biol. Chem. 260, 3440–3450 (1985).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Womack, M., MacDermott, A. & Jessell, T. Sensory transmitters regulate intracellular calcium in dorsal horn neurons. Nature 334, 351–353 (1988). https://doi.org/10.1038/334351a0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/334351a0
This article is cited by
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.