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. 1985 Aug;365:59–75. doi: 10.1113/jphysiol.1985.sp015759

Two calcium-sensitive spike after-hyperpolarizations in visceral sensory neurones of the rabbit.

J C Fowler, R Greene, D Weinreich
PMCID: PMC1192989  PMID: 4040969

Abstract

Intracellular recordings were made from rabbit nodose neurones in vitro. Two temporally distinct spike after-hyperpolarizations (a.h.p.s) were identified in a subpopulation of C-type neurones. The fast a.h.p. after a single spike lasted no longer than 500 ms, while the slow a.h.p. persisted for seconds. Both a.h.p.s. were increased in amplitude in low K+ (0.56 mM) solutions and decreased in amplitude in high K+ (11.2 mM) solutions, and both were reversed at hyperpolarized membrane potentials. The slow a.h.p. was reduced in low Ca2+ (0.22 mM), in the presence of Ca2+ antagonists (Ni2+, 1 mM; Cd2+, 100 microM; or Co2+, 1 mM) and was enhanced in tetraethylammonium (5 mM). In approximately half of the cells tested, the fast a.h.p. was reduced in low Ca2+ and in the presence of the Ca2+ antagonists. In the remaining cells the fast a.h.p. was insensitive to these procedures. Prostaglandin (PGE1, 1-10 micrograms/ml) reduced the slow a.h.p. in all cells tested. Neither the Ca2+-sensitive nor the Ca2+-insensitive fast a.h.p. was affected by the prostaglandin. It is concluded that there is a subpopulation of C-type nodose neurones possessing a slow a.h.p. which is due to a Ca2+-dependent K+ current. This subpopulation of neurones can further be divided on the basis of the presence of a Ca2+-sensitive fast a.h.p. Furthermore, PGE1 pharmacologically separates the fast and slow a.h.p.s by selectively blocking the slow one. The blockage by the PGE1 is most probably not due to a reduction in Ca2+ influx.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams P. R., Constanti A., Brown D. A., Clark R. B. Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones. Nature. 1982 Apr 22;296(5859):746–749. doi: 10.1038/296746a0. [DOI] [PubMed] [Google Scholar]
  2. Ahmed Z., Connor J. A. Measurement of calcium influx under voltage clamp in molluscan neurones using the metallochromic dye arsenazo III. J Physiol. 1979 Jan;286:61–82. doi: 10.1113/jphysiol.1979.sp012607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Akaike N., Lee K. S., Brown A. M. The calcium current of Helix neuron. J Gen Physiol. 1978 May;71(5):509–531. doi: 10.1085/jgp.71.5.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barrett E. F., Barret J. N. Separation of two voltage-sensitive potassium currents, and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurones. J Physiol. 1976 Mar;255(3):737–774. doi: 10.1113/jphysiol.1976.sp011306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belmonte C., Gallego R. Membrane properties of cat sensory neurones with chemoreceptor and baroreceptor endings. J Physiol. 1983 Sep;342:603–614. doi: 10.1113/jphysiol.1983.sp014871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown D. A., Constanti A., Adams P. R. Ca-activated potassium current in vertebrate sympathetic neurons. Cell Calcium. 1983 Dec;4(5-6):407–420. doi: 10.1016/0143-4160(83)90017-9. [DOI] [PubMed] [Google Scholar]
  7. Buck S. H., Walsh J. H., Yamamura H. I., Burks T. F. Neuropeptides in sensory neurons. Life Sci. 1982 May 31;30(22):1857–1866. doi: 10.1016/0024-3205(82)90465-9. [DOI] [PubMed] [Google Scholar]
  8. Choi D. W., Fischbach G. D. GABA conductance of chick spinal cord and dorsal root ganglion neurons in cell culture. J Neurophysiol. 1981 Apr;45(4):605–620. doi: 10.1152/jn.1981.45.4.605. [DOI] [PubMed] [Google Scholar]
  9. Coleridge H. M., Coleridge J. C., Ginzel K. H., Baker D. G., Banzett R. B., Morrison M. A. Stimulation of 'irritant' receptors and afferent C-fibres in the lungs by prostaglandins. Nature. 1976 Dec 2;264(5585):451–453. doi: 10.1038/264451a0. [DOI] [PubMed] [Google Scholar]
  10. Coleridge J. C., Coleridge H. M. Afferent C-fibers and cardiorespiratory chemoreflexes. Am Rev Respir Dis. 1977 Jun;115(6 Pt 2):251–260. doi: 10.1164/arrd.1977.115.S.251. [DOI] [PubMed] [Google Scholar]
  11. Gallego R., Eyzaguirre C. Membrane and action potential characteristics of A and C nodose ganglion cells studied in whole ganglia and in tissue slices. J Neurophysiol. 1978 Sep;41(5):1217–1232. doi: 10.1152/jn.1978.41.5.1217. [DOI] [PubMed] [Google Scholar]
  12. Gallego R. The ionic basis of action potentials in petrosal ganglion cells of the cat. J Physiol. 1983 Sep;342:591–602. doi: 10.1113/jphysiol.1983.sp014870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Helke C. J., Jacobowitz D. M., Thoa N. B. Capsaicin and potassium evoked substance P release from the nucleus tractus solitarius and spinal trigeminal nucleus in vitro. Life Sci. 1981 Oct 26;29(17):1779–1785. doi: 10.1016/0024-3205(81)90188-0. [DOI] [PubMed] [Google Scholar]
  14. Hermann A., Gorman A. L. Effects of tetraethylammonium on potassium currents in a molluscan neurons. J Gen Physiol. 1981 Jul;78(1):87–110. doi: 10.1085/jgp.78.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hermann A., Hartung K. Ca2+ activated K+ conductance in molluscan neurones. Cell Calcium. 1983 Dec;4(5-6):387–405. doi: 10.1016/0143-4160(83)90016-7. [DOI] [PubMed] [Google Scholar]
  16. Higashi H., Nishi S. 5-Hydroxytryptamine receptors of visceral primary afferent neurones on rabbit nodose ganglia. J Physiol. 1982 Feb;323:543–567. doi: 10.1113/jphysiol.1982.sp014091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Higashi H., Shinnick-Gallagher P., Gallagher J. P. Morphine enhances and depresses Ca2+-dependent responses in visceral primary afferent neurons. Brain Res. 1982 Nov 11;251(1):186–191. doi: 10.1016/0006-8993(82)91291-4. [DOI] [PubMed] [Google Scholar]
  18. Jaffe R. A., Sampson S. R. Analysis of passive and active electrophysiologic properties of neurons in mammalian nodose ganglia maintained in vitro. J Neurophysiol. 1976 Jul;39(4):802–815. doi: 10.1152/jn.1976.39.4.802. [DOI] [PubMed] [Google Scholar]
  19. Kalia M., Mesulam M. M. Brain stem projections of sensory and motor components of the vagus complex in the cat: II. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol. 1980 Sep 15;193(2):467–508. doi: 10.1002/cne.901930211. [DOI] [PubMed] [Google Scholar]
  20. Katz D. M., Karten H. J. Substance P in the vagal sensory ganglia: localization in cell bodies and pericellular arborizations. J Comp Neurol. 1980 Sep 15;193(2):549–564. doi: 10.1002/cne.901930216. [DOI] [PubMed] [Google Scholar]
  21. Koketsu K., Akasu T., Miyagawa M. Identification of gK systems activated by [Ca2+]. Brain Res. 1982 Jul 15;243(2):369–372. doi: 10.1016/0006-8993(82)90263-3. [DOI] [PubMed] [Google Scholar]
  22. Kuba K., Morita K., Nohmi M. Origin of calcium ions involved in the generation of a slow afterhyperpolarization in bullfrog sympathetic neurones. Pflugers Arch. 1983 Nov;399(3):194–202. doi: 10.1007/BF00656714. [DOI] [PubMed] [Google Scholar]
  23. Lundberg J. M., Saria A. Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature. 1983 Mar 17;302(5905):251–253. doi: 10.1038/302251a0. [DOI] [PubMed] [Google Scholar]
  24. MacDermott A. B., Weight F. F. Action potential repolarization may involve a transient, Ca2+-sensitive outward current in a vertebrate neurone. Nature. 1982 Nov 11;300(5888):185–188. doi: 10.1038/300185a0. [DOI] [PubMed] [Google Scholar]
  25. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  26. Meech R. W., Standen N. B. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol. 1975 Jul;249(2):211–239. doi: 10.1113/jphysiol.1975.sp011012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Morita K., North R. A., Tokimasa T. The calcium-activated potassium conductance in guinea-pig myenteric neurones. J Physiol. 1982 Aug;329:341–354. doi: 10.1113/jphysiol.1982.sp014306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Neering I. R., McBurney R. N. Role for microsomal Ca storage in mammalian neurones? Nature. 1984 May 10;309(5964):158–160. doi: 10.1038/309158a0. [DOI] [PubMed] [Google Scholar]
  29. North R. A., Tokimasa T. Depression of calcium-dependent potassium conductance of guinea-pig myenteric neurones by muscarinic agonists. J Physiol. 1983 Sep;342:253–266. doi: 10.1113/jphysiol.1983.sp014849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rang H. P., Ritchie J. M. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol. 1968 May;196(1):183–221. doi: 10.1113/jphysiol.1968.sp008502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith S. J., MacDermott A. B., Weight F. F. Detection of intracellular Ca2+ transients in sympathetic neurones using arsenazo III. 1983 Jul 28-Aug 3Nature. 304(5924):350–352. doi: 10.1038/304350a0. [DOI] [PubMed] [Google Scholar]
  32. Suzuki T., Kusano K. Hyperpolarizing potentials induced by Ca-mediated K-conductance increase in hamster submandibular ganglion cells. J Neurobiol. 1978 Sep;9(5):367–392. doi: 10.1002/neu.480090504. [DOI] [PubMed] [Google Scholar]

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