Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1985 Apr;361:165–184. doi: 10.1113/jphysiol.1985.sp015639

Noradrenaline hyperpolarization and depolarization in cat vesical parasympathetic neurones.

T Akasu, J P Gallagher, T Nakamura, P Shinnick-Gallagher, M Yoshimura
PMCID: PMC1192853  PMID: 2580974

Abstract

Responses to noradrenaline (NA) applied by superfusion, ionophoresis or pressure pulse were analysed using conventional intracellular recording and voltage-clamp methods in cat vesical parasympathetic ganglia. NA (1 microM) hyperpolarized 60% of the neurones, depolarized 25%, and produced a biphasic potential, which comprised a membrane hyperpolarization followed by a membrane depolarization, in 10%. About 5% of the neurones did not respond to NA. The NA hyperpolarization was blocked by yohimbine (1 microM), an alpha 2-adrenoceptor antagonist, whereas the NA depolarization was blocked by prazosin (0.1-1 microM), an alpha 1-adrenoceptor antagonist. These data indicated that the NA hyperpolarization was mediated through alpha 2-adrenoceptors and the NA depolarization through alpha 1-adrenoceptors. The NA hyperpolarization was accompanied by an increase in conductance, while the NA depolarization was associated with a decrease in conductance measured under manual-clamp conditions. Similar conductance changes were observed under voltage clamp. NA hyperpolarizations became smaller as the membrane was hyperpolarized and reversed polarity beyond -100 mV. NA depolarizations also became smaller at hyperpolarized membrane potentials and reversed polarity around -90 mV. The NA responses were enhanced in low-K media and depressed in high-K Krebs solution. The NA hyperpolarization was blocked by the Ca antagonists, Cd, Mn and Co. Intracellular injection of EGTA caused a slowly developing, progressive block of the NA hyperpolarization. The NA depolarization was not affected by low Ca concentrations, Ca antagonists or intracellular injection of EGTA. In some neurones the NA depolarization was unmasked in solutions containing Ca antagonists and after intracellular EGTA injection. The NA hyperpolarization was depressed by intracellular injection and extracellular superfusion of Cs but not by TEA. Ba (10-100 microM) depressed the NA hyperpolarization by 30%. The NA depolarization persisted in the presence of muscarine (10 microM) and was not blocked by Cs or TEA but was depressed 70% by Ba (10 microM). These data are consistent with the hypotheses that alpha 2-adrenoceptor activation produces a membrane hyperpolarization that is mediated through a Ca-dependent K conductance, and that alpha 1-adrenoceptor activation produces a membrane depolarization through closure of a voltage-insensitive K channel.

Full text

PDF

Selected References

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

  1. Adams P. R., Brown D. A., Constanti A. M-currents and other potassium currents in bullfrog sympathetic neurones. J Physiol. 1982 Sep;330:537–572. doi: 10.1113/jphysiol.1982.sp014357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams P. R., Brown D. A., Constanti A. Pharmacological inhibition of the M-current. J Physiol. 1982 Nov;332:223–262. doi: 10.1113/jphysiol.1982.sp014411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Akasu T., Gallagher J. P., Koketsu K., Shinnick-Gallagher P. Slow excitatory post-synaptic currents in bull-frog sympathetic neurones. J Physiol. 1984 Jun;351:583–593. doi: 10.1113/jphysiol.1984.sp015264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Armstrong C. M. Potassium pores of nerve and muscle membranes. Membranes. 1975;3:325–358. [PubMed] [Google Scholar]
  6. 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]
  7. Brown D. A., Adams P. R. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature. 1980 Feb 14;283(5748):673–676. doi: 10.1038/283673a0. [DOI] [PubMed] [Google Scholar]
  8. Brown D. A., Caulfield M. P. Hyperpolarizing 'alpha 2'-adrenoceptors in rat sympathetic ganglia. Br J Pharmacol. 1979 Mar;65(3):435–445. doi: 10.1111/j.1476-5381.1979.tb07848.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown D. A., Constanti A. Intracellular observations on the effects of muscarinic agonists on rat sympathetic neurones. Br J Pharmacol. 1980 Dec;70(4):593–608. doi: 10.1111/j.1476-5381.1980.tb09778.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brown D. A., Dunn P. M. Depolarization of rat isolated superior cervical ganglia mediated by beta 2-adrenoceptors. Br J Pharmacol. 1983 Jun;79(2):429–439. doi: 10.1111/j.1476-5381.1983.tb11016.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown D. A., Griffith W. H. Calcium-activated outward current in voltage-clamped hippocampal neurones of the guinea-pig. J Physiol. 1983 Apr;337:287–301. doi: 10.1113/jphysiol.1983.sp014624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Constanti A., Adams P. R., Brown D. A. Who do barium ions imitate acetylcholine? Brain Res. 1981 Feb 9;206(1):244–250. doi: 10.1016/0006-8993(81)90125-6. [DOI] [PubMed] [Google Scholar]
  13. Constanti A., Brown D. A. M-Currents in voltage-clamped mammalian sympathetic neurones. Neurosci Lett. 1981 Jul 17;24(3):289–294. doi: 10.1016/0304-3940(81)90173-7. [DOI] [PubMed] [Google Scholar]
  14. De Groat W. C., Saum W. R. Adrenergic inhibition in mammalian parasympathetic ganglia. Nat New Biol. 1971 Jun 9;231(23):188–189. doi: 10.1038/newbio231188a0. [DOI] [PubMed] [Google Scholar]
  15. De Groat W. C., Volle R. L. The actions of the catecholamines on transmission in the superior cervical ganglion of the cat. J Pharmacol Exp Ther. 1966 Oct;154(1):1–13. [PubMed] [Google Scholar]
  16. Deth R., van Breemen C. Agonist induced release of intracellular Ca2+ in the rabbit aorta. J Membr Biol. 1977 Jan 28;30(4):363–380. doi: 10.1007/BF01869677. [DOI] [PubMed] [Google Scholar]
  17. Eaton D. C., Brodwick M. S. Effects of barium on the potassium conductance of squid axon. J Gen Physiol. 1980 Jun;75(6):727–750. doi: 10.1085/jgp.75.6.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Exton J. H. Mechanisms involved in alpha-adrenergic phenomena: role of calcium ions in actions of catecholamines in liver and other tissues. Am J Physiol. 1980 Jan;238(1):E3–12. doi: 10.1152/ajpendo.1980.238.1.E3. [DOI] [PubMed] [Google Scholar]
  19. Fray J. C., Laurens N. J. Mechanism by which albumin stimulates renin secretion in isolated kidneys and juxtaglomerular cells. J Physiol. 1981 Nov;320:31–39. doi: 10.1113/jphysiol.1981.sp013932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gallagher J. P., Griffith W. H., Shinnick-Gallagher P. Cholinergic transmission in cat parasympathetic ganglia. J Physiol. 1982 Nov;332:473–486. doi: 10.1113/jphysiol.1982.sp014425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gay L. A., Stanfield P. R. Cs(+) causes a voltage-dependent block of inward K currents in resting skeletal muscle fibres. Nature. 1977 May 12;267(5607):169–170. doi: 10.1038/267169a0. [DOI] [PubMed] [Google Scholar]
  22. Gorman A. L., Hermann A. Internal effects of divalent cations on potassium permeability in molluscan neurones. J Physiol. 1979 Nov;296:393–410. doi: 10.1113/jphysiol.1979.sp013012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Griffith W. H., 3rd, Gallagher J. P., Shinnick-Gallagher P. An intracellular investigation of cat vesical pelvic ganglia. J Neurophysiol. 1980 Feb;43(2):343–354. doi: 10.1152/jn.1980.43.2.343. [DOI] [PubMed] [Google Scholar]
  24. HAMBERGER B., NORBERG K. A. ADRENERGIC SYNAPTIC TERMINALS AND NERVE CELLS IN BLADDER GANGLIA OF THE CAT. Int J Neuropharmacol. 1965 Feb;4:41–45. doi: 10.1016/0028-3908(65)90045-6. [DOI] [PubMed] [Google Scholar]
  25. Hagiwara S., Miyazaki S., Moody W., Patlak J. Blocking effects of barium and hydrogen ions on the potassium current during anomalous rectification in the starfish egg. J Physiol. 1978 Jun;279:167–185. doi: 10.1113/jphysiol.1978.sp012338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Halliwell J. V., Adams P. R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 1982 Oct 28;250(1):71–92. doi: 10.1016/0006-8993(82)90954-4. [DOI] [PubMed] [Google Scholar]
  28. Hamberger B., Norberg K. A. Studies on some systems of adrenergic synaptic terminals in the abdominal ganglia of the cat. Acta Physiol Scand. 1965 Nov;65(3):235–242. doi: 10.1111/j.1748-1716.1965.tb04266.x. [DOI] [PubMed] [Google Scholar]
  29. Hart D. T., Borowitz J. L. Adrenal catecholamine release by divalent mercury and cadmium. Arch Int Pharmacodyn Ther. 1974 May;209(1):94–99. [PubMed] [Google Scholar]
  30. Hermann A., Gorman A. L. Blockade of voltage-dependent and Ca2+-dependent K+ current components by internal Ba2+ in molluscan pacemaker neurons. Experientia. 1979 Feb 15;35(2):229–231. doi: 10.1007/BF01920633. [DOI] [PubMed] [Google Scholar]
  31. Hermann A., Gorman A. L. External and internal effects of tetraethylammonium on voltage-dependent and Ca-dependent K+ currents components in molluscan pacemaker neurons. Neurosci Lett. 1979 Apr;12(1):87–92. doi: 10.1016/0304-3940(79)91485-x. [DOI] [PubMed] [Google Scholar]
  32. Heyer C. B., Lux H. D. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia. J Physiol. 1976 Nov;262(2):349–382. doi: 10.1113/jphysiol.1976.sp011599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hirst G. D., Silinsky E. M. Some effects of 5-hydroxytryptamine, dopamine and noradrenaline on neurones in the submucous plexus of guinea-pig small intestine. J Physiol. 1975 Oct;251(3):817–832. doi: 10.1113/jphysiol.1975.sp011124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Horn J. P., Dodd J. Monosynaptic muscarinic activation of K+ conductance underlies the slow inhibitory postsynaptic potential in sympathetic ganglia. Nature. 1981 Aug 13;292(5824):625–627. doi: 10.1038/292625a0. [DOI] [PubMed] [Google Scholar]
  35. Horn J. P., McAfee D. A. Alpha-drenergic inhibition of calcium-dependent potentials in rat sympathetic neurones. J Physiol. 1980 Apr;301:191–204. doi: 10.1113/jphysiol.1980.sp013198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Iwatsuki N., Petersen O. H. Membrane potential, resistance, and intercellular communication in the lacrimal gland: effects of acetylcholine and adrenaline. J Physiol. 1978 Feb;275:507–520. doi: 10.1113/jphysiol.1978.sp012204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Johnston D., Hablitz J. J., Wilson W. A. Voltage clamp discloses slow inward current in hippocampal burst-firing neurones. Nature. 1980 Jul 24;286(5771):391–393. doi: 10.1038/286391a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Koketsu K., Nakamura M. The electrogenesis of adrenaline-hyperpolarization of sympathetic ganglion cells in bullfrogs. Jpn J Physiol. 1976;26(1):63–77. doi: 10.2170/jjphysiol.26.63. [DOI] [PubMed] [Google Scholar]
  40. Krnjević K., Puil E., Werman R. EGTA and motoneuronal after-potentials. J Physiol. 1978 Feb;275:199–223. doi: 10.1113/jphysiol.1978.sp012186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kuba K., Koketsu K. Synaptic events in sympathetic ganglia. Prog Neurobiol. 1978;11(2):77–169. doi: 10.1016/0301-0082(78)90010-2. [DOI] [PubMed] [Google Scholar]
  42. Kuba K. Release of calcium ions linked to the activation of potassium conductance in a caffeine-treated sympathetic neurone. J Physiol. 1980 Jan;298:251–269. doi: 10.1113/jphysiol.1980.sp013079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kuffler S. W., Sejnowski T. J. Peptidergic and muscarinic excitation at amphibian sympathetic synapses. J Physiol. 1983 Aug;341:257–278. doi: 10.1113/jphysiol.1983.sp014805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. LUNDBERG A. Adrenaline and transmission in the sympathetic ganglion of the cat. Acta Physiol Scand. 1952 Sep 10;26(2-3):252–263. doi: 10.1111/j.1748-1716.1952.tb00908.x. [DOI] [PubMed] [Google Scholar]
  45. Langley J. N., Anderson H. K. The Innervation of the Pelvic and adjoining Viscera: Part II. The Bladder. Part III. The External Generative Organs. Part IV. The Internal Generative Organs. Part V. Position of the Nerve Cells on the Course of the Efferent Nerve Fibres. J Physiol. 1895 Dec 30;19(1-2):71–139. doi: 10.1113/jphysiol.1895.sp000587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Langley J. N., Anderson H. K. The Innervation of the Pelvic and adjoining Viscera: Part VII. Anatomical Observations. J Physiol. 1896 Oct 19;20(4-5):372–406. doi: 10.1113/jphysiol.1896.sp000629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Libet B., Kobayashi H. Adrenergic mediation of slow inhibitory postsynaptic potential in sympathetic ganglia of the frog. J Neurophysiol. 1974 Jul;37(4):805–814. doi: 10.1152/jn.1974.37.4.805. [DOI] [PubMed] [Google Scholar]
  48. Mayer M. L., Higashi H., Gallagher J. P., Shinnick-Gallagher P. On the mechanism of action of GABA in pelvic vesical ganglia: biphasic responses evoked by two opposing actions on membrane conductance. Brain Res. 1983 Feb 7;260(2):233–248. doi: 10.1016/0006-8993(83)90677-7. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Moolenaar W. H., Spector I. The calcium current and the activation of a slow potassium conductance in voltage-clamped mouse neuroblastoma cells. J Physiol. 1979 Jul;292:307–323. doi: 10.1113/jphysiol.1979.sp012852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Morita K., North R. A. Clonidine activates membrane potassium conductance in myenteric neurones. Br J Pharmacol. 1981 Oct;74(2):419–428. doi: 10.1111/j.1476-5381.1981.tb09987.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. PORTZEHL H., CALDWELL P. C., RUEEGG J. C. THE DEPENDENCE OF CONTRACTION AND RELAXATION OF MUSCLE FIBRES FROM THE CRAB MAIA SQUINADO ON THE INTERNAL CONCENTRATION OF FREE CALCIUM IONS. Biochim Biophys Acta. 1964 May 25;79:581–591. doi: 10.1016/0926-6577(64)90224-4. [DOI] [PubMed] [Google Scholar]
  53. Putney J. W., Jr Muscarinic, alpha-adrenergic and peptide receptors regulate the same calcium influx sites in the parotid gland. J Physiol. 1977 Jun;268(1):139–149. doi: 10.1113/jphysiol.1977.sp011851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Suzuki T., Volle R. L. Nicotinic, muscarinic and adrenergic receptors in a parasympathetic ganglion. J Pharmacol Exp Ther. 1979 Oct;211(1):252–256. [PubMed] [Google Scholar]
  55. Tillotson D. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1497–1500. doi: 10.1073/pnas.76.3.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Trautmann A., Marty A. Activation of Ca-dependent K channels by carbamoylcholine in rat lacrimal glands. Proc Natl Acad Sci U S A. 1984 Jan;81(2):611–615. doi: 10.1073/pnas.81.2.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Triggle C. R., Grant W. F., Triggle D. J. Intestinal smooth muscle contraction and the effects of cadmium and A23187. J Pharmacol Exp Ther. 1975 Jul;194(1):182–190. [PubMed] [Google Scholar]
  58. Williams B. J., Laubach D. J., Nechay B. R., Steinsland O. S. The effect of cadmium on adrenergic neurotransmission in vitro. Life Sci. 1978 Nov 9;23(19):1929–1933. doi: 10.1016/0024-3205(78)90559-3. [DOI] [PubMed] [Google Scholar]
  59. de Groat W. C., Booth A. M. Inhibition and facilitation in parasympathetic ganglia of the urinary bladder. Fed Proc. 1980 Oct;39(12):2990–2996. [PubMed] [Google Scholar]
  60. de Groat W. C., Krier J. An electrophysiological study of the sacral parasympathetic pathway to the colon of the cat. J Physiol. 1976 Sep;260(2):425–445. doi: 10.1113/jphysiol.1976.sp011523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. el-Badawi A., Shenk E. A. A new theory of the innervation of bladder musculature. 1. Morphology of the intrinsic vesical innervation apparatus. J Urol. 1968 May;99(5):585–587. doi: 10.1016/S0022-5347(17)62753-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES