Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1987 Dec;394:331–349. doi: 10.1113/jphysiol.1987.sp016873

Two calcium-activated potassium conductances in a subpopulation of coeliac neurones of guinea-pig and rabbit.

J F Cassell 1, E M McLachlan 1
PMCID: PMC1191964  PMID: 2451019

Abstract

1. Some of the sympathetic neurones in coeliac ganglia isolated from young guinea-pigs and rabbits were found to generate action potentials followed by after-hyperpolarizations with durations of 3-8 s, much longer than those (congruent to 300-500 ms) observed in the majority of other mammalian sympathetic neurones. 2. This type of ganglion cell discharged only once at the onset of a depolarizing step unless a very high intensity current was applied. Passive and voltage-dependent membrane conductances studied in detail in guinea-pig ganglia differed from those in the two other classes of sympathetic ganglion cell described previously (Cassell, Clark & McLachlan, 1986). 3. By using a single microelectrode to voltage clamp the soma, it was possible to demonstrate that both fast and slow components of the tail current following initiation of an uncontrolled 'action current' in neurones with long after-hyperpolarizations (l.a.h.) were carried by K+ ions, as was the fast tail current (time constant, tau congruent to 130 ms) present in other coeliac neurones. 4. The amplitude of both components of the tail current in l.a.h. neurones was markedly reduced by the replacement of Ca2+ by Mn2+, Co2+ or Ba2+ ions. These manoeuvres had similar effects on the fast tail current in other coeliac neurones. 5. Both time course and amplitude of the fast tail current were increased when Ca2+ concentration was raised, or when several 'action currents' were initiated, whereas only the amplitude of the slow tail current was affected. 6. The time course of the slow tail current could be described by the sum of two exponentials with tau on = 285 ms and tau off = 1.3 s at 35 degrees C occurring after a delay of 60 ms. This current had a Q10 of about 4 between 35 and 25 degrees C. In contrast, the Q10 of the fast component was about 2. 7. Morphine (10(-6) M) and vasoactive intestinal polypeptide (10(-6) M) had no effect on the outward tail current in l.a.h. neurones, but 5-hydroxytryptamine (10(-6) M) was found to abolish the slow component without affecting the fast component. 8. The slow tail current was activated in the subthreshold range of membrane potentials, and its properties could account for the firing characteristics of this subpopulation of sympathetic neurones. 9. The two calcium-activated potassium conductances that are responsible for the prolonged after-hyperpolarization resemble those in a subpopulation of nodose ganglion cells with unmyelinated axons (Fowler, Greene & Weinreich, 1985).(ABSTRACT TRUNCATED AT 400 WORDS)

Full text

PDF
331

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. Belluzzi O., Sacchi O., Wanke E. Identification of delayed potassium and calcium currents in the rat sympathetic neurone under voltage clamp. J Physiol. 1985 Jan;358:109–129. doi: 10.1113/jphysiol.1985.sp015543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berridge M. J., Irvine R. F. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984 Nov 22;312(5992):315–321. doi: 10.1038/312315a0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Cassell J. F., Clark A. L., McLachlan E. M. Characteristics of phasic and tonic sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 Mar;372:457–483. doi: 10.1113/jphysiol.1986.sp016020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cassell J. F., McLachlan E. M. Muscarinic agonists block five different potassium conductances in guinea-pig sympathetic neurones. Br J Pharmacol. 1987 Jun;91(2):259–261. doi: 10.1111/j.1476-5381.1987.tb10279.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cassell J. F., McLachlan E. M. The effect of a transient outward current (IA) on synaptic potentials in sympathetic ganglion cells of the guinea-pig. J Physiol. 1986 May;374:273–288. doi: 10.1113/jphysiol.1986.sp016079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Costa M., Furness J. B. Somatostatin is present in a subpopulation of noradrenergic nerve fibres supplying the intestine. Neuroscience. 1984 Nov;13(3):911–919. doi: 10.1016/0306-4522(84)90105-2. [DOI] [PubMed] [Google Scholar]
  10. Decktor D. L., Weems W. A. An intracellular characterization of neurones and neural connexions within the left coeliac ganglion of cats. J Physiol. 1983 Aug;341:197–211. doi: 10.1113/jphysiol.1983.sp014801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dun N. J., Kiraly M., Ma R. C. Evidence for a serotonin-mediated slow excitatory potential in the guinea-pig coeliac ganglia. J Physiol. 1984 Jun;351:61–76. doi: 10.1113/jphysiol.1984.sp015232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dunlap K., Fischbach G. D. Neurotransmitters decrease the calcium conductance activated by depolarization of embryonic chick sensory neurones. J Physiol. 1981 Aug;317:519–535. doi: 10.1113/jphysiol.1981.sp013841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fowler J. C., Greene R., Weinreich D. Two calcium-sensitive spike after-hyperpolarizations in visceral sensory neurones of the rabbit. J Physiol. 1985 Aug;365:59–75. doi: 10.1113/jphysiol.1985.sp015759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Freschi J. E. Membrane currents of cultured rat sympathetic neurons under voltage clamp. J Neurophysiol. 1983 Dec;50(6):1460–1478. doi: 10.1152/jn.1983.50.6.1460. [DOI] [PubMed] [Google Scholar]
  15. Galvan M., Sedlmeir C. Outward currents in voltage-clamped rat sympathetic neurones. J Physiol. 1984 Nov;356:115–133. doi: 10.1113/jphysiol.1984.sp015456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Hirst G. D., Johnson S. M., van Helden D. F. The calcium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 Apr;361:297–314. doi: 10.1113/jphysiol.1985.sp015647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hirst G. D., Johnson S. M., van Helden D. F. The slow calcium-dependent potassium current in a myenteric neurone of the guinea-pig ileum. J Physiol. 1985 Apr;361:315–337. doi: 10.1113/jphysiol.1985.sp015648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hirst G. D., McLachlan E. M. Development of dendritic calcium currents in ganglion cells of the rat lower lumbar sympathetic chain. J Physiol. 1986 Aug;377:349–368. doi: 10.1113/jphysiol.1986.sp016191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hökfelt T., Elfvin L. G., Elde R., Schultzberg M., Goldstein M., Luft R. Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3587–3591. doi: 10.1073/pnas.74.8.3587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Macrae I. M., Furness J. B., Costa M. Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tissue Res. 1986;244(1):173–180. doi: 10.1007/BF00218395. [DOI] [PubMed] [Google Scholar]
  23. McAfee D. A., Yarowsky P. J. Calcium-dependent potentials in the mammalian sympathetic neurone. J Physiol. 1979 May;290(2):507–523. doi: 10.1113/jphysiol.1979.sp012787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McLachlan E. M., Llewellyn-Smith I. J. The immunohistochemical distribution of neuropeptide Y in lumbar pre- and paravertebral sympathetic ganglia of the guinea pig. J Auton Nerv Syst. 1986 Dec;17(4):313–324. doi: 10.1016/0165-1838(86)90097-4. [DOI] [PubMed] [Google Scholar]
  25. McLachlan E. M. The effects of strontium and barium ions at synapses in sympathetic ganglia. J Physiol. 1977 May;267(2):497–518. doi: 10.1113/jphysiol.1977.sp011823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Schultzberg M., Hökfelt T., Terenius L., Elfvin L. G., Lundberg J. M., Brandt J., Elde R. P., Goldstein M. Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience. 1979;4(2):249–270. doi: 10.1016/0306-4522(79)90087-3. [DOI] [PubMed] [Google Scholar]
  29. Tokimasa T., Morita K., North A. Opiates and clonidine prolong calcium-dependent after-hyperpolarizations. Nature. 1981 Nov 12;294(5837):162–163. doi: 10.1038/294162a0. [DOI] [PubMed] [Google Scholar]
  30. Weems W. A., Szurszewski J. H. An intracellular analysis of some intrinsic factors controlling neural output from inferior mesenteric ganglion of guinea pigs. J Neurophysiol. 1978 Mar;41(2):305–321. doi: 10.1152/jn.1978.41.2.305. [DOI] [PubMed] [Google Scholar]
  31. Yarom Y., Sugimori M., Llinás R. Ionic currents and firing patterns of mammalian vagal motoneurons in vitro. Neuroscience. 1985 Dec;16(4):719–737. doi: 10.1016/0306-4522(85)90090-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES