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. 1995 Jul 1;486(Pt 1):15–31. doi: 10.1113/jphysiol.1995.sp020787

Potassium currents in adult rat intracardiac neurones.

S X Xi-Moy 1, N J Dun 1
PMCID: PMC1156493  PMID: 7562632

Abstract

1. Properties of K+ currents were studied in isolated adult rat parasympathetic intracardiac neurones with the use of single-electrode voltage-clamp techniques. 2. A hyperpolarization-activated inward rectifier current was revealed when the membrane was clamped close to the resting level (-60 mV). The slowly developing inward relaxation had a mean amplitude of 450 pA at -150 mV, an activation threshold of -60 to -70 mV and a relaxation time constant of 41 ms at -120 mV. The current was reversibly blocked by Cs+ (1 mM) and became smaller with reduced [K+]o and [Na+]o, indicating that this inward rectifier current probably is a time- and voltage-dependent Na(+)-K+ current. 3. Step depolarizations from the holding potential of -80 mV evoked a transient (< 100 ms at -40 mV) outward K+ current (IA) which was blocked by 4-aminopyridine (4-AP, 1 mM). The time constants for IA inactivation were 20 ms at -50 mV and 16 ms at -20 mV. The steady-state activation and (removal of) inactivation curve showed a small overlap between -70 and -40 mV; the reversal potential of IA was close to EK. 4. Step hyperpolarizations from the depolarized potentials, i.e. -30 mV, revealed a slow inward relaxation associated with the deactivation of a time- and voltage-dependent current. The inward relaxation became faster at more hyperpolarized potentials and reversed at -85 and -53 mV in 4.7 and 15 mM [K+]o. This current was blocked by muscarine (20 microM) and Ba2+ (1 mM) but not affected by Cs+ (1 mM); this current may correspond to the M-current (IM). 5. Depolarization-activated outward K+ currents were evoked by holding the membrane close to the resting potential in the presence of tetrodotoxin (TTX, 3 microM), 4-AP (1 mM) and Ba2+ (1 mM). The amplitude of the outward relaxation and the tail current became smaller as the [K+]o was elevated. The outward tail current was reduced in a Ca(2+)-free solution and the residual current was eliminated by the addition of tetraethylammonium (TEA, 10 mM); the reversal potential was shifted in a direction predicted by the Nernst equation. These findings suggest the presence of delayed rectifier K+ current and Ca(2+)-activated K+ current. 6. Superfusion of TEA, Ba2+ and 4-AP, but not Cs+, induced rhythmic discharges in some of the otherwise quiescent intracardiac neurones.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  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. Akasu T., Tokimasa T. Potassium currents in submucous neurones of guinea-pig caecum and their synaptic modification. J Physiol. 1989 Sep;416:571–588. doi: 10.1113/jphysiol.1989.sp017778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Allen T. G., Burnstock G. A voltage-clamp study of the electrophysiological characteristics of the intramural neurones of the rat trachea. J Physiol. 1990 Apr;423:593–614. doi: 10.1113/jphysiol.1990.sp018042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Allen T. G., Burnstock G. M1 and M2 muscarinic receptors mediate excitation and inhibition of guinea-pig intracardiac neurones in culture. J Physiol. 1990 Mar;422:463–480. doi: 10.1113/jphysiol.1990.sp017995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Brown D. M-currents: an update. Trends Neurosci. 1988 Jul;11(7):294–299. doi: 10.1016/0166-2236(88)90089-6. [DOI] [PubMed] [Google Scholar]
  8. Burkholder T., Chambers M., Hotmire K., Wurster R. D., Moody S., Randall W. C. Gross and microscopic anatomy of the vagal innervation of the rat heart. Anat Rec. 1992 Mar;232(3):444–452. doi: 10.1002/ar.1092320313. [DOI] [PubMed] [Google Scholar]
  9. Connor J. A., Stevens C. F. Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J Physiol. 1971 Feb;213(1):31–53. doi: 10.1113/jphysiol.1971.sp009366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Constanti A., Galvan M. Fast inward-rectifying current accounts for anomalous rectification in olfactory cortex neurones. J Physiol. 1983 Feb;335:153–178. doi: 10.1113/jphysiol.1983.sp014526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DiFrancesco D. A study of the ionic nature of the pace-maker current in calf Purkinje fibres. J Physiol. 1981 May;314:377–393. doi: 10.1113/jphysiol.1981.sp013714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. DiFrancesco D., Ojeda C. Properties of the current if in the sino-atrial node of the rabbit compared with those of the current iK, in Purkinje fibres. J Physiol. 1980 Nov;308:353–367. doi: 10.1113/jphysiol.1980.sp013475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fain G. L., Lisman J. E. Membrane conductances of photoreceptors. Prog Biophys Mol Biol. 1981;37(2):91–147. doi: 10.1016/0079-6107(82)90021-9. [DOI] [PubMed] [Google Scholar]
  15. Flamm R. E., Harris-Warrick R. M. Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J Neurophysiol. 1986 May;55(5):847–865. doi: 10.1152/jn.1986.55.5.847. [DOI] [PubMed] [Google Scholar]
  16. Flamm R. E., Harris-Warrick R. M. Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit. J Neurophysiol. 1986 May;55(5):866–881. doi: 10.1152/jn.1986.55.5.866. [DOI] [PubMed] [Google Scholar]
  17. Galligan J. J., North R. A., Tokimasa T. Muscarinic agonists and potassium currents in guinea-pig myenteric neurones. Br J Pharmacol. 1989 Jan;96(1):193–203. doi: 10.1111/j.1476-5381.1989.tb11800.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goh J. W., Kelly M. E., Pennefather P. S. Electrophysiological function of the delayed rectifier (IK) in bullfrog sympathetic ganglion neurones. Pflugers Arch. 1989 Mar;413(5):482–486. doi: 10.1007/BF00594177. [DOI] [PubMed] [Google Scholar]
  19. Grace A. A., Bunney B. S. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci. 1984 Nov;4(11):2877–2890. doi: 10.1523/JNEUROSCI.04-11-02877.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Grace A. A., Bunney B. S. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci. 1984 Nov;4(11):2866–2876. doi: 10.1523/JNEUROSCI.04-11-02866.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Griffith W. H. Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J Neurophysiol. 1988 May;59(5):1590–1612. doi: 10.1152/jn.1988.59.5.1590. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Hagiwara S., Takahashi K. The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol. 1974;18(1):61–80. doi: 10.1007/BF01870103. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Harris-Warrick R. M., Johnson B. R. Potassium channel blockade induces rhythmic activity in a conditional burster neuron. Brain Res. 1987 Jul 28;416(2):381–386. doi: 10.1016/0006-8993(87)90923-1. [DOI] [PubMed] [Google Scholar]
  26. Hassall C. J., Burnstock G. Intrinsic neurones and associated cells of the guinea-pig heart in culture. Brain Res. 1986 Jan 29;364(1):102–113. doi: 10.1016/0006-8993(86)90991-1. [DOI] [PubMed] [Google Scholar]
  27. Jones S. W. On the resting potential of isolated frog sympathetic neurons. Neuron. 1989 Aug;3(2):153–161. doi: 10.1016/0896-6273(89)90028-7. [DOI] [PubMed] [Google Scholar]
  28. Jones S. W. Sodium currents in dissociated bull-frog sympathetic neurones. J Physiol. 1987 Aug;389:605–627. doi: 10.1113/jphysiol.1987.sp016674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Malor R., Taylor S., Chesher G. B., Griffin C. J. The intramural ganglia and chromaffin cells in guinea pig atria: an ultrastructural study. Cardiovasc Res. 1974 Nov;8(6):731–744. doi: 10.1093/cvr/8.6.731. [DOI] [PubMed] [Google Scholar]
  30. Mayer M. L., Westbrook G. L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol. 1983 Jul;340:19–45. doi: 10.1113/jphysiol.1983.sp014747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Moravec M., Moravec J. Intrinsic innervation of the atrioventricular junction of the rat heart. Am J Anat. 1984 Nov;171(3):307–319. doi: 10.1002/aja.1001710307. [DOI] [PubMed] [Google Scholar]
  32. Selyanko A. A. Membrane properties and firing characteristics of rat cardiac neurones in vitro. J Auton Nerv Syst. 1992 Jul;39(3):181–189. doi: 10.1016/0165-1838(92)90011-5. [DOI] [PubMed] [Google Scholar]
  33. Selyanko A. A., Zidichouski J. A., Smith P. A. The effects of muscarine and adrenaline on patch-clamped frog cardiac parasympathetic neurones. J Physiol. 1991 Nov;443:355–370. doi: 10.1113/jphysiol.1991.sp018837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shepard P. D., Bunney B. S. Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca(2+)-activated K+ conductance. Exp Brain Res. 1991;86(1):141–150. doi: 10.1007/BF00231048. [DOI] [PubMed] [Google Scholar]
  35. Tanaka K., Kuba K. The Ca2+-sensitive K+-currents underlying the slow afterhyperpolarization of bullfrog sympathetic neurones. Pflugers Arch. 1987 Oct;410(3):234–242. doi: 10.1007/BF00580271. [DOI] [PubMed] [Google Scholar]
  36. Tokimasa T., Akasu T. Cyclic AMP regulates an inward rectifying sodium-potassium current in dissociated bull-frog sympathetic neurones. J Physiol. 1990 Jan;420:409–429. doi: 10.1113/jphysiol.1990.sp017920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weihe E., Reinecke M., Forssmann W. G. Distribution of vasoactive intestinal polypeptide-like immunoreactivity in the mammalian heart. Interrelation with neurotensin- and substance P-like immunoreactive nerves. Cell Tissue Res. 1984;236(3):527–540. doi: 10.1007/BF00217219. [DOI] [PubMed] [Google Scholar]
  38. Xi-Moy S. X., Randall W. C., Wurster R. D. Nicotinic and muscarinic synaptic transmission in canine intracardiac ganglion cells innervating the sinoatrial node. J Auton Nerv Syst. 1993 Mar;42(3):201–213. doi: 10.1016/0165-1838(93)90365-2. [DOI] [PubMed] [Google Scholar]
  39. Xi X. H., Thomas J. X., Jr, Randall W. C., Wurster R. D. Intracellular recordings from canine intracardiac ganglion cells. J Auton Nerv Syst. 1991 Feb;32(2):177–182. doi: 10.1016/0165-1838(91)90068-e. [DOI] [PubMed] [Google Scholar]
  40. Xi X., Randall W. C., Wurster R. D. Morphology of intracellularly labeled canine intracardiac ganglion cells. J Comp Neurol. 1991 Dec 8;314(2):396–402. doi: 10.1002/cne.903140213. [DOI] [PubMed] [Google Scholar]
  41. Xu Z. J., Adams D. J. Resting membrane potential and potassium currents in cultured parasympathetic neurones from rat intracardiac ganglia. J Physiol. 1992 Oct;456:405–424. doi: 10.1113/jphysiol.1992.sp019343. [DOI] [PMC free article] [PubMed] [Google Scholar]

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