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. 1982 Sep;330:537–572. doi: 10.1113/jphysiol.1982.sp014357

M-currents and other potassium currents in bullfrog sympathetic neurones

P R Adams 1,*, D A Brown 1,†, A Constanti 1,†
PMCID: PMC1225314  PMID: 6294290

Abstract

1. Bullfrog lumbar sympathetic neurones were voltage-clamped in vitro through twin micro-electrodes. Four different outward (K+) currents could be identified: (i) a large sustained voltage-sensitive delayed rectifier current (IK) activated at membrane potentials more positive than -25 mV; (ii) a calcium-dependent sustained outward current (IC) activated at similar positive potentials and peaking at +20 to +60 mV; (iii) a transient current (IA) activated at membrane potentials more positive than -60 mV after a hyperpolarizing pre-pulse, but which was rapidly and totally inactivated at all potentials within its activation range; and (iv) a new K+ current, the M-current (IM).

2. IM was detected as a non-inactivating current with a threshold at -60 mV. The underlying conductance GM showed a sigmoidal activation curve between -60 and -10 mV, with half-activation at -35 mV and a maximal value (ḠM) of 84±14 (S.E.M.) nS per neurone. The voltage sensitivity of GM could be expressed in terms of a simple Boltzmann distribution for a single multivalent gating particle.

3. IM activated and de-activated along an exponential time course with a time constant uniquely dependent upon voltage, maximizing at ≃ 150 ms at -35 mV at 22 °C.

4. Instantaneous current—voltage (I/V) curves were approximately linear in the presence of IM, suggesting that the M-channels do not show appreciable rectification. However, the time- and voltage-dependent opening of the M-channels induced considerable rectification in the steady-state I/V curves recorded under both voltage-clamp and current-clamp modes between -60 and -25 mV. Both time- and voltage-dependent rectification in the voltage responses to current injection over this range could be predicted from the kinetic properties of IM.

5. It is suggested that IM exerts a strong potential-clamping effect on the behaviour of these neurones at membrane potentials subthreshold to excitation.

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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. Aldrich R. W. Inactivation of voltage-gated delayed potassium current in molluscan neurons. A kinetic model. Biophys J. 1981 Dec;36(3):519–532. doi: 10.1016/S0006-3495(81)84750-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aldrich R. W., Jr, Getting P. A., Thompson S. H. Inactivation of delayed outward current in molluscan neurone somata. J Physiol. 1979 Jun;291:507–530. doi: 10.1113/jphysiol.1979.sp012828. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arnett D., Spraker T. E. Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J Physiol. 1981 Aug;317:29–47. doi: 10.1113/jphysiol.1981.sp013812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BLACKMAN J. G., GINSBORG B. L., RAY C. Synaptic transmission in the sympathetic ganglion of the frog. J Physiol. 1963 Jul;167:355–373. doi: 10.1113/jphysiol.1963.sp007155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barrett E. F., Barrett J. N., Crill W. E. Voltage-sensitive outward currents in cat motoneurones. J Physiol. 1980 Jul;304:251–276. doi: 10.1113/jphysiol.1980.sp013323. [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., Constanti A., Adams P. R. Slow cholinergic and peptidergic transmission in sympathetic ganglia. Fed Proc. 1981 Sep;40(11):2625–2630. [PubMed] [Google Scholar]
  9. Brown H. F., Clark A., Noble S. J. Analysis of pace-maker and repolarization currents in frog atrial muscle. J Physiol. 1976 Jul;258(3):547–577. doi: 10.1113/jphysiol.1976.sp011435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brown H., Difrancesco D. Voltage-clamp investigations of membrane currents underlying pace-maker activity in rabbit sino-atrial node. J Physiol. 1980 Nov;308:331–351. doi: 10.1113/jphysiol.1980.sp013474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. DiFrancesco D., Noma A., Trautwein W. Kinetics and magnitude of the time-dependent potassium current in the rabbit sinoatrial node: effect of external potassium. Pflugers Arch. 1979 Sep;381(3):271–279. doi: 10.1007/BF00583259. [DOI] [PubMed] [Google Scholar]
  14. Dubois J. M., Bergman C. Potassium accumulation in the perinodal space of frog myelinated axons. Pflugers Arch. 1975 Jul 21;358(2):111–124. doi: 10.1007/BF00583922. [DOI] [PubMed] [Google Scholar]
  15. Dubois J. M. Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J Physiol. 1981 Sep;318:297–316. doi: 10.1113/jphysiol.1981.sp013865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dubois J. M. Simultaneous changes in the equilibrium potential and potassium conductance in voltage clamped Ranvier node in the frog. J Physiol. 1981 Sep;318:279–295. doi: 10.1113/jphysiol.1981.sp013864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ehrenstein G., Blumenthal R., Latorre R., Lecar H. Kinetics of the opening and closing of individual excitability-inducing material channels in a lipid bilayer. J Gen Physiol. 1974 Jun;63(6):707–721. doi: 10.1085/jgp.63.6.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ehrenstein G., Gilbert D. L. Slow changes of potassium permeability in the squid giant axon. Biophys J. 1966 Sep;6(5):553–566. doi: 10.1016/S0006-3495(66)86677-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. FRANKENHAEUSER B. A QUANTITATIVE DESCRIPTION OF POTASSIUM CURRENTS IN MYELINATED NERVE FIBRES OF XENOPUS LAEVIS. J Physiol. 1963 Nov;169:424–430. doi: 10.1113/jphysiol.1963.sp007268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. FRANKENHAEUSER B., HODGKIN A. L. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol. 1956 Feb 28;131(2):341–376. doi: 10.1113/jphysiol.1956.sp005467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. HUNT C. C., NELSON P. G. STRUCTURAL AND FUNCTIONAL CHANGES IN THE FROG SYMPATHETIC GANGLION FOLLOWING CUTTING OF THE PRESYNAPTIC NERVE FIBRES. J Physiol. 1965 Mar;177:1–20. doi: 10.1113/jphysiol.1965.sp007571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Lee K. S., Weeks T. A., Kao R. L., Akaike N., Brown A. M. Sodium current in single heart muscle cells. Nature. 1979 Mar 15;278(5701):269–271. doi: 10.1038/278269a0. [DOI] [PubMed] [Google Scholar]
  25. Maughan D. W. Some effects of prolonged polarization on membrane currents in bullfrog atrial muscle. J Membr Biol. 1973;11(4):331–352. doi: 10.1007/BF01869829. [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. Moolenaar W. H., Spector I. Ionic currents in cultured mouse neuroblastoma cells under voltage-clamp conditions. J Physiol. 1978 May;278:265–286. doi: 10.1113/jphysiol.1978.sp012303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NISHI S., KOKETSU K. Electrical properties and activities of single sympathetic neurons in frogs. J Cell Comp Physiol. 1960 Feb;55:15–30. doi: 10.1002/jcp.1030550104. [DOI] [PubMed] [Google Scholar]
  29. Neher E., Lux H. D. Properties of somatic membrane patches of snail neurons under voltage clamp. Pflugers Arch. 1971;322(1):35–38. doi: 10.1007/BF00586662. [DOI] [PubMed] [Google Scholar]
  30. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. doi: 10.1085/jgp.58.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nishi S., Soeda H., Koketsu K. Studies on sympathetic B and C neurons and patterns of pregnaglionic innervation. J Cell Physiol. 1965 Aug;66(1):19–32. doi: 10.1002/jcp.1030660103. [DOI] [PubMed] [Google Scholar]
  32. Noble D., Tsien R. W. The kinetics and rectifier properties of the slow potassium current in cardiac Purkinje fibres. J Physiol. 1968 Mar;195(1):185–214. doi: 10.1113/jphysiol.1968.sp008454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Noble S. J. Potassium accumulation and depletion in frog atrial muscle. J Physiol. 1976 Jul;258(3):579–613. doi: 10.1113/jphysiol.1976.sp011436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Noma A., Irisawa H. Membrane currents in the rabbit sinoatrial node cell as studied by the double microelectrode method. Pflugers Arch. 1976 Jun 29;364(1):45–52. doi: 10.1007/BF01062910. [DOI] [PubMed] [Google Scholar]
  35. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tosaka T., Chichibu S., Libet B. Intracellular analysis of slow inhibitors and excitatory postsynaptic potentials in sympathetic ganglia of the frog. J Neurophysiol. 1968 May;31(3):396–409. doi: 10.1152/jn.1968.31.3.396. [DOI] [PubMed] [Google Scholar]
  37. Weitsen H. A., Weight F. F. Synaptic innervation of sympathetic ganglion cells in the bullfrog. Brain Res. 1977 Jun 10;128(2):197–211. doi: 10.1016/0006-8993(77)90988-x. [DOI] [PubMed] [Google Scholar]
  38. Yanagihara K., Irisawa H. Inward current activated during hyperpolarization in the rabbit sinoatrial node cell. Pflugers Arch. 1980 May;385(1):11–19. doi: 10.1007/BF00583909. [DOI] [PubMed] [Google Scholar]

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