Summary
Delayed potassium channels were studied in internally perfused neurone somata from land snails. Relaxation and fluctuation analysis of this class of ion channels revealed Hodgkin-Huxley type K channels with an average single channel conductance (γ K) of 2.40±0.15 pS. The conductance of open channels is independent of voltage and virtually all K channels seem to be open at maximum K conductance (g K) of the membrane. Voltage dependent time constants of activation ofg K, calculated from K current relaxation and from cut-off frequencies of power spectra, are very similar indicating dominant first-order kinetics. Ion selectivity of K channels was studied by ion substitution in the external medium and exhibited the following sequence: T1+>K+>Rb+>Cs+>NH +4 >Li+>Na+. The sequence of the alkali cations does not conform to any of the sequences predicted by Eisenman's theory. However, the data are well accommodated by a new theory assuming a single rate-limiting barrier that governs ion movement through the channel.
Similar content being viewed by others
References
Adams, D.J., Gage, P.W. 1979. Ionic currents in response to membrane depolarization in anAplysia neurone.J. Physiol. (London) 289:115
Anderson, C.R., Stevens, C.F. 1973. Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction.J. Physiol. (London) 235:655
Armstrong, C.M. 1975. Ionic pores, gates, and gating currents.Q. Rev. Biophys. 7:179
Begenisich, T., Stevens, C.F. 1975. How many conductance states do potassium channels have?Biophys. J. 15:843
Bezanilla, F., Armstrong, C.M. 1972. Negative conductance caused by entry of sodium and cesium ions into the potassium channels of squid axons.J. Gen. Physiol. 60:588
Bockris, J.O'M., Reddy, A.K.N. 1973. Modern Electrochemistry, Vol. 1. Plenum, New York
Born, M. 1920. Volumen und Hydratationswärme der Ionen.Z. Phys. 1:45
Buckingham, A.D. 1957. A theory of ion-solvent interaction.Faraday Soc. Disc. 24:151
Connor, J.A., Stevens, C.F. 1971a. Inward and delayed outward membrane currents in isolated neural somata under voltage clamp.J. Physiol. (London) 213:1
Connor, J.A., Stevens, C.F. 1971b. Voltage clamp studies of a transient outward membrane current in gastropod neural somata.J. Physiol. (London) 213:21
Conti, F., DeFelice, L.J., Wanke, E. 1975. Potassium and sodium ion current noise in the membrane of the squid giant axon.J. Physiol. (London) 248:45
Diamond, J.M., Wright, E.M. 1969. Biological membranes: The physical basis of ion and nonelectrolyte selectivity.Annu. Rev. Physiol. 31:581
Dogonadze, R.R., Kornyshev, A.A. 1974. Polar solvent structure in the theory of ionic solvation.J. Chem. Soc. Faraday Trans. 2.70:1121
Eisenman, G. 1963. Cation selective glass electrodes and their mode of operation.Biophys. J. 2 (suppl. 2):259
Fishman, H.M., Moore, L.E., Poussart, D.J.M. 1975. Potassiumion conduction noise in squid axon membrane.J. Membrane Biol. 24:305
Gay, L.A., Stanfield, P.R. 1978. The selectivity of the delayed potassium conductance of frog skeletal muscle fibers.Pfluegers Arch. 378:177
Goldman, D.E. 1943. Potential impedance and rectification in membranes.J. Gen. Physiol. 27:37
Heyer, C.B., Lux, H.D. 1976. Control of the delayed outward potassium currents in bursting pace-makers neurones of the snail.Helix Pomatia.J. Physiol. (London) 262:349
Hille, B. 1973. Potassium channels in myelinated nerve. Selective permeability to small ions.J. Gen. Physiol. 61:669
Hille, B. 1975. Ionic selectivity of Na and K channels of nerve membranes.In: Membranes — A Series of Advances, Vol. 3, Dynamic Properties of Lipid Bilayers & Biological Membranes. G. Eisenman, editor. p. 255. Marcel Dekker, Inc., New York
Hille, B. 1977. Ionic basis of resting and action potentials.In: Handbook of Physiology, The Nervous System I. E. Kandel, editor. p. 99. Williams & Wilkin, Baltimore
Hodgkin, A.L., Katz, B. 1949. The effect of sodium ions on the electrical activity of the giant axon of the squid.J. Physiol. (London) 108:37
Horn, R., Stevens, C.F. 1980. Relation between structure and function of ion channels.Comm. Mol. Cell. Biophys. (in press)
Huang, L.M., Catterall, W.A., Ehrenstein, G. 1978. Selectivity of cations and nonelectrolytes for acetylcholine-activated channels in cultured muscle cells.J. Gen. Physiol. 71:397
Joesten, M.D., Schaad, L.J. 1974. Hydrogen Bonding. Marcel Dekker, Inc., New York
Kostyuk, P.G., Krishtal, O.A. 1977. Separation of sodium and calcium currents in the somatic membrane of mollusc neurones.J. Physiol. (London) 270:545
Kostyuk, P.G., Krishtal, O.A., Doroshenko, P.A. 1975. Outward currents in isolated snail neurones. II. Effect of TEA.Comp. Biochem. Physiol. 51C:265
Kostyuk, P.G., Krishtal, O.A., Pidoplichko, U.T. 1975. Effects of internal fluoride and phosphate on membrane currents during intracellular dialysis of nerve cells.Nature (London) 257:691
Krasne, S., Eisenman, G. 1973. The molecular basis of ion selectivity.In: Membranes—A Series of Advances, Vol. 2, G. Eisenman, editor. p. 179. Marcel Dekker, Inc., New York
Lee, A.G. 1977. The coordination chemistry of thallium (I).Coord. Chem. Rev. 8:281
Lee, K.S., Akaike, N., Brown, A.M. 1978. Properties of internally perfused, voltage clamped, isolated nerve cell bodies.J. Gen. Physiol. 71:489
Matsuoka, O., Clementi, E., Yoshimine, M. 1976. Cl study of the water dimer potential surface.J. Chem. Phys. 64:1351
Meech, R.W. 1978. Calcium-dependent potassium activation in nervous tissue.Ann. Rev. Biophys. Bioeng. 7:1
Meech, R.W., Standen, N.B. 1975. Potassium activation inHelix aspersa neurones under voltage clamp: A component mediated by calcium influx.J. Physiol. (London) 249:211
Meves, H. 1968. The ionic requirements for the production of action potentials inHelix pomatia neurones.Pfluegers Arch. 304:215
Neher, E. 1971. Two fast transient current components during voltage clamp on snail neurones.J. Gen. Physiol. 58:36
Neher, E., Lux, H.D. 1973. Rapid changes of potassium concentration at the outer surface of exposed neurones during membrane current flow.J. Gen. Physiol. 61:385
Neher, E., Stevens, C.F. 1977. Conductance fluctuations and ionic pores in membranes.Annu. Rev. Biophys. Bioeng. 6:345
Noyes, R.M. 1962. Thermodynamics of ion hydration as a measure of effective dielectric properties of water.J. Am. Chem. Soc. 84:513
Partridge, L.D., Stevens, C.F. 1976. A mechanism for spike frequency adaptation.J. Physiol. (London) 256:315
Payzant, J.D., Cunningham, A.J., Kebarle, P. 1973. Gas phase solvation of the ammonium ion by NH3 and H2O and stabilities of mixed clusters NHa(NH3)n(H2O)w.Can. J. Chem. 51:3242
Robinson, R.A., Stokes, R.H. 1959. Electrolyte Solutions. Butterworths, London
Scheiner, S., Kern, C.W. 1977. Theoretical studies of environmental effects on protein conformation. 1. Flexibility of the peptide bond.J. Am. Chem. Soc. 99:7042
Siebenga, E., Meyer, A.W.A., Verveen, A.A. 1973. Membrane shotnoise in electrically depolarized nodes ofRanvier.Pfluegers Arch. 341:87
Sigworth, F.J. 1979. Analysis of nonstationary sodium current fluctuations in frog myelinated nerve. Ph.D. Thesis, Yale University, New Haven, Connecticut
Stevens, C.F. 1972. Inferences about membrane properties from electrical noise measurements.Biophys. J. 12:1028
Stevens, C.F., Tsien, R.W. 1979. Membrane Transport Processes. Vol. 3. Ion Permeation Through Membrane Channels. Raven Press, New York
Thompson, S.H. 1977. Three pharmacologically distinct potassium channels in molluscan neurones.J. Physiol. (London) 265:465
Wolbarsht, M.L., MacNichol, E.F., Wagner, H.G. 1960. Glass insulated platinum electrode.Science 132:1309
Author information
Authors and Affiliations
Additional information
This paper is dedicated to the memory of Walther Wilbrandt.
Rights and permissions
About this article
Cite this article
Reuter, H., Stevens, C.F. Ion conductance and ion selectivity of potassium channels in snail neurones. J. Membrain Biol. 57, 103–118 (1980). https://doi.org/10.1007/BF01868997
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF01868997