Summary
Miniature end-plate currents (MEPCs) and acetylcholine-induced current fluctuations were recorded in voltageclamped, glycerol-treated toad sartorius muscle fibers in control solution and in solutions with added divalent cations. In isosmotic solutions containing 20mm Ca or Mg, MEPCs had time constants of decay (τ D ) which were about 30% slower than normal. In isotonic Ca solutions (Na-free), greater increases in both τ D and channel lifetime were seen; the null potential was −34 mV, and single-channel conductance decreased to approximately 5 pS. Zn or Ni, at concentrations of 0.1–5mm, were much more effective in increasing τ D than Ca or Mg, although they did not greatly affect channel conductance. The normal temperature and voltage sensitivity of τ was not significantly altered by any of the added divalent cations. Surface potential shifts arising from screening of membrane fixed charge by divalent cations cannot entirely explain the observed increases in τ, especially when taken together with changes in channel conductance.
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Adams, D.J., Dwyer, T.M., Hille, B. 1980. The permeability of end-plate channels to monovalent and divalent metal cations.J. Gen. Physiol. 75:493–510
Adams, P.R. 1976. Drug blockade of open end-plate channels.J. Physiol. (London) 260:531–552
Adams, P.R., 1977. Voltage jump analysis of procaine action at frog end-plate.J. Physiol. (London) 268:291–318
Adams, P.R., Sakmann, B. 1978. Decamethonium both opens and blocks end-plate channels.Proc. Natl. Acad. Sci. USA 75:2994–2998
Anderson, C.R., Stevens, C.F. 1973. Voltage clamp analysia of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction.J. Physiol. (London) 235:655–691
Armstrong, C.M. 1975. Channels and voltage dependent gates in nerve.In: Membranes — A Series of Advances. Artificial and Biological Membranes. G. Eisenman, editor. Vol. 3, pp. 325–358. Marcel Dekker, N.Y.
Armstrong, C.M., Gilly, W.F. 1979. Fast and slow steps in the activation of sodium channels.J. Gen. Physiol. 74:691–711
Ascher, P., Marty, A., Neild, T.O. 1978. Lifetime and elementary conductance of the channels mediating the excitatory effects of acetylcholine inAplysia neurones.J. Physiol. (London) 278:177–206
Bamberg, E., Läuger, P. 1977. Blocking of the Gramicidin channel by divalent cations.J. Membrane Biol. 35:351–375
Barry, P.H., Gage, P.W., Van Helden, D.F. 1979a. Cation permeation at the amphibian motor end-plate.J. Membrane Biol. 45:245–276
Barry, P.H., Gage, P.W., Van Helden, D.F. 1979b. Cation permeation through single end-plate channels.Excerpta Med. Int. Congr. Ser. 473:174–184
Begenisich, T., Lynch, C. 1974. Effects of internal divalent cations on voltage-clamped squid axons.J. Gen. Physiol. 63:675–689
Blaustein, M.P., Goldman, D.E. 1968. The action of certain polyvalent cations on the voltage-clamped lobster axon.J. Gen. Physiol. 51:279–291
Bregestovski, P.D., Miledi, R., Parker, I. 1979. Calcium conductance of acetylcholine induced end-plate channels.Nature (London) 279:638–639
Cohen, I., Van der Kloot, W.G. 1978. Effects of [Ca2+] and [Mg2+] on the decay of miniature end-plate currents.Nature (London) 271:77–79
Dwyer, T.M., Adams, D.J., Hille, B. 1980. The permeability of end-plate channels to organic cations in frog muscle.J. Gen. Physiol. 75:469–492
Frankenhaeuser, B., Hodgkin, A.L. 1957. The action of calcium on the electrical properties of squid axons.J. Physiol. (London) 137:218–244
Gage, P.W., McBurney, R.N. 1975. Effects of membrane potential, temperature and neostigmine on the conductance change caused by a quantum of acetylcholine at the toad neuromuscular junction.J. Physiol. (London) 244:385–407
Gage, P.W., McBurney, R.N., Van Helden, D.F. 1978. Octanol reduces end-plate channel lifetime.J. Physiol. (London) 274:279–298
Gage, P.W., Van Helden, D.F. 1979. Effects of permeant monovalent cations on end-plate channels.J. Physiol. (London) 288:509–528
Grahame, D.C. 1947. The electrical double layer and the theory of electrocapillarity.Chem. Rev. 41:441–501
Hille, B., Woodhull, A.M., Shapiro, B.I. 1975. Negative surface charge near sodium channels of nerve: Divalent ions, monovalent ions and pH.Philos. Trans. R. Soc. London B. 270:301–318
Katz, B., Miledi, R. 1969. Spontaneous and evoked activity of motor nerve endings in calcium Ringer.J. Physiol. (London) 203:689–706
Katz, B., Miledi, R. 1973. The binding of acetylcholine to receptors and its removal from the synaptic cleft.J. Physiol. (London) 231:549–574
Kehoe, J.S. 1972. Ionic mechanisms of a two-component cholinergic inhibition inAplysia neurones.J. Physiol. (London) 225:85–114
Kolb, H.A., Bamberg, E. 1977. Influence of membrane thickness and ion concentration on the properties of the Gramicidin A channel. Autocorrelation, spectral power density, relaxation and single channel properties.Biochim. Biophys. Acta 464:127–141
Lewis, C.A. 1979. Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction.J. Physiol. (London) 286:417–445
Lewis, C.A., Stevens, C.F. 1979. Mechanism of ion permeation through channels in a postsynaptic membrane.In: Membrane Transport Processes. C.F. Stevens, and R.W. Tsien, editors. Vol. 3, pp. 133–151. Raven Press, N.Y.
Linder, T.M., Quastel, D.M.J. 1978. A voltage-clamp study of the permeability change induced by quanta of transmitter at the mouse end-plate.J. Physiol. (London) 281:535–556
Magleby, K.L., Stevens, C.F. 1972 A quantitative description of end-plate currents.J. Physiol. (London) 223:173–197
Magleby, K.L., Weinstock, M.M. 1980. Nickel and calcium ions modify the characteristics of the acetylcholine receptor-channel complex at the frog neuromuscular junction.J. Physiol. (London) 299:203–218
Mallart, A., Molgó, J. 1978. The effects of pH and curare on the time course of end-plate currents at the neuromuscular junction of the frog.J. Physiol. (London) 276:343–352
Marchais, D., Marty, A. 1979. Interaction of permeant ions with channels activated by acetylcholine inAplysia neurones.J. Physiol. (London) 297:9–45
McLaughlin, S.G.A., Szabo, G., Eisenman, G. 1971. Divalent ions and the surface potential of charged phospholipid membranes.J. Gen. Physiol. 58:667–687
Miledi, R., Parker, I. 1980. Effects of strontium ions on end-plate channel properties.J. Physiol. (London) 306:567–577
Neher, E., Steinbach, J.H. 1978. Local anaesthetics transiently block currents through single acetylcholine channels.J. Physiol. (London) 277:153–176
Nonner, W., Adams, D.J., Dwyer, T.M., Hille, B. 1980. Conductance fluctuation measurements with organic cations at the end-plate channel.Fed. Proc. 39:2064
Rang, H.P. 1975. Acetylcholine receptors.Quart. Rev. Biophys. 7:283–399
Ruff, R.L. 1977. A quantitative analysis of local anaesthetic alteration of miniature end-plate currents and end-plate current fluctuations.J. Physiol. (London) 264:89–124
Scuka, M. 1975. The amplitude and the time course of the end-plate current at various pH levels in the frog sartorius muscle.J. Physiol. (London) 249:183–195
Takeda, K., Barry, P.H., Gage, P.W. 1980a. Effects of ammonium ions on end-plate channels.J. Gen. Physiol. 75:589–613
Takeda, K., Barry, P.H., Gage, P.W. 1980b. Divalent cations lengthen channel lifetime at the toad neuromuscular junction.Proc. Aust. Soc. Biophys. 4:2A
Takeda, K., Datyner, N.B., Barry, P.H., Gage, P.W. 1978. Postsynaptic effects of Zn2+ at the motor end-plate.Proc. Aust. Physiol. Pharmacol. Soc. 9:126P
Takeuchi, A., Takeuchi, N. 1959. Active phase of frog's end-plate potential.J. Neurophysiol. 22:395–411
Takeuchi, A., Takeuchi, N. 1960. On the permeability of end-plate membrane during the action of transmitter.J. Physiol. (London) 154:52–67
Van der Kloot, W.G., Cohen, I. 1979. Membrane surface potential changes may alter drug interactions: An example, acetylcholine and curare.Science 203:1351–1353
Van Helden, D.F., Hamill, O.P., Gage, P.W. 1977. Permeant cations alter end-plate channel characteristics.Nature (London) 269:711–713
Watanabe, S., Narahashi, T. 1979. Cation selectivity of acetylcholine-activated ionic channels of frog end-plate.J. Gen. Physiol. 74:615–628
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Takeda, K., Gage, P.W. & Barry, P.H. Effects of divalent cations on toad end-plate channels. J. Membrain Biol. 64, 55–66 (1982). https://doi.org/10.1007/BF01870768
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DOI: https://doi.org/10.1007/BF01870768