Skip to main content
Log in

Characteristics of fast excitatory postsynaptic current in bullfrog sympathetic ganglion cells

Effects of membrane potential, temperature and Ca ions

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The membrane current underlying the fast excitatory postsynaptic potential (EPSC) of bullfrog sympathetic ganglion cells was studied. The relationship between the EPSC amplitude and membrane potential was linear at negative levels of membrane potential, but deviated from the linearity toward a smaller amplitude at positive levels. The falling phase of EPSC almost followed a single exponential decay. The half-decay time (HDT) of EPSC's increased exponentially with an increase in the negativity of membrane potential. The rise time (RT) was also prolonged slightly with membrane hyperpolarization. Lowering of temperature decreased the EPSC amplitude, lengthened markedly the HDT and increased the slope relating the logarithm of the HDT to membrane potential. Neostigmine (1×10−5 M) prolonged both the RT and HDT. A decrease in Ca2+ concentration caused a marked reduction in the EPSC amplitude, and a slight shortening in the RT and HDT. An increase in Ca2+ concentration significantly prolonged the RT and HDT without altering the slope of the relationship between the HDT and membrane potential, while the amplitude of EPSC was increased slightly. The HDT was independent of EPSC amplitude. It is suggested that the mechanism responsible for closing the ion channels of the nicotinic receptor at the subsynaptic membrane is regulated by membrane potential. The possible mechanisms of the action of Ca2+ on the decay phase of EPSC were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams, D. J., Gage, P. W., Hamill, O. P.: Voltage sensitivity of inhibitory postsynaptic currents inAplysia buccal ganglia. Brain Res.115, 506–511 (1976)

    Google Scholar 

  • Adrian, R. H.: The effect of internal and external potassium concentration on the membrane potential of frog muscle. J. Physiol. (Lond.)133, 631–658 (1956)

    Google Scholar 

  • Albuquerque, E. X., Kuba, K., Daly, J.: Effect of histrionicotoxin on the ionic conductance modulator of the cholinergic receptor: A quantitative analysis of the end-plate current. J. Pharmacol. Exp. Ther.189, 513–524 (1974)

    Google Scholar 

  • Anderson, C. R., Stevens, C. F.: Voltage clamp analysis of acetylcholine produced end-plate current fluctuations at frog neuromuscular junction. J. Physiol. (Lond.)235, 655–691 (1973)

    Google Scholar 

  • Anderson, C. R., Cull-Candy, S. G., Miledi, R.: Glutamate and quisqualate noise in voltage-clamped locust muscle fibers. Nature261, 151–153 (1976)

    Google Scholar 

  • Barrett, E. F., Stevens, C. F.: The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. (Lond.)227, 691–708 (1972)

    Google Scholar 

  • Blackman, J. G., Ginsborg, B. L., Ray, C.: Synaptic transmission in the sympathetic ganglion of the frog. J. Physiol. (Lond.)167, 355–373 (1963)

    Google Scholar 

  • Chang, C. C., Lee, C. Y.: Electrophysiological study of neuromuscular blocking action of cobra neurotoxin. Br. J. Pharmacol. Chemother.28, 172–181 (1966).

    Google Scholar 

  • Chang, H. W., Neumann, E.: Dynamic properties of isolated acetylcholine receptor proteins: Release of calcium ions caused by acetylcholine binding. Proc. Natl. Acad. Sci. U.S.A.73, 3364–3368 (1976)

    Google Scholar 

  • Changeux, J.-P., Kasai, M., Lee, C. Y.: Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc. Natl. Acad. Sci. U.S.A.67, 1241–1247 (1970)

    Google Scholar 

  • Cohen, I., Van der Kloot, W.: Effects of [Ca2+] and [Mg2+] on the decay of miniature endplate currents. Nature271, 77–79 (1978)

    Google Scholar 

  • Dionne, V. E., Stevens, C. F.: Voltage dependence of agonist effectiveness at the frog neuromuscular junction: resolution of a paradox. J. Physiol. (Lond.)251, 245–270 (1975)

    Google Scholar 

  • Dudel, J.: Nonlinear voltage dependence of excitatory synaptic current in crayfish muscle. Pflügers Arch.352, 227–241 (1974)

    Google Scholar 

  • Feltz, A., Large, W. A., Trautmann, A.: Analysis of atropine action at the frog neuromuscular junction. J. Physiol. (Lond.)269, 109–130 (1977)

    Google Scholar 

  • Frankenhauser, B., Hodgkin, A. L.: The action of calcium on the electrical properties of squid axons. J. Physiol. (Lond.)137, 218–244 (1957)

    Google Scholar 

  • Gage, P. W.: Generation of end-plate potentials. Physiol. Rev.56, 177–247 (1976)

    Google Scholar 

  • Gage, P. W., Mcburney, R. N.: Effects of membrane potential, temperature and neostigmine on the conductance change caused by a quantum of acetylcholine at the toad neuromuscular junction. J. Physiol. (Lond.)244, 385–407 (1975)

    Google Scholar 

  • Ginsborg, B. L., Guerrero, S.: On the action of depolarizing drugs on sympathetic ganglion cells of the frog. J. Physiol. (Lond.)172, 189–206 (1964)

    Google Scholar 

  • Kato, E., Kuba, K., Koketsu, K.: Effects of elabutoxins on neuromuscular transmission in frog skeletal muscles. J. Pharmacol. Exp. Ther.204, 446–453 (1978)

    Google Scholar 

  • Katz, B.: The release of neuronal transmitter substances. Springfield, Ill.: Ch. C. Thomas 1969

    Google Scholar 

  • Katz, B., Miledi, R.: The measurement of synaptic delay, and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Lond. [Biol.]161, 483–495 (1965)

    Google Scholar 

  • Katz, B., Miledi, R.: The statistical nature of the acetylcholine potential and its molecular components. J. Physiol. (Lond.)224, 665–699 (1972)

    Google Scholar 

  • Katz, B., Miledi, R.: The binding of acetylcholine to receptors and its removal from the synaptic cleft. J. Physiol. (Lond.)231, 549–574 (1973)

    Google Scholar 

  • Koketsu, K.: Cholinergic synaptic potentials and the underlying ionic mechanisms. Fed. Proc.28, 101–111 (1969)

    Google Scholar 

  • Kordas, M.: An attempt at an analysis of the factors determining the time course of the end-plate current, I. The effects of prostigmine and of the ratio of Mg2+ to Ca2+ J. Physiol. (Lond.)224, 317–332 (1972a)

    Google Scholar 

  • Kordas, M.: An attempt at an analysis of the factors determining the time course of the end-plate current, II. Temperature. J. Physiol. (Lond.)224, 333–348 (1972b)

    Google Scholar 

  • Kuba, K.: Ca2+ and the action of acetylcholine on the subsynaptic membrane. In: Neurobiology of chemical transmission (M. Otsuka, Z. W. Hall, eds.). New York: John Wiley and Sons Inc. (in press, 1978)

    Google Scholar 

  • Kuba, K., Nishi, S.: Membrane current associated with the fast EPSP of sympathetic neurons. Physiologist14, 176 (1971)

    Google Scholar 

  • Kuba, K., Albuquerque, E. X., Barnard, E. A.: Diisopropylfluorophosphate: Suppression of ionic conductance of the cholinergic receptor. Science181, 853–855 (1973)

    Google Scholar 

  • Kuba, K., Albuquerque, E. X., Daly, J., Barnard, E. A.: A study of the irreversible cholinesterase inhibitor, diisopropylfluorophosphate, on time course of end-plate currents in frog sartorius muscle. J. Pharmacol. Exp. Ther.189, 499–512 (1974)

    Google Scholar 

  • Kuba, K., Chikazawa, K., Koketsu, K.: Novel action of a piperazine derivative on the end-plate of the frog. Jap. J. Physiol.26, 159–175 (1976)

    Google Scholar 

  • Kuba, K., Koketsu, K.: Synaptic events in sympathetic ganglia: Progress in neurobiology (J. W. Phillis, ed.), Oxford-New York, Pergamon Press (in press, 1978)

    Google Scholar 

  • Lambert, D. H., Parsons, R. L.: Influence of polyvalent cations on the activation of muscle end-plate receptors. J. Gen. Physiol.56, 309–321 (1970)

    Google Scholar 

  • Maeno, T., Edwards, C., Hashimura, S.: Difference in effects on end-plate potentials between procaine and lidocaine as revealed by voltage-clamp experiments. J. Neurophysiol.34, 32–46 (1971)

    Google Scholar 

  • Magazanik, L. G., Vyskočil, F.: Dependence of acetylcholine desensitization on the membrane potential of frog muscle fibre and on the ionic changes in the medium. J. Physiol. (Lond.)210, 507–518 (1970)

    Google Scholar 

  • Magazanik, L. G., Ivanov, A. Ya., Lukomskaya, N. Ya.: Inability of snake venom polypeptides to block the cholinoreception in the isolated sympathetic ganglion of rabbit. Neurophysiology6, 652–654 (1974) (in Russian)

    Google Scholar 

  • Magleby, K. L., Stevens, C. F.: The effect of voltage on the time course of end-plate currents. J. Physiol. (Lond.)223, 151–171 (1972a)

    Google Scholar 

  • Magleby, K. L., Stevens, C. F.: A quantitative description of end-plate currents. J. Physiol. (Lond.)223, 173–197 (1972b)

    Google Scholar 

  • Mallart, A., Molgó, J.: The effects of pH and curare on the time course of end-plate currents at the neuromuscular junction of the frog. J. Physiol. (Lond.)276, 343–352 (1978)

    Google Scholar 

  • Mallart, A., Dreyer, F., Peper, K.: Current-voltage relation and reversal potential at junctional and extrajunctional ACh-receptors of the frog neuromuscular junction. Pflügers Arch.362, 43–47 (1976)

    Google Scholar 

  • Nachmansohn, D.: Action of ions on choline esterase. Nature145, 513–514 (1940)

    Google Scholar 

  • Nastuk, W. L., Liu, J. H.: Muscle postjunctional membrane: changes in chemosensitivity produced by calcium. Science154, 266–267 (1966)

    Google Scholar 

  • Nastuk, W. L., Parsons, R. L.: Factors in the inactivation of postjunctional membrane receptors of frog skeletal muscle. J. Gen. Physiol.56, 218–249 (1970)

    Google Scholar 

  • Neher, E., Sakman, B.: Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature260, 799–801 (1976)

    Google Scholar 

  • Nishi, S.: Ganglionic transmission. In: The peripheral nervous system, pp. 225–255 (J. I. Hubbard, ed.). New York-London: Plenum Press 1974

    Google Scholar 

  • Nishi, S., Koketsu, K.: Electrical properties and activities of single sympathetic neurons in frogs. J. Cell Comp. Physiol.55, 15–30 (1960)

    Google Scholar 

  • Nishi, S., Koketsu, K.: Excitatory and inhibitory postsynaptic potentials of amphibian sympathetic ganglion cells. Fed. Proc.26, 329 (1967)

    Google Scholar 

  • Onodera, K., Takeuchi, A.: Effects of membrane potential and temperature on the excitatory post-synaptic current in the crayfish muscle. J. Physiol. (Lond.)276, 183–192 (1978)

    Google Scholar 

  • Oomura, Y., Tomita, T.: Studies on properties of neuromuscular junction. In: Electrical Activity of Single Cells, pp. 181–205 (Y. Katsuki, ed.). Tokyo: Igaku-shoin 1960

    Google Scholar 

  • Paton, W. D. M., Perry, W. L. M.: The relationship between depolarization and block in the cat's superior cervical ganglion. J. Physiol. (Lond.)119, 43–57 (1953)

    Google Scholar 

  • Scuka, M.: The amplitude and the time course of the end-plate current at various pH levels in the frog sartorius muscle. J. Physiol. (Lond.)249, 183–195 (1975)

    Google Scholar 

  • Takeuchi, A., Takeuchi, N.: Active phase of frog's end-plate potential. J. Neurophysiol.22, 395–411 (1959)

    Google Scholar 

  • Takeuchi, A., Takeuchi, N.: On the permeability of end-plate membrane during the action of transmitter. J. Physiol. (Lond.)154, 52–67 (1960)

    Google Scholar 

  • Takeuchi, N.: Effects of calcium on the conductance changes at the end-plate membrane during the action of transmitter. J. Physiol. (Lond.)167, 141–155 (1963)

    Google Scholar 

  • Taxi, J.: Etude de l'ultrastructure des zones synaptiques dans les ganglions sympathiques de la grenouille. C. R. Acad. Sci. (Paris)252, 174–176 (1961)

    Google Scholar 

  • Trautmann, A., Zilber-Gachelin, N. F.: Further investigations on the effect of denervation and pH on the conductance change at the neuromuscular junction of the frog. Pflügers Arch.364, 53–58 (1976)

    Google Scholar 

  • Wilson, I. B., Cabib, E.: Is acetylcholineesterase a metallo enzyme? J. Am. Chem. Soc.76, 5154–5156 (1954)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuba, K., Nishi, S. Characteristics of fast excitatory postsynaptic current in bullfrog sympathetic ganglion cells. Pflugers Arch. 378, 205–212 (1979). https://doi.org/10.1007/BF00592737

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00592737

Key words

Navigation