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. 1968 Mar 1;51(3):321–345. doi: 10.1085/jgp.51.3.321

The Ionic Permeability Changes during Acetylcholine-Induced Responses of Aplysia Ganglion Cells

Makoto Sato 1, George Austin 1, Hideko Yai 1, Juro Maruhashi 1
PMCID: PMC2201135  PMID: 5648831

Abstract

ACh-induced depolarization (D response) in D cells markedly decreases as the external Na+ is reduced. However, when Na+ is completely replaced with Mg++, the D response remains unchanged. When Na+ is replaced with Tris(hydroxymethyl)aminomethane, the D response completely disappears, except for a slight decrease in membrane resistance. ACh-induced hyperpolarization (H response) in H cells is markedly depressed as the external Cl- is reduced. Frequently, the reversal of the H response; i.e., depolarization, is observed during perfusion with Cl--free media. In cells which show both D and H responses superimposed, it was possible to separate these responses from each other by perfusing the cells with either Na+-free or Cl--free Ringer's solution. High [K+]0 often caused a marked hyperpolarization in either D or H cells. This is due to the primary effect of high [K+]0 on the presynaptic inhibitory fibers. The removal of this inhibitory afferent interference by applying Nembutal readily disclosed the predicted K+ depolarization. In perfusates containing normal [Na+]0, the effects of Ca++ and Mg++ on the activities of postsynaptic membrane were minimal, supporting the current theory that the effects of these ions on the synaptic transmission are mainly presynaptic. The possible mechanism of the hyperpolarization produced by simultaneous perfusion with both high [K+]0 and ACh in certain H cells is explained quantitatively under the assumption that ACh induces exclusively an increase in Cl- permeability of the H membrane.

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Selected References

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  1. ARAKI T., ITO M., OSCARSSON O. Anion permeability of the synaptic and non-synaptic motoneurone membrane. J Physiol. 1961 Dec;159:410–435. doi: 10.1113/jphysiol.1961.sp006818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BOISTEL J., FATT P. Membrane permeability change during inhibitory transmitter action in crustacean muscle. J Physiol. 1958 Nov 10;144(1):176–191. doi: 10.1113/jphysiol.1958.sp006094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BURGEN A. S., TERROUX K. G. On the negative inotropic effect in the cat's auricle. J Physiol. 1953 Jun 29;120(4):449–464. doi: 10.1113/jphysiol.1953.sp004910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BURNSTOCK G. The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pig. J Physiol. 1958 Aug 29;143(1):165–182. doi: 10.1113/jphysiol.1958.sp006051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. COOMBS J. S., ECCLES J. C., FATT P. Excitatory synaptic action in motoneurones. J Physiol. 1955 Nov 28;130(2):374–395. doi: 10.1113/jphysiol.1955.sp005413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. COOMBS J. S., ECCLES J. C., FATT P. The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol. 1955 Nov 28;130(2):326–374. doi: 10.1113/jphysiol.1955.sp005412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DEL CASTILLO J., ENGBAEK L. The nature of the neuromuscular block produced by magnesium. J Physiol. 1954 May 28;124(2):370–384. doi: 10.1113/jphysiol.1954.sp005114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. DEL CASTILLO J., KATZ B. The membrane change produced by the neuromuscular transmitter. J Physiol. 1954 Sep 28;125(3):546–565. doi: 10.1113/jphysiol.1954.sp005180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. ECCLES J., ECCLES R. M., ITO M. EFFECTS OF INTRACELLULAR POTASSIUM AND SODIUM INJECTIONS ON THE INHIBITORY POSTSYNAPTIC POTENTIAL. Proc R Soc Lond B Biol Sci. 1964 May 19;160:181–196. doi: 10.1098/rspb.1964.0035. [DOI] [PubMed] [Google Scholar]
  10. ECCLES J., ECCLES R. M., ITO M. EFFECTS PRODUCED ON INHIBITORY POSTSYNAPTIC POTENTIALS BY THE COUPLED INJECTIONS OF CATIONS AND ANIONS INTO MOTONEURONS. Proc R Soc Lond B Biol Sci. 1964 May 19;160:197–210. doi: 10.1098/rspb.1964.0036. [DOI] [PubMed] [Google Scholar]
  11. EDWARDS C., KUFFLER S. W., TRAUTWEIN W. Changes in membrane characteristics of heart muscle during inhibition. J Gen Physiol. 1956 Sep 20;40(1):135–145. doi: 10.1085/jgp.40.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. EDWARDS C., OTTOSON D. The site of impulse initiation in a nerve cell of a crustacean stretch receptor. J Physiol. 1958 Aug 29;143(1):138–148. doi: 10.1113/jphysiol.1958.sp006049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FATT P., KATZ B. An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol. 1951 Nov 28;115(3):320–370. doi: 10.1113/jphysiol.1951.sp004675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. FESSARD A., TAUC L. Capacité, résistance et variations actives d'impédance d'un soma neuronique. J Physiol (Paris) 1956 May-Jun;48(3):541–544. [PubMed] [Google Scholar]
  15. GERSCHENFELD H. M., TAUC L. DIFF'ERENTS ASPECTS DE LA PHARMACOLOGIE DES SYNAPSES DANS LE SYST'EME NERVEUX CENTRAL DES MOLLUSQUES. J Physiol (Paris) 1964 May-Jun;56:360–361. [PubMed] [Google Scholar]
  16. HAGIWARA S., KUSANO K., SAITO S. Membrane changes in crayfish stretch receptor neutron during synaptic inhibition and under action of gamma-aminobutyric acid. J Neurophysiol. 1960 Sep;23:505–515. doi: 10.1152/jn.1960.23.5.505. [DOI] [PubMed] [Google Scholar]
  17. HAGIWARA S., WATANABE A., SAITO N. Potential changes in syncytial neurons of lobster cardiac ganglion. J Neurophysiol. 1959 Sep;22:554–572. doi: 10.1152/jn.1959.22.5.554. [DOI] [PubMed] [Google Scholar]
  18. HUBBARD J. I. The effect of calcium and magnesium on the spontaneous release of transmitter from mammalian motor nerve endings. J Physiol. 1961 Dec;159:507–517. doi: 10.1113/jphysiol.1961.sp006824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. HUTTER O. F., KOSTIAL K. Effect of magnesium and calcium ions on the release of acetylcholine. J Physiol. 1954 May 28;124(2):234–241. doi: 10.1113/jphysiol.1954.sp005102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Harvey A. M., Macintosh F. C. Calcium and synaptic transmission in a sympathetic ganglion. J Physiol. 1940 Jan 15;97(3):408–416. doi: 10.1113/jphysiol.1940.sp003818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. ITO M., KOSTYUK P. G., OSHIMA T. Further study on anion permeability of inhibitory post-synaptic membrane of cat motoneurones. J Physiol. 1962 Oct;164:150–156. doi: 10.1113/jphysiol.1962.sp007009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. KERKUT G. A., THOMAS R. C. ACETYLCHOLINE AND THE SPONTANEOUS INHIBITORY POST SYNAPTIC POTENTIALS IN THE SNAIL NEURONE. Comp Biochem Physiol. 1963 Jan;8(1):39–45. doi: 10.1016/0010-406x(63)90067-7. [DOI] [PubMed] [Google Scholar]
  23. KUFFLER S. W., EDWARDS C. Mechanism of gamma aminobutyric acid (GABA) action and its relation to synaptic inhibition. J Neurophysiol. 1958 Nov;21(6):589–610. doi: 10.1152/jn.1958.21.6.589. [DOI] [PubMed] [Google Scholar]
  24. KUSANO K., HAGIWARA S. On the integrative synaptic potentials of Onchidium nerve cell. Jpn J Physiol. 1961 Feb 15;11:96–101. doi: 10.2170/jjphysiol.11.96. [DOI] [PubMed] [Google Scholar]
  25. Kerkut G. A., Meech R. W. Microelectrode determination of the intracellular chloride concentration in nerve cells. Life Sci. 1966 Mar;5(5):453–456. doi: 10.1016/0024-3205(66)90161-5. [DOI] [PubMed] [Google Scholar]
  26. LOYNING Y., OSHIMA T., YOKOTA T. SITE OF ACTION OF THIAMYLAL SODIUM ON THE MONOSYNAPTIC SPINAL REFLEX PATHWAY IN CATS. J Neurophysiol. 1964 May;27:408–428. doi: 10.1152/jn.1964.27.3.408. [DOI] [PubMed] [Google Scholar]
  27. NASTUK W. L. Some ionic factors that influence the action of acetylcholine at the muscle end-plate membrane. Ann N Y Acad Sci. 1959 Aug 28;81:317–327. doi: 10.1111/j.1749-6632.1959.tb49316.x. [DOI] [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. SOMJEN G. G., GILL M. The mechanism of the blockade of synaptic transmission in the mammalian spinal cord by diethyl ether and by thiopental. J Pharmacol Exp Ther. 1963 Apr;140:19–30. [PubMed] [Google Scholar]
  30. Sato M., Austin G. M., Yai H. Increase in permeability of the postsynaptic membrane to potassium produced by 'nembutal'. Nature. 1967 Sep 30;215(5109):1506–1508. doi: 10.1038/2151506a0. [DOI] [PubMed] [Google Scholar]
  31. TAKEUCHI A., TAKEUCHI N. Further analysis of relationship between end-plate potential and end-plate current. J Neurophysiol. 1960 Jul;23:397–402. doi: 10.1152/jn.1960.23.4.397. [DOI] [PubMed] [Google Scholar]
  32. TRAUTWEIN W., DUDEL J. Zum Mechanismus der Membranwirkung des Acetylcholin an der Herzmuskelfaser. Pflugers Arch. 1958;266(3):324–334. doi: 10.1007/BF00416781. [DOI] [PubMed] [Google Scholar]
  33. USHERWOOD P. N., GRUNDFEST H. INHIBITORY POSTSYNAPTIC POTENTIALS IN GRASSHOPPER MUSCLE. Science. 1964 Feb 21;143(3608):817–818. doi: 10.1126/science.143.3608.817. [DOI] [PubMed] [Google Scholar]

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