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. 1976 Apr;256(2):441–464. doi: 10.1113/jphysiol.1976.sp011332

Chloride distribution in Aplysia neurones

P Ascher 1, Diana Kunze 1,*, T O Neild 1,
PMCID: PMC1309315  PMID: 16992510

Abstract

1. The intracellular Cl- concentration (Cli) and the membrane potential (Em) were measured in the medial pleural neurones of Aplysia under various experimental conditions designed to determine the Cl- conductance of the neurones and investigate the possibility of an active Cl- transport.

2. The magnitude of the Cl- conductance of the cell depends on the experimental conditions.

3. In normal sea water, large changes of Em produced by passing current across the cell membrane caused no change of Cli, suggesting that the Cl- conductance was low. Similarly, moderate changes of ECl produced by decreasing Clo or increasing Cli had little or no effect on Em.

4. A high Cl- conductance was observed in high Ko or very low Clo. It was greatly reduced if the external Ca2+ was replaced by Co2+, or in the presence of tubocurarine, or if the experiment was performed on an isolated cell soma. The high Cl- conductance is therefore attributed to the release of ACh and perhaps other transmitters from synaptic terminals.

5. High concentrations of tetraethylammonium ions or procaine induced a depolarization of the cell, but a decrease of Cli. The rate of fall of Cli was increased by lowering external K+ or raising external Ca2+, and was decreased by replacing external Ca2+ by Co2+.

6. NH4+ ions applied externally had effects similar to those of K+ ions. In situations in which intracellular NH4+ might be increased a fall in Cli was observed.

7. The changes of Cli caused by TEA, procaine, or internal NH4+ occur against the driving force for passive Cl- movements. They are still observed in isolated cell bodies, and cannot be attributed to the activation of synaptic channels.

8. Some interpretations of these anomalous Cl- movements are discussed which could also account for the difference between ECl and Em observed under normal conditions.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adrian R. H., Chandler W. K., Hodgkin A. L. Voltage clamp experiments in striated muscle fibres. J Physiol. 1970 Jul;208(3):607–644. doi: 10.1113/jphysiol.1970.sp009139. [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. Barker J. L., Levitan H. Salicylate: effect on membrane permeability of molluscan neurons. Science. 1971 Jun 18;172(3989):1245–1247. doi: 10.1126/science.172.3989.1245. [DOI] [PubMed] [Google Scholar]
  4. Brown A. M., Sutton R. B., Walker J. L., Jr Increased chloride conductance as the proximate cause of hydrogen ion concentration effects in Aplysia neurons. J Gen Physiol. 1970 Nov;56(5):559–582. doi: 10.1085/jgp.56.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. GIRARDIER L., REUBEN J. P., BRANDT P. W., GRUNDFEST H. EVIDENCE FOR ANION-PERMSELECTIVE MEMBRANE IN CRAYFISH MUSCLE FIBERS AND ITS POSSIBLE ROLE IN EXCITATION-CONTRACTION COUPLING. J Gen Physiol. 1963 Sep;47:189–214. doi: 10.1085/jgp.47.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gerasimov V. D., Kostiuk P. G., Maiskii V. A. Izmeneniia élektricheskikh kharakteristik membrany gigantskogo neirona pri uvelichenii naruzhnoi kontsentratsii ionov kaliia. Biofizika. 1965;10(2):272–280. [PubMed] [Google Scholar]
  7. Gorman A. L., Marmor M. F. Contributions of the sodium pump and ionic gradients to the membrane potential of a molluscan neurone. J Physiol. 1970 Nov;210(4):897–917. doi: 10.1113/jphysiol.1970.sp009248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gorman A. L., Mirolli M. The passive electrical properties of the membrane of a molluscan neurone. J Physiol. 1972 Dec;227(1):35–49. doi: 10.1113/jphysiol.1972.sp010018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HAGIWARA S., KUSANO K., SAITO N. Membrane changes of Onchidium nerve cell in potassium-rich media. J Physiol. 1961 Mar;155:470–489. doi: 10.1113/jphysiol.1961.sp006640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. HODGKIN A. L., HOROWICZ P. The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol. 1959 Oct;148:127–160. doi: 10.1113/jphysiol.1959.sp006278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. KERKUT G. A., THOMAS R. C. THE EFFECT OF ANION INJECTION AND CHANGES IN THE EXTERNAL POTASSIUM AND CHLORIDE CONCENTRATION ON THE REVERSAL POTENTIALS OF THE IPSP AND ACETYLCHOLINE. Comp Biochem Physiol. 1964 Feb;11:199–213. doi: 10.1016/0010-406x(64)90163-x. [DOI] [PubMed] [Google Scholar]
  12. KEYNES R. D. CHLORIDE IN THE SQUID GIANT AXON. J Physiol. 1963 Dec;169:690–705. doi: 10.1113/jphysiol.1963.sp007289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kehoe J. Ionic mechanisms of a two-component cholinergic inhibition in Aplysia neurones. J Physiol. 1972 Aug;225(1):85–114. doi: 10.1113/jphysiol.1972.sp009930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kehoe J. Pharmacological characteristics and ionic bases of a 2 component postsynaptic inhibition. Nature. 1967 Sep 30;215(5109):1503–1505. doi: 10.1038/2151503b0. [DOI] [PubMed] [Google Scholar]
  15. Kehoe J. Single presynaptic neurone mediates a two component postsynaptic inhibition. Nature. 1969 Mar 1;221(5183):866–868. doi: 10.1038/221866a0. [DOI] [PubMed] [Google Scholar]
  16. Kehoe J. Three acetylcholine receptors in Aplysia neurones. J Physiol. 1972 Aug;225(1):115–146. doi: 10.1113/jphysiol.1972.sp009931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kerkut G. A., Meech R. W. The effect of ions on the membrane potential of snail neurones. Comp Biochem Physiol. 1967 Feb;20(2):411–429. doi: 10.1016/0010-406x(67)90257-5. [DOI] [PubMed] [Google Scholar]
  18. Levitan H., Tauc L. Polyphasic synaptic potentials in the ganglion of the mollusc, Navanax. J Physiol. 1975 Jun;248(1):35–44. doi: 10.1113/jphysiol.1975.sp010961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Llinas R., Baker R., Precht W. Blockage of inhibition by ammonium acetate action on chloride pump in cat trochlear motoneurons. J Neurophysiol. 1974 May;37(3):522–532. doi: 10.1152/jn.1974.37.3.522. [DOI] [PubMed] [Google Scholar]
  20. Lux H. D. Ammonium and chloride extrusion: hyperpolarizing synaptic inhibition in spinal motoneurons. Science. 1971 Aug 6;173(3996):555–557. doi: 10.1126/science.173.3996.555. [DOI] [PubMed] [Google Scholar]
  21. Lux H. D., Loracher C., Neher E. The action of ammonium on postsynaptic inhibition of cat spinal motoneurons. Exp Brain Res. 1970;11(5):431–447. doi: 10.1007/BF00233967. [DOI] [PubMed] [Google Scholar]
  22. Meyer H., Lux H. D. Action of ammonium on a chloride pump. Removal of hyperpolarizing inhibition in an isolated neuron. Pflugers Arch. 1974;350(2):185–195. doi: 10.1007/BF00586236. [DOI] [PubMed] [Google Scholar]
  23. Miledi R., Slater C. R. The action of calcium on neuronal synapses in the squid. J Physiol. 1966 May;184(2):473–498. doi: 10.1113/jphysiol.1966.sp007927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Motokizawa F., Reuben J. P., Grundfest H. Ionic permeability of the inhibitory postsynaptic membrane of lobster muscle fibers. J Gen Physiol. 1969 Oct;54(4):437–461. doi: 10.1085/jgp.54.4.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Neild T. O., Thomas R. C. Intracellular chloride activity and the effects of acetylcholine in snail neurones. J Physiol. 1974 Oct;242(2):453–470. doi: 10.1113/jphysiol.1974.sp010717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Paton W. D., Vizi E. S., Zar M. A. The mechanism of acetylcholine release from parasympathetic nerves. J Physiol. 1971 Jul;215(3):819–848. doi: 10.1113/jphysiol.1971.sp009500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Russell J. M., Brown A. M. Active transport of chloride by the giant neuron of the Aplysia abdominal ganglion. J Gen Physiol. 1972 Nov;60(5):499–518. doi: 10.1085/jgp.60.5.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sato M., Austin G., Yai H., Maruhashi J. The ionic permeability changes during acetylcholine-induced responses of Aplysia ganglion cells. J Gen Physiol. 1968 Mar;51(3):321–345. doi: 10.1085/jgp.51.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stinnakre J., Tauc L. Calcium influx in active Aplysia neurones detected by injected aequorin. Nat New Biol. 1973 Mar 28;242(117):113–115. doi: 10.1038/newbio242113b0. [DOI] [PubMed] [Google Scholar]
  30. Thomas R. C. A floating current clamp for intracellular injection of salts by interbarrel iontophoresis. J Physiol. 1975 Feb;245(2):20P–22P. [PubMed] [Google Scholar]
  31. Thomas R. C. Intracellular pH of snail neurones measured with a new pH-sensitive glass mirco-electrode. J Physiol. 1974 Apr;238(1):159–180. doi: 10.1113/jphysiol.1974.sp010516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Weakly J. N. The action of cobalt ions on neuromuscular transmission in the frog. J Physiol. 1973 Nov;234(3):597–612. doi: 10.1113/jphysiol.1973.sp010363. [DOI] [PMC free article] [PubMed] [Google Scholar]

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