Summary
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1.
The effect of polarizing currents, ions and drugs on the action potentials of individual neurones in the sub-oesophageal ganglion of the snail Helix pomatia has been examined.
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2.
The current-voltage relation showed a marked decrease of resistance for the outward current (delayed rectification). AtI=0, the average membrane resistance was 8.3 kΩ×cm2.
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3.
Tetrodotoxin in a concentration of 4.6×10−6 g/ml did not affect the overshoot or the maximum rate of rise. 0.4% cocaine inhibited delayed rectification, but did not abolish the action potential.
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4.
Ringer solution with twice the normal Na concentration augmented the overshoot by 5–6 mV and increased the maximum rate of rise to 130% of its normal value. Na-free Ringer decreased the overshoot by only 5–8 mV and reduced the maximum rate of rise to about half its normal value.
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5.
Even after prolonged perfusion with Na-free solution action potentials were still obtained. The overshoot stayed constant during a 2 hours perfusion period whereas the maximum rate of rise declined slowly. Na-free Ringer with Mn depressed the spike.
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6.
Raising the Ca concentration of the Na-free Ringer increased the overshoot (average 15.9 mV for a 10-fold increase of [Ca]0), shifted the threshold potential towards zero and slightly augmented the maximum rate of rise.
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7.
Nominally Ca-free solution markedly reduced the action potential. Excitability was maintained in Na- and Ca-free Ringer with 10 mM Sr or Ba.
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8.
Part of the results could be explained by assuming a reservoir of Na+ ions in or close to the cell membrane. An alternative explanation is that Ca++ ions participate in carrying charge across the membrane during the rising phase of the action potential. The second hypothesis appears more likely although a definite decision could not be reached.
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References
Abbot, B. C., andI. Parnas: Electrical and mechanical responses in deep abdominal extensor muscles of crayfish and lobster. J. gen. Physiol.48, 919–931 (1965).
Araki, T., andT. Otani: Response of single motoneurons to direct stimulation in toad's spinal cord. J. Neurophysiol.18, 472–485 (1955).
Arvanitaki, A., G. Romey etH. Takeuchi: Variations de la relation caractéristique V(i) de la neuromembrane en fonction de lapO2. Implications fonctionelles. C. R. Soc. Biol. (Paris)161, 1629–1633 (1967).
Bullock, T. H., andG. A. Horridge: Structure and function in the nervous systems of invertebrates, Vol. I and II. San Francisco-London: W. H. Freeman & Co. 1965.
Chamberlain, S. G., andG. A. Kerkut: Voltage clamp studies on snail (Helix aspersa) neurones. Nature (Lond.)216, 89 (1967).
Chandler, W. K., A. L. Hodgkin, andH. Meves: The effect of changing the internal solution on sodium inactivation and related phenomena in giant axons. J. Physiol. (Lond.)180, 821–836 (1965).
David, G. B.: Cytoplasmic networks in neurons. In: Comparative Neurochemistry, ed. byD. Richter. London: Pergamon Press 1964.
Fatt, P., andB. L. Ginsborg: The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. (Lond.)142, 516–543 (1958).
—, andB. Katz: The electrical properties of crustacean muscle fibres. J. Physiol. (Lond.)120, 171–204 (1953).
Frankenhaeuser, B., andA. L. Hodgkin: The action of calcium on the electrical properties of squid axons. J. Physiol. (Lond.)137, 217–244 (1957).
Gerasimov, V. D.: Effect of ion composition of medium on excitation process in giant neurons of snail. Fiziol. Sh. SSSR50, 457–463 (1964).—Fed. Proc.24, T 371–374 (1965).
—,L. Janiszewski, andE. Skubaljanka: Rectifier properties of the membrane of giant neurones in solutions of varying ion composition. Biofizika12, 97–103 (1967) (in Russian).
—,P. G. Kostyuk, andV. A. Maiskii: Excitability of giant nerve cells of various pulmonate mollusks in sodium-free solutions. Byull. éksp. Biol. Med.58, 3–6 (1964).—Fed. Proc.24, T 676–678 (1965).
———: Influence of divalent cations on electrical characteristics of giant neurone membrane. Biofizika10, 447–453 (1965) (in Russian).
Gerschenfeld, H. M., andA. Lasansky: Action of glutamic acid and other naturally occurring amino-acids on snail central neurons. Int. J. Neuropharmacol.3, 301–314 (1964).
Gola, M.: Effets de lapO2 sur la résistance électrique de la neuromembrane d'Helix pomatia. C. R. Soc. Biol. (Paris)161, 1634–1638 (1967).
Goldman, D. E.: Potential, impedance, and rectification in membranes. J. gen. Physiol.27, 37–60 (1943).
Hagiwara, S., andK.-I. Naka: The initiation of spike potential in barnacle muscle fibers under low intracellular Ca++. J. gen. Physiol.48, 141–162 (1964).
—, andS. Nakajima: Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine, and manganese ions. J. gen. Physiol.49, 793–806 (1966).
—, andK. Takahashi: Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane. J. gen. Physiol.50, 583–601 (1967).
Hille, B.: Charges and potentials at the nerve surface. Divalent ions and pH. J. gen. Physiol.51, 221–236 (1968).
Hodgkin, A. L., andB. Katz: The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. (Lond.)108, 37–77 (1949).
Junge, D.: Multi-ionic action potentials in molluscan giant neurones. Nature (Lond.)215, 546–548 (1967).
Kandel, E. R., andL. Tauc: Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission. J. Physiol. (Lond.)183, 287–304 (1966).
Kao, C. Y.: Tetrodotoxin, saxitoxin and their significance in the study of excitation phenomena. Pharmacol. Rev.18, 997–1049 (1966).
Kerkut, G. A., andD. R. Gardner: The role of calcium ions in the action potentials of Helix aspersa neurones. Comp. Biochem. Physiol.20, 147–162 (1967).
—, andR. W., Meech: The effect of ions on the membrane potential of snail neurones. Comp. Biochem. Physiol.20, 411–429 (1967).
—, andR. C. Thomas: 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.11, 199–213 (1964).
——: An electrogenic sodium pump in snail nerve cells. Comp. Biochem. Physiol.14, 167–183 (1965).
—, andR. J. Walker: The specific chemical sensitivity of Helix nerve cells. Comp. Biochem. Physiol.7, 277–288 (1962).
Koketsu, K., andS. Nishi: Calcium spikes of nerve cell membrane: Role of calcium in the production of action potentials. Nature (Lond.)217, 468–469 (1968).
Maiskii, V. A.: Electrical characteristics of surface membrane of the giant nerve cells of Helix pomatia. Fiziol. Sh. SSSR49, 1468 (1963).—Fed. Proc.23, T 1173–1176 (1964).
Meves, H.: Das Aktionspotential der Riesennervenzellen der Weinbergschnecke Helix pomatia. Pflügers Arch. ges. Physiol.289, R 10 (1966).
—: Calciumströme durch erregbare membranen. Elektrophysiologische Untersuchungen an den Riesennervenzellen der Weinbergschnecke Helix pomatia. Ber. Bunsenges. physik. Chem.71, 831–834 (1967).
Moreton, R. B.: An application of the constant-field theory to the behaviour of giant neurones of the snail, Helix aspersa. J. exp. Biol.48, 611–623 (1968a).
— Ionic mechanism of the action potentials of giant neurones of Helix aspersa. Nature (Lond.)219, 70–71 (1968b).
Nakamura, Y., S. Nakajima, andH. Grundfest: The action of tetrodotoxin on electrogenic components of squid giant axons. J. gen. Physiol.48, 985–996 (1965).
Niedergerke, R., andR. K. Orkand: The dual effect of calcium on the action potential of the frog's heart. J. Physiol. (Lond.)184, 291–311 (1966).
Oomura, Y., S. Ozaki, andT. Maéno: Electrical activity of a giant nerve cell under abnormal conditions. Nature (Lond.)191, 1265–1267 (1961).
Ozeki, M., A. R. Freeman, andH. Grundfest: The membrane components of crustacean neuromuscular systems. I. Immunity of different electrogenic components to tetrodotoxin and saxitoxin. J. gen. Physiol.49, 1319–1334 (1966).
Rall, W.: Branching dendritic trees and motoneuron membrane resistivity. Exp. Neurol.1, 491–527 (1959).
—: Membrane potential transients and membrane time constant of motoneurons. Exp. Neurol.2, 503–532 (1960).
Reuter, H.: The dependence of slow inward current in Purkinje fibres on the extracellular calcium-concentration. J. Physiol. (Lond.)192, 479–492 (1967).
Takeda, K.: Permeability changes associated with the action potential in procainetreated crayfish abdominal muscle fibers. J. gen. Physiol.50, 1049–1074 (1967).
Tauc, L.: Les divers modes d'activité du soma neuronique ganglionnaire de l'aplysie et de l'escargot. In: Microphysiologie comparée des éléments excitables. Centre National de la Recherche Scientifique. Paris 1957.
—, andH. M. Gerschenfeld: Effet inhibiteur ou excitateur du chlorure d'acétylcholine sur le neurone d'Escargot. J. Physiol. (Paris).52, 236 (1960).
—, andG. M. Hughes: Modes of initiation and propagation of spikes in the branching axons of molluscan central neurons. J. gen. Physiol.46, 533–549 (1962).
Thomas, R. C.: Measurement of current produced by the sodium pump in a snail neurone. J. Physiol. (Lond.)195, 23–24 P (1968).
Walker, R. J., andA. Hedges: The effect of cholinergic agonists on the spontaneous activity of neurones of Helix aspersa. Comp. Biochem. Physiol.24, 355 to 376 (1968).
Weed, R. I., andA. Rothstein: The uptake of divalent manganese ion by mature normal human red blood cells. J. gen. Physiol.44, 301–314 (1960).
Werman, R., andH. Grundfest: Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J. gen. Physiol.44, 997–1027 (1961).
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Meves, H. The ionic requirements for the production of action potentials in helix pomatia neurones. Pflugers Arch. 304, 215–241 (1968). https://doi.org/10.1007/BF00592126
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DOI: https://doi.org/10.1007/BF00592126