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Activities of the sodium pump in cat pyramidal tract cells investigated with intracellular injection of sodium ions

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Sodium ions were injected into cat pyramidal tract (PT) cells electrophoretically through an intracellular NaCl or Na glutamate-filled microelectrode. Following an injection there were decreases in the maximum rates of rise and fall of the spike potential and there was displacement of the inhibitory postsynaptic potential in a depolarizing direction. These changes recovered with an exponential time course, indicating concomitant changes in the internal sodium, potassium and chloride concentrations under the operation of the sodium pump in extruding excess sodium. From the exponential recovery curve, the rate constant of active sodium extrusion was estimated as about 60 hr−1 in fast PT cells and about 90 hr−1 in slow PT cells. It was suggested that the sodium pump was at least partly electrogenic, since the resting membrane was hyperpolarized by the sodium injection to the degree which depended on the amount of sodium-injecting current. Further support for this possibility was obtained by the experiment of high-frequency activation of PT cells, in which the sodium entry through the active membrane developed a slow post-tetanic hyperpolarization.

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References

  • Adrian, R.H., Slayman, C.L.: Membrane potential and conductance during transport of sodium, potassium and rubidium in frog muscle. J. Physiol. (Lond.) 184, 970–1014 (1966).

    Google Scholar 

  • Baylor, D.A., Nicholls, J.G.: Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. J. Physiol. (Lond.) 203, 555–569 (1969a).

    Google Scholar 

  • —: After-effects of nerve impulses on signalling in the central nervous system of the leech. J. Physiol. (Lond.) 203, 571–589 (1969b).

    Google Scholar 

  • Bittar, E.E.: Effect of inhibitors and uncouplers on the Na pump of the Maia muscle fibre. J. Physiol. (Lond.) 187, 81–103 (1966).

    Google Scholar 

  • Carpenter, D.O., Alving, B.O.: A contribution of an electrogenic Na+ pump to membrane potential in Aplysia neurons. J. gen. Physiol. 52, 1–21 (1968).

    Google Scholar 

  • Chiarandini, D.J., Stefani, E.: Two different ionic mechanisms generating the spike positive afterpotential in molluscan neurones. J. gen. Physiol. 50, 1183–1200 (1967).

    Google Scholar 

  • Connelly, C.M.: Recovery process and metabolism of nerve. Rev. Mod. Phys. 31, 475–484 (1959).

    Google Scholar 

  • Coombs, J.S., Eccles, J.C., Fatt, P.: The electrical properties of the motoneurone membrane. J. Physiol. (Lond.) 130, 291–325 (1955a).

    Google Scholar 

  • —: The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J. Physiol. (Lond.) 130, 326–373 (1955b).

    Google Scholar 

  • Cross, S.B., Keynes, R.D., Rybová, R.: The coupling of sodium efflux and potassium influx in frog muscle. J. Physiol. (Lond.) 181, 865–880 (1965).

    Google Scholar 

  • Dockry, M., Kernan, R.P., Tangney, A.: Active transport of sodium and potassium in mammalian skeletal muscle and its modification by nerve and by cholinergic and adrenergic agents. J. Physiol. (Lond.) 186, 187–200 (1968).

    Google Scholar 

  • Eccles, J.C., Eccles, R.M., Ito, M.: Effects of intracellular potassium and sodium injections on the inhibitory postsynaptic potential. Proc. roy. Soc. B. 160, 181–196 (1964).

    Google Scholar 

  • Frankenhaeuser, B., Hodgkin, A.L.: The after-effects of impulses in the giant nerve fibres of Loligo. J. Physiol. (Lond.) 131, 341–376 (1956).

    Google Scholar 

  • Frumento, A.S.: Sodium pump: its electrical effects in skeletal muscle. Science 147, 1442–1443 (1965).

    Google Scholar 

  • Gage, P.W., Hubbard, J.I.: Ionic changes responsible for post-tetanic hyperpolarization. Nature (Lond.) 203, 653–654 (1964).

    Google Scholar 

  • Harris, E.J., Ochs, S.: Effects of sodium extrusion and local anaesthetics on muscle membrane resistance and potential. J. Physiol. (Lond.) 187, 5–21 (1966).

    Google Scholar 

  • Hodgkin, A.L., Keynes, R.D.: Experiments on the injection of substances into squid giant axons by means of a microsyringe. J. Physiol. (Lond.) 131, 592–616 (1956).

    Google Scholar 

  • Hubbard, J.I., Gage, P.W.: A method for the investigation of post-tetanic hyperpolarization in motor nerve terminals. XXIII. International Congress of Physiological Sciences, Tokyo. Abstracts of Papers, p. 384 (1965).

  • Ito, M., Oshima, T.: Temporal summation of after-hyperpolarization following a motoneurone spike. Nature (Lond.) 195, 910–911 (1962).

    Google Scholar 

  • —: The electrogenic action of cations on cat spinal motoneurons. Proc. roy. Soc. B. 161, 92–108 (1964a).

    Google Scholar 

  • —: The extrusion of sodium from cat spinal motoneurons. Proc. roy. Soc. B. 161, 109–131 (1964b).

    Google Scholar 

  • — Further study on the active transport of sodium across the motoneuronal membrane. Proc. roy. Soc. B. 161, 132–141 (1964c).

    Google Scholar 

  • Keesey, J.C., Wallgren, H., McIlwain, H.: The sodium, potassium and chloride of cerebral tissues: Maintenance, change on stimulation and subsequent recovery. Biochem. J. 95, 289–300 (1965).

    Google Scholar 

  • Kerkut, G.A., Thomas, R.C.: An eleotrogenic sodium pump in snail nerve cells. Comp. Biochem. Physiol. 14, 167–183 (1965).

    Google Scholar 

  • Kernan, R.P.: Membrane potential changes during sodium transport in frog sartorius muscle. Nature (Lond.) 193, 986–987 (1962).

    Google Scholar 

  • Keynes, R.D., Rybová, R.: The coupling between sodium and potassium fluxes in frog sartorius muscle. J. Physiol. (Lond.) 168, 58P (1963).

    Google Scholar 

  • Koike, H., Brown, H.M., Hagiwara, S.: Hyperpolarization of a barnacle photoreceptor membrane following illumination. J. gen. Physiol. 57, 723–737 (1971).

    Google Scholar 

  • —, Mano, N., Okada, Y., Oshima, T.: Repetitive impulses generated in fast and slow pyramidal tract cells by intracellularly applied current steps. Exp. Brain Res. 11, 263–281 (1970).

    Google Scholar 

  • - - - - Sodium pump in cat pyramidal tract cells. Proc. Int. Union Physiol. Sci. 9, 314 (XXV. International Congress, Munich, 1971).

  • —, Okada, Y., Oshima, T.: Accomodative properties of fast and slow pyramidal tract cells and their modification by different levels of their membrane potential. Exp. Brain Res. 5, 189–202 (1968b).

    Google Scholar 

  • —, Takahashi, K.: Accommodative behaviour of cat pyramidal tract cells investigated with intracellular injection of currents. Exp. Brain Res. 5, 173–188 (1968a).

    Google Scholar 

  • Kuno, M., Miyahara, J.T., Weakly, J.N.: Post-tetanic hyperpolarization produced by an electrogenic pump in dorsal spinocerebellar tract neurones of the cat. J. Physiol. (Lond.) 210, 839–855 (1970).

    Google Scholar 

  • Mullins, L.J., Awad, M.Z.: The control of the membrane potential of muscle fibers by the sodium pump. J. gen. Physiol. 48, 761–775 (1965).

    Google Scholar 

  • Nakajima, S., Takahashi, K.: Post-tetanic hyperpolarization and electrogenic Na pump in stretch receptor neurone of crayfish. J. Physiol. (Lond.) 187, 105–127 (1966).

    Google Scholar 

  • Nishi, S., Koketsu, K.: Analysis of slow inhibitory postsynaptio potential of bullfrog sympathetic ganglion, J. Neurophysiol. 31, 717–728 (1968).

    Google Scholar 

  • —, Soeda, H.: Hyperpolarization of neurone membrane by barium. Nature (Lond.) 204, 761–764 (1964).

    Google Scholar 

  • Orkand, R.K., Nicholls, J.G., Kuffler, S.W.: Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29, 788–806 (1966).

    Google Scholar 

  • Oshima, T.: The sodium pump of mammalian nerve cells. In: “Studies in Physiology”, pp. 226–232. Ed. by D.R. Curtis, A.K. McIntyre. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • —: Studies of pyramidal tract cells, In: “Basic Mechanisms of the Epilepsies”, pp. 253–261. Ed. by H.H. Jasper, A.A. Ward, Jr., A. Pope. Boston: Little, Brown and Co. 1969.

    Google Scholar 

  • Page, E., Storm, S.R.: Cat heart muscle in vitro. VIII. Active transport of sodium in papillary muscles. J. gen. Physiol. 48, 957–972 (1965).

    Google Scholar 

  • Phillips, C.G.: Intracellular records from Betz cells in the cat. Quart. J. exp. Physiol. 41, 58–69 (1956).

    Google Scholar 

  • —: Actions of antidromic pyramidal volleys on single Betz cells in the cat. Quart. J. exp. Physiol. 44, 1–25 (1959).

    Google Scholar 

  • Rang, H.P., Ritchie, J.M.: On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J. Physiol. (Lond.) 196, 183–221 (1968).

    Google Scholar 

  • Ritchie, J.M., Straub, R.W.: The hyperpolarization which follows activity in mammalian non-medullated fibres. J. Physiol. (Lond.) 136, 80–97 (1957).

    Google Scholar 

  • Senft, J.P.: Effects of some inhibitors on the temperature-dependent component of resting potential in lobster axon. J. gen. Physiol. 50, 1835–1848 (1967).

    Google Scholar 

  • Sholl, D.A.: Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. (Lond.) 87, 387–406 (1953).

    Google Scholar 

  • Sokolove, P.G., Cooke, I.M.: Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J. gen. Physiol. 57, 125–163 (1971).

    Google Scholar 

  • Stefanis, C., Jasper, H.: Intracellular microelectrode studies of antidromic responses in cortical pyramidal tract neurons. J. Neurophysiol. 27, 828–854 (1964a).

    Google Scholar 

  • —: Recurrent collateral inhibition in pyramidal tract neurons. J. Neurophysiol. 27, 855–877 (1964b).

    Google Scholar 

  • Straub, R.W.: On the mechanism of post-tetanic hyperpolarization in myelinated nerve fibres from the frog. J. Physiol. (Lond.) 159, 19–20P (1961).

    Google Scholar 

  • Takahashi, K.: Slow and fast groups of pyramidal tract cells and their respective membrane properties. J. Neurophysiol. 28, 908–924 (1965).

    Google Scholar 

  • —, Kubota, K., Uno, M.: Recurrent facilitation in cat pyramidal tract cells. J. Neurophysiol. 30, 22–34 (1967).

    Google Scholar 

  • Thomas, R.C.: Membrane current and intracellular sodium changes in a snail neurone during extrusion of injected sodium. J. Physiol. (Lond.) 201, 495–514 (1969).

    Google Scholar 

  • Van Harreveld, A., Ochs, S.: Cerebral impedance changes after circulatory arrest. Amer. J. Physiol. 187, 180–192 (1956).

    Google Scholar 

  • —, Schade, P.: Chloride movements in cerebral cortex after circulatory arrest and during spreading depression. J. cell. comp. Physiol. 54, 65–77 (1959).

    Google Scholar 

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Koike, H., Mano, N., Okada, Y. et al. Activities of the sodium pump in cat pyramidal tract cells investigated with intracellular injection of sodium ions. Exp Brain Res 14, 449–462 (1972). https://doi.org/10.1007/BF00236587

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