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Mechanisms for the Passive Regulation of Extracellular K+ in the Central Nervous System: The Implications of Invertebrate Studies

  • N. Joan Abbott
  • Y. Pichon
Part of the Advances in Experimental Medicine and Biology book series (AEMB)

Abstract

Homeostasis of the brain extracellular K concentration is a necessary prerequisite for neuronal functioning and synaptic integration3,7. There is considerable evidence for such regulation in vertebrate brain, and when the interstitial K concentration is maintained constant in the face of chronically altered K levels in blood, an active, energy-dependent mechanism is suggested7. However, it is not known to what extent the brain can maintain a degree of internal homeostasis by purely passive ‘K buffering’ systems. In this paper we shall examine the evidence for active and passive regulation of K in the brain microenvironment and discuss some results from a crustacean preparation which indicate that passive K buffering may occur. Possible involvement of glia, and alternative mechanisms, will be discussed. As astrocytes have been suggested as a major site for K buffering in the vertebrate brain, evidence for a homeostatic function of astrocytes will be considered.

Keywords

Ethacrynic Acid Extracellular Potassium Passive Mechanism Vertebrate Brain Glial Membrane 
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References

  1. 1.
    Abbott, N.J., Moreton, R.B., and Pichon, Y., Electrophysiological analysis of potassium and sodium movements in crustacean nervous system, J. exp. Biol., 63 (1975) 85–115.Google Scholar
  2. 2.
    Baylor, D.A., and Nicholls, J.G., Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. J. Physiol. (Lond.), 203 (1969a) 555–569.Google Scholar
  3. 3.
    Baylor, D.A., and Nicholls, J.G., After-effects of nerve impulses on signalling in the central nervous system of the leech. J. Physiol. (Lond.) 203 (1969b) 571–589.Google Scholar
  4. 4.
    Bourke, R.S., Nelson, K.M., Naumann, R.A., and Young, O.M., Studies of the production and subsequent reduction of swelling in primate cortex under isosmotic conditions in vivo, Exp. Brain Res., 10 (1970) 427–446.CrossRefGoogle Scholar
  5. 5.
    Bracho, H., and Orkand, R.K., Neuron-glia interaction: dependence on temperature. Brain Res., 36 (1972) 416–419.CrossRefGoogle Scholar
  6. 6.
    Bracho, H., Orkand, P.M., and Orkand, R.K., A further study of the fine structure and membrane properties of neuroglia in the optic nerve of Necturus, J. Neurobiol., 6 (1975) 395–410.CrossRefGoogle Scholar
  7. 7.
    Bradbury, M.W.B., and Stulcovä, B., Efflux mechanism contributing to the stability of the potassium concentration in cerebro-spinal fluid, J. Physiol. (Lond.) 208 (1970) 415–430.Google Scholar
  8. 8.
    Dennis, M.J. and Gerschenfeld, H.M., Some physiological properties of identified mammalian neuroglial cells, J. Physiol. (Lond.) 203 (1969) 211–222.Google Scholar
  9. 9.
    Henn, F.A., Haljamäe, H., Hamberger, A., Glial cell function: active control of extracellular K+ concentration. Brain Res., 43 (1972) 437–444.CrossRefGoogle Scholar
  10. 10.
    Hertz, L., Neuroglial localization of potassium and sodium effects on respiration in brain. J. Neurochem. 13 (1966) 1373–1387.CrossRefGoogle Scholar
  11. 11.
    Kristensson, K., Strömberg, E., Elofsson, R., and Olsson, Y., Distribution of protein tracers in the nervous system of the crayfish (Astacus astacus Linné) following systemic and local application, J. Neurocytol., 1 (1972) 35–47.CrossRefGoogle Scholar
  12. 12.
    Křiž, N., Syková, E., and Vyklický, L., Extracellular potassium changes in the spinal cord of the cat and their relation to slow potentials, active transport and impulse transmission. J.Physiol., (Lond.) 249 (1975) 167–182.Google Scholar
  13. 13.
    Kuffler, S.W., Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on the glial membrane potential, Proc. R. Soc. B, 168 (1967) 1–21.CrossRefGoogle Scholar
  14. 14.
    Kuffler, S.W., and Nicholls, J.G., The physiology of neuroglial cells. Ergebn, Physiol., 57 (1966) 1–90.Google Scholar
  15. 15.
    Kuffler, S.W., Nicholls, J.G., and Orkand, R.K., Physiological properties of glial cells in the central nervous system of Amphibia. J. Neurophysiol., 29 (1966) 768–787.Google Scholar
  16. 16.
    Lane, N.J., and Abbott, N.J., The organization of the nervous system in the crayfish Procambarus clarkii with emphasis on the blood-brain interface. Cell and Tissue Res., 156 (1975) 173–187.CrossRefGoogle Scholar
  17. 17.
    Lewis, D.V., and Schuette, W.H., NADH fluorescence and [k]0 change during hippocampal electrical stimulation, J. Neurophysiol., 38 (1975) 405–417.Google Scholar
  18. 18.
    Lux, H.D., and Neher, E., The equilibrium time course of [K+]0 in cat cortex. Exp. Brain Res., 17 (1973) 190–205.CrossRefGoogle Scholar
  19. 19.
    Miller, R.F., and Dowling, J.E., Intracellular responses of the Müller (glial) cells of Mudpuppy retina: their relation to b - wave of the electroretinogram, J. Neurophysiol., 33 (1970) 323–341.Google Scholar
  20. 20.
    Orkand, P.M., Bracho, H., and Orkand, R.K., Glial metabolism: alterations by potassium levels comparable to those during neural activity, Brain Res., 55 (1973) 467–471.CrossRefGoogle Scholar
  21. 21.
    Orkand, R.K., Nicholls, J.G., and Kuffler, S.W., Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia, J. Neurophysiol., 29 (1966) 788–806.Google Scholar
  22. 22.
    Pape, L., and Katzman, R., Response of glia in cat sensorimotor cortex to increased extracellular potassium. Brain Res., 38 (1972) 71–92.CrossRefGoogle Scholar
  23. 23.
    Ransom, B.R., and Goldring, S., Slow h3rperpolarization in cells presumed to be glia in cerebral cortex of cat, J. Neurophysiol., 36 (1973) 879–892.Google Scholar
  24. 24.
    Shousboe, A., Booher, J., Hertz, L., Content of ATP in cultivated neurons and astrocytes exposed to balanced and potassium-rich media, J. Neurochem., 17 (1970) 1502–1504.Google Scholar
  25. 25.
    Somjen, G.G., Electrogenesis of sustained potentials. In G.A. Kerkut and J.W. Phillis (Eds.), Progress in Neurobiology, Pergamon, Oxford and New York, 1973, Ch. 6, pp. 201–232.Google Scholar
  26. 26.
    Stein, W.D., The movement of molecules across the cell membrane. Academic Press, New York and London, 1967.Google Scholar
  27. 27.
    Sugaya, E., Takato, M., and Nöda, Y., Neuronal and glial activity during spreading depression in cerebral cortex of cat, J. Neurophysiol., 38 (1975) 822–841.Google Scholar
  28. 28.
    Sypert, G.W., and Ward, A.A., Unidentified neuroglia potentials during propagated seizures in neocortex, Exp. Neurol., 33 (1971) 239–255.CrossRefGoogle Scholar
  29. 29.
    Trachtenberg, MOC., and Pollen, D.A., Neuroglia: biophysical properties and physiologic function. Science, 167 (1970) 1248–1251.CrossRefGoogle Scholar
  30. 30.
    Vyskocil, F., Křiž, N., and Bureš, J., Potassium selective microelectrodes used for measuring the extracellular potassium during spreading depression and anoxic depolarization in rats, Brain Res., 39 (1972) 255–259.CrossRefGoogle Scholar
  31. 31.
    Walker, J.L., Ion specific liquid ion exchanger microelectrodes. Analyt. Chem., 43 (1971) 89A-93A.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1976

Authors and Affiliations

  • N. Joan Abbott
    • 1
  • Y. Pichon
    • 2
  1. 1.Department of PhysiologyKing’s CollegeLondonUK
  2. 2.Laboratoire de Neurobiologie CellulaireCNRSGif-Sur-YvetteFrance

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