Advertisement

Neurons, Glia and Ions in Hypoxia, Hypercapnia and Acidosis

  • Alfred Lehmenkühler
  • Heinz Caspers
  • Erwin-Josef Speckmann
  • Dieter Bingmann
  • Hans G. Lipinski
  • Ulrich Kersting
Part of the Advances in Behavioral Biology book series (ABBI, volume 35)

Summary

Effects of hypoxia, hypercapnia and/or acidosis on membrane properties were investigated in cortical neurons, glial cells and spinal neurons in-vivo as well as in pyramidal cells of hippocampal slice preparations and in cultured sensory spinal ganglion (SSG) cells in-vitro.

  1. (1)

    O 2 -pressure: Studies on SSG cells revealed that the membrane potential of these neurons were highly insensitive to lowering of the bath PO2 down to 5 mmHg. CA3 neurons in hippocampal slices found in layers remote from the interface between tissue and bath fluid depolarized during hypoxia. The same reaction was observed in spinal as well as in neocortical neurons and in glial cells in-vivo. The neuronal depolarization was often preceded by a transient hyperpolarization. The hypoxia-induced decreases of membrane potentials corresponded to changes of K+ concentration in the extracellular fluid.

     
  2. (2)

    pH and CO 2 -pressure: SSG cells depolarized when pH in the bath was lowered. When PCO2 was elevated at constant bicarbonate concentrations in the bath, SSG cells depolarized as well. In bath fluid, however, containing buffer proteins like hemoglobin SSG cells were found to hyper-polarize during hypercapnia. Hyperpolarization occurred also when the bicarbonate concentration in the bath fluid was raised during hypercapnic periods. When the extracellular milieu of superficial CA3 neurons in hippocampal slices was predominantly determined by the ionic composition of the bath fluid, hypercapnia depolarized these cells. Neurons in the innermost layers of the slice and the overwhelming majority of spinal motoneurones as well as neocortical nerve cells, however, hyperpolarized in-vivo with the postsynaptic potentials simultaneously being reduced. In contrast to this neuronal response, glial cells were found to depolarize during hypercapnia. Simultaneous measurements of the extracellular ionic milieu showed a rise of extracellular K+ concentration which may in part be due to a specific increase of the neuronal K+ conductance.

     

Keywords

Membrane Potential Glial Cell Hippocampal Slice Neurochemical Pathology Tortuosity Factor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bingmann, D., Kienecker, E.W., Caspers, H., and Knoche, H., 1981, Chemoreceptor activity of sinus nerve fibres after their implantation into the wall of the external carotid artery, la: “Arterial Chemoreceptors,” C. Belmonte, D.J. Pallot, H. Acker, and S. Fidone, ed., Leicester, Leicester University Press.Google Scholar
  2. Bingmann, D., and Kolde, H., 1982, Pprofiles in hippocampal slices of the guinea pig. Exp. Brain Res. 48: 89.CrossRefGoogle Scholar
  3. Bingmann, D., Kolde, G., and Lipinski, H.G., 1984, Relations between P02 and neuronal activity in hippocampal slices, ij,: “Oxygen Transport to Tissue, Vol. V.,” D.W. Lubbers, H. Acker, E. Leniger-Follert, and T.R. Goldstick, ed., Plenum Press, New York.Google Scholar
  4. Caspers, H., Speckmann, E.-J., and Lehmenkühler, A., 1980, Electrogenesis of cortical DC potentials, Prog. Brain Res., 54: 3Google Scholar
  5. Caspers, H., Speckmann, E.-J., and Lehmenkühler, A., 1987, DC potentials of the cerebral cortex. Seizure activity and changes in gas pressures, Rev. Phvsiol. Biochem. Pharmacol., 106: 127.CrossRefGoogle Scholar
  6. Caspers, H., Speckmann, E.-J., Bingmann, D., and Lehmenkühler, A., 1986, Wirkungen von CO2 auf das Membranpotential einzelner Neurone, in: “Aktuelle Probleme der Atmungs-und Kreislaufregulation, (Funktionsanalyse biologischer Systeme, vol. 15),” J. Grote, and G. Thews, ed., Steiner, Stuttgart.Google Scholar
  7. Fujiwara, N., Higashi, H., Shimoji, K., and Yoshimura, M., 1987, Effects of hypoxia on rat hippocampal neurones in vitro, J. Phvsiol. (tond.), 384: 131.Google Scholar
  8. Hansen, A.J., Hounsgaard, J., and Jahnsen, H., 1982, Anoxia increases potassium conductance in hippocampal nerve cells. Acta ohvsiol. scand., 99, 412.CrossRefGoogle Scholar
  9. Hansen, A.J., 1985, Effect of anoxia on ion distribution in the brain. Phvsiol. Rev., 65: 101.Google Scholar
  10. Kersting, U., and Lehmenkühler, A., 1986, CO2-induced decrease of potassium permeability across the blood-brain barrier, Neurosci. Lett., 28: 5488.Google Scholar
  11. Kirino, T., Tamura, A., and Sano, K., 1985, Selective vulnerability of the hippocampus to ischemia - reversible and irreversible types of ischemic cell damage, Frog. Brain Res., 63: 39.CrossRefGoogle Scholar
  12. Kraig, R.P., Pulsinelli, W.A., and Plum, F., 1985, Heterogeneous distribution of hydrogen and bicarbonate ions during complete brain ischemia, 1985, Proa. Brain Res, 63: 155.CrossRefGoogle Scholar
  13. Krishtal, O.A., and Pidoplichko, V.I., 1981, A receptor for protons in the membrane of sensory neurons may participate in nociception, Neurosci., 6: 2599.CrossRefGoogle Scholar
  14. Lehmenkühler, A., 1976, Cortical spreading depression in relation to potassium activity, oxygen tension, local flow and carbon dioxide tension, in: “Ion and Enzyme Electrodes in Biology and Medicine,” M. Kessler, L.C. Clark Jr, D.W. Lübbers, I. A. Silver, and W. Simon, ed., Urban and Schwarzenberg, München.Google Scholar
  15. Lehmenkühler, A., 1979, Interrelationships between DC potentials, potassium activity, p02 and pCO2 in the cerebral cortex of the rat,.: “Origin of Cerebral Field Potentials,” E.-J. Speckmann, and H. Caspers, ed., Thieme, Stuttgart.Google Scholar
  16. Lehmenkühler, A., Zidek, W., Staschen, M., and Caspers, H., 1981, Cortical pH and pCa in relation to DC potential shifts during spreading depression and asphyxiation, in: “Ion-Selective Micro-electrodes and Their Use in Excitable Tissues,” E. Sykova, P. Hnik, and L. Vyklicky, ed., Plenum Press, New York.Google Scholar
  17. Lehmenkühler, A., Caspers, H., and Kersting, U., 1985, Relations between DC-potentials, extracellular ion activities and extracellular volume fraction in the cerebral cortex with changes in pCO2, in “Ion Measurements in Physiology and Medicine,” M. Kessler, D.K. Harrison, and J. Höper, ed., Springer, Berlin-Heidelberg-New York-Tokyo.Google Scholar
  18. Lipinski, H.G. and Bingmann, D., 1986, Dependent distribution of potassium in hippocampal slices of the guinea pig, Brain Res., 380: 267.CrossRefGoogle Scholar
  19. Lux, H.D., and Müller, T.H., 1987, Calzium-abhängige Schrittmacherprozesse an der neuronalen Membran mit dem Zeitbedarf paroxysmaler Vorgänge, la: “Epilepsie 86,” E.-J. Speckmann, ed., Einhorn Presse Verlag, Reinbek.Google Scholar
  20. Neher, E., and Lux, H.D., 1973, Rapid changes of potassium concentration at the outer surface of exposed single neurons during membrane current flow, J. Gen. Phvsiol., 61: 385.CrossRefGoogle Scholar
  21. Nicholson, C., and Phillips, J.M., 1981, Ion diffusion by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum, J. Phvsiol. ( Lond. ), 321: 225.Google Scholar
  22. Pulsinelli, W.A., 1985, Selective neuronal vulnerability: morphological and molecular characteristics, Proa. Brain Res., 63: 29.CrossRefGoogle Scholar
  23. Rothman, S.M., and Olney, J.W., 1987, Excitotoxicity and the NMDA receptor, Trends Neurosci., 10: 299.CrossRefGoogle Scholar
  24. Siesjö, B.K., 1985, Acid-base homeostasis in the brain: physiology, chemistry, and neurochemical pathology, Proar. Brain Res., 63: 121.CrossRefGoogle Scholar
  25. Siesjö, B.K., Ingvar, M., and Wieloch, T., 1986, Cellular and molecular events underlying epileptic brain damage, Ann. NY Acad. Sci., 462: 207.CrossRefGoogle Scholar
  26. Somjen, G.G., 1984, Interstitial ion concentration and the role of neuro-glia in seizures, la: Electrophysiology of Epilepsy, P.A. Schwartzkroin, and H. V. Wheal, ed., Academic Press, London.Google Scholar
  27. Somjen, G.G., 1979, Extracellular potassium in the mammalian central nervous system Ann. Rev. Phvsiol., 41: 159.CrossRefGoogle Scholar
  28. Speckmann, E.-J., and Caspers, H., 1974, The effect of 02- and CO2-tensions in the nervous tissue on neuronal activity and DC potentials, in: Handbook of Electroencephalography and Clinical Neurophysiology, vol.2, part C, A. Remond, ed., Elsevier, AmsterdamLondon-New York.Google Scholar
  29. Suzuki, R., Yamaguchi, T., Inaba, Y., and Wagner, H.G., 1985, Microphysiology of selectively vulnerable neurons, 1985, Proa. Brain Res., 63: 59.CrossRefGoogle Scholar
  30. Wieloch, T., 1985, Neurochemical correlate’s to selective neuronal vulnerability, 1985, Prog. Brain Res, 63: 69.CrossRefGoogle Scholar
  31. Zidek, W., Lehmenkühler, A., Caspers, H., and Lange-Asschenfeldt, H., 1978, Macromolecular buffering reverses the CO2 effect on the membrane potential in snail neurons, Pflügers Arch., 377: R43.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Alfred Lehmenkühler
    • 1
  • Heinz Caspers
    • 1
  • Erwin-Josef Speckmann
    • 1
  • Dieter Bingmann
    • 1
  • Hans G. Lipinski
    • 1
  • Ulrich Kersting
    • 1
  1. 1.Institut für Physiologie/Bereich NeurophysiologieUniversität MünsterMünsterF.R.Germany

Personalised recommendations