Hyperexcitability of Neurons and Astrocytes in Epileptic Human Cortex

  • Ann H. Cornell-Bell
  • Anne Williamson
Part of the Altschul Symposia Series book series (ALSS, volume 2)

Abstract

Glutamate elicits an excitatory physiological response from most neurons and glia throughout the vertebrate CNS (Shank and Aprison, 1988). With the development of selective agonists and antagonists, five classes of excitatory amino acid receptors (EAA) have been defined. Three of these receptors have been described by their depolarizing actions (NMDA, Kainate [KA], Quisqualate [QUIS/AMPA]). AMPA has recently been shown to be a more selective agonist for the receptor-ion channel complex (Monaghan et al, 1989). A fourth, the AP4 receptor, appears to represent an inhibitory autoreceptor (Watkins et al, 1990). The fifth receptor (metabotropic), which is activated by trans-ACPD and modifies inositol phosphate metabolism (Palmer et al, 1989), appears to have a role in intracellular calcium regulation (Miller et al., 1992). The distribution of these multiple subtypes of glutamate receptors varies among cell types. The array of glutamate receptors that are found on neurons includes the NMDA receptor which is apparently lacking from the glial composite.

Keywords

NMDA Receptor Glutamate Receptor Excitatory Amino Acid Epileptic Focus Excitatory Amino Acid Receptor 
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.

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References

  1. Ahmed, Z., Lewis, C.A. and Farber, D.S., 1990, Glutamate stimulates release of Cat+ from internal stores in astroglia. Brain Res. 516: 165.PubMedCrossRefGoogle Scholar
  2. Aram, J. A., Lodge, D., 1987, Epileptifonn activity induced by alkalosis in rat neocortical slices: block by antagonist of N-methyl-D-aspartate. Neuroscience Letters, 83, 345–350.PubMedCrossRefGoogle Scholar
  3. Astion, M.L., Chvatal, A. and Orkand, R.K., 1989, Na+/H+ exchanges in glial cells of Necturus optic nerve. Neurosci. Lett. 107: 167.PubMedCrossRefGoogle Scholar
  4. Awad, I. A., Rosenfeld, J., Ahl, J., Hahn, J.F. and Luders, H., 1991, Intractable epilepsy and structural lesions of the brain: mapping, resection strategies, and seizure outcome. Epilepsia, 32: 179.PubMedCrossRefGoogle Scholar
  5. Backus, K.H., Kettenmann, H., Orkand, R.K., 1989, Pharmacologic characterization of the glutamate receptor in cultured astrocytes. J. Neurosci. Res. 22: 274.PubMedCrossRefGoogle Scholar
  6. Ballanyi, K. and Grafe, P., 1988, Cell volume regulation in the nervous system. Renal Physiol B iochem. 3: 142.Google Scholar
  7. Ballanyi, K. and Schlue W.-R., 1990, Intracellular chloride activity in glial cells of the leach central nervous system. J. Physiol. (Lond.) 420: 325.Google Scholar
  8. Bates, R. G., 1973, Determination of pH: Theory and Practice. New York: Wiley.Google Scholar
  9. Bevan, S., 1990, Ion channels and neurotransmitter receptors in glia. Seminars in Neurosci. 2: 467.Google Scholar
  10. Boon, P. A., Williamson, P.D., Fried, I., Spencer, D.D. Novelly, R.A., Spencer, S.S. and Mattson, R.H., 1991, Intracranial, intraaxial, space-occupying lesions in patients with intractable partial seizures: an anatomical, neuropsychological, and surgical correlation. Epilepsia, 32: 467.Google Scholar
  11. Chessler, M.L. and Kraig, R.P., 1989, Intracellular pH transients of mammalian astrocytes. J. Neurosci. 8: 2011.Google Scholar
  12. Choi, D.W., 1987, Ionic dependence of glutamate neurotoxcity. J. Neurosci. 7: 369.PubMedGoogle Scholar
  13. Choi, D.W. and Rothman, S.M., 1990, The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev. Neurosci. 13: 171.PubMedCrossRefGoogle Scholar
  14. Church, J. and. McLellan., H., 1989, Electrophysiological properties of rat CAl pyramidal neurons in vitro modified by changes in extracellular bicarbonate. J. Physiol. 415, 85–108.Google Scholar
  15. Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S. and Smith, S. J., 1990, Glutamate induces calcium waves in astrocytes: Long-range signalling. Science 247: 470.PubMedCrossRefGoogle Scholar
  16. Cornell-Bell, A.H. and Finkbeiner, S.M., 1991, Ca2+ waves in astrocytes. Cell Calcium 12: 185.PubMedCrossRefGoogle Scholar
  17. Cornell-Bell, A.H., Magge, S. and During, M., 1992, Human cortical astrocytes from hyperexcitable epileptic foci are themselves hyperexcitable. In: Excitatory Amino Acids. Simon, R. P (ed.) Thieme Medical, N.Y. 273.Google Scholar
  18. Cornell-Bell, A.H. Thomas, P.G. and Caffrey, 1992, Ca2+ and filopodial responses to glutamate in cultured astrocytes and neurons. Can. J., Physiol and Pharmacol. (In Press).Google Scholar
  19. Croucher, M.J., Collins, J.F., Meldrum, B.S., 1982, Anticonvulsant action of excitatory amino acid antagonists. Science 216: 899.PubMedCrossRefGoogle Scholar
  20. Cserr, H.F. and Bundgaard, M., 1986, The neuronal microenvironment. A comparative view. Ann. N.Y. Acad. Sci. 481: 1.PubMedCrossRefGoogle Scholar
  21. Dani, J. W., Chemayski, A. and Smith, S.J, 1992, Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8: 429.PubMedCrossRefGoogle Scholar
  22. Diemer, N.H., and Siemkowicz, E., 1981, Regional neurone damage after cerebral ischemia in thenormal and hypoglycemic rat. Neuropathol. Appl. Neurobiol. 17: 217.CrossRefGoogle Scholar
  23. Dipolo, R. and Marty, A., 1989, Measurement of Na.-K, pump in acinar cells of rat lacrimal glands. Biophys J. 55: 571.PubMedCrossRefGoogle Scholar
  24. Deitmer, J.W. and Schlue W. R., 1989, An inwardly directed electrogenic sodium-bicarbonate co-transport in leech glial cell. J. Physiol. (Lund.) 411: 179.Google Scholar
  25. Doze, V.A., Cohen, G.A., and Madison, D.V., 1991, Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron. 6 (6): 889–990.PubMedCrossRefGoogle Scholar
  26. During, M. and Spencer, D.D., 1990, Neurotransmitter release in the human hippocampus in vivo: physiological and pharmacological studies of complex partial epilepsy. Epilepsia 31: 623.Google Scholar
  27. Fisher, R.S., 1991, Glutamate and epilepsy. In: Neurotransmitters and Epilepsy, Wiley Liss, New York: 131.Google Scholar
  28. Fried, I., Kim, J.H. and Spencer, D.D., 1992, Hippocampal pathology in patients with intractable seizures and temporal lobe masses. J. Neurosurg. 76: 735.PubMedCrossRefGoogle Scholar
  29. Garthwaite, J. and Wilkin, G.P., 1982, Kainic acid receptors and neurotoxicity in adult and immature rat cerebellar slices. Neuroscience 7: 2499–2514.PubMedCrossRefGoogle Scholar
  30. Glaum, S.R., Holzwarth, J.A. and Miller, R.J., 1990, Glutamate receptors activate Ca2+ mobilization and Ca2+ influx into astrocytes. Proc. Natl. Acad. Sci. 87: 3454.PubMedCrossRefGoogle Scholar
  31. Griffiths, T., Evans, M.C., and Meldrum, B.S., 1983, Intracellular calcium accumulation in rat hippocampus during seizures induced by bicculine or L-allylglycine. Neurosci. 10: 385.CrossRefGoogle Scholar
  32. Hamprecht, B., 1986, Astroglia cells in culture. In Receptors and cyclic nucleotides in Astrocytes,Vol II. New York, Academic Press, 77.Google Scholar
  33. Hertz, L., 1965, Possible role of neuroglia: A potassium mediated neuronal-neuroglial-neuronal impulse transmission system. Nature 206: 1091.PubMedCrossRefGoogle Scholar
  34. Huang, H.Y., Herttig, G., Allgaier, C. and Jackisch, R., 1991, 3, 4-Diaminopyridine-evoked noradrenaline release in rat hippocampus: role of Na’ entry on Ca2+ pools and of protein kinase C. Eur. J. Pharmacol. 206: 221.Google Scholar
  35. Jendelova, P. and Sykova, E., 1991, Role of glia in K+ and pH homeostasis in the neonatal rat spinal cord. Glia 4: 56.PubMedCrossRefGoogle Scholar
  36. Jensen, A.M. and Chiu, S.Y., 1990, Fluorescence measurement of changes in intracellular calcium induced by excitatory amino acids in cultured astrocytes. J. Neurosci. 11: 1674.Google Scholar
  37. Kawasaki, K., Traynelis, S.F., and Dingledine, R., 1990, Different responses of the CAI and CA3 regions to hypoxia in rat hippocampal slice. J. Neurophysiol. 63 (3): 385–94.PubMedGoogle Scholar
  38. Kettenmann H. and Schlue, W-R., 1988, Intracellular pH regulation in cultured mouse oligodendrocytes. J. Physiol. (Lond.) 406: 147.Google Scholar
  39. Knight, D.E., Sugden, D. and Baker, P.F., 1988, Evidence implicating protein kinase C in exocytosis from electropermeabilized bovine chromaffin cells. J. Membr. Biol. 104: 21.PubMedCrossRefGoogle Scholar
  40. Lehman, A., 1987, Alterations in hippocampal extracellular amino acids and purine catabolites during limbic seizure induced by folate injections into the rabbit amygdala. Neuroscience 22: 573.CrossRefGoogle Scholar
  41. Levan, E.R., Franck, H. J., Gelfand, R., Luophlin, S. E. and Kaplan, G., 1990, Naturetic peptide receptors in cultured rat diencephalon. J. Biol. Chem. 265; 10019.Google Scholar
  42. Lieberman, E.M. and Hassan, S., 1988, Studies of axon-glial cell interactions and periaxonal K+ homeostasis III. The effect of anisosmotic media and potassium on the relationship between the resistance in series with the axon membrane and glial cell volume. Neurosci. 25: 971.CrossRefGoogle Scholar
  43. Meldrum, B. S., 1981, In: Metabolic Disorders of the Nervous System, Rose, F.C. ( Ed) Pitman-Medical, London: 175.Google Scholar
  44. Meldrum, B.S. Smith, S.E., Le Peillet, E., Moncada, C. and Arvin, B., 1992, Antagonists acting at non-NMDA receptors as cerebroprotective agents in global and focal ischemia. In: Excitatory Amino Acids. Simon, R. P (ed.) Thieme Medical, N.Y.: 235.Google Scholar
  45. Meyer, T., 1991, Cell signalling by second messenger waves. Cell 64: 675.PubMedCrossRefGoogle Scholar
  46. Meyer, T. and Stryer, L., 1991, Calcium spiking. Annu. Rev. Biophy. Biophys. Chem. 20: 153–174.CrossRefGoogle Scholar
  47. Miller, S., Cotman, C.W. and Bridges, R.J., 1992, 1-Aminocyclopentane-trans-1,3-dicarboxylic acid induces glutamine synthetase activity in cultured astrocytes. J. Neurochem. 58: 1967.Google Scholar
  48. Monaghan, D.T., Bridges, R.J., Cotman, C.W., 1989, The excitatory amino acid receptors: Their classes, pharmacology and distinct properties in the function of the nervous system. Annu. Rev. Pharmacol. Toxicol. 29: 365.PubMedCrossRefGoogle Scholar
  49. Newman, E.A., 1986, High potassium conductance in astrocytic endfeet. Science 233: 453.PubMedCrossRefGoogle Scholar
  50. Nicholls, D. and Atwell, D., 1990, The release and uptake of excitatory amino acids. Trends. Pharmacol. Sci. 11: 462.PubMedCrossRefGoogle Scholar
  51. Nicholson, C., 1980, Dynamics of the brain cell microenvironment. Neurosci. Res. Prog. Bull. 18: 177.Google Scholar
  52. Nicholson, C. and Phillips, J.M., 1981, Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. J. Physiol. (Lond) 29: 788.Google Scholar
  53. Palmer, E. Monoghan, D.T., Cotman, C.W., 1989, Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor. Eur. J. Pharmacol. 166: 585.Google Scholar
  54. Patel, A., Hunt, A., 1989, Regulation of production by primary cultures of rat forebrain astrocytes of a trophic factor important for the development of cholinergic neurons. Neurosci. Letts., 99: 223.CrossRefGoogle Scholar
  55. Pearse, B.R., Morrow, C. and Murphy, S., 1986, Receptor-mediated inoisitol phospholipid hydrolysis in astrocytes. Eur. J. Pharmacol., 121: 231.CrossRefGoogle Scholar
  56. Philibert, R.A. Rogers, K.L., Allen, A. J. and Dutton, G.R., 1988, Dose-dependent K+-stimulated efflux of endogenous taurine from primary astrocyte culutres is Ca2+-dependent. J. Neurochem. 51: 122.PubMedCrossRefGoogle Scholar
  57. Pontremoli, S., Melloni, E., Salamino, F., Patron, Michetti, M and Horecker, B.L., 1989, Activation of neutrophil calpain following its translocation to the plasma membrane induced by phorbol ester or fMet-Leu-Phe. Biochem. Biophys. Res. Comm. 160: 737.PubMedCrossRefGoogle Scholar
  58. Prince, D.A., Pedley, T.A., Ransom, B.R., 1978, Fluctuations in ion concentrations during excitation and seizures. In: Schoffenals, E., Franck, G., Hertz, L. and Towers, D.B. (Eds) Dynamic Properties of Glial Cells. Pergamon Press, 281.Google Scholar
  59. Rasmussen, C. D. and Means, A.R., 1989, Calmodulin is required for cell-cycle progression during G1 and mitosis. EMBO J. 8: 73.PubMedGoogle Scholar
  60. Robinson, M.B., Blakely, R.D., Couto, R. and Coyle, J.T., 1987, Hydrolysis of the brain dipeptide N-acetyl-L-aspartyl-L-glutamate: identification and characterization of a novel N-acetylatedalpha-linked-acidic dipeptidase activity from rat brain, J. Biol. Chem., 262: 14498.PubMedGoogle Scholar
  61. Shaun, W., Connor, J.A., Madelian, V., Martin, D.L., 1989, Spontaneous and beta-adrenergic receptor-mediated taurine release from astroglial cells are independent of manipulations of intracellular calcium. J. Neurosci. 9: 2306.Google Scholar
  62. Shank, R. P. and Aprison, M.H., 1988, Glutamate as a neurotransmitter. In: Kvamme, E. (Ed.) Glutamine and Glutamate in Mammals, CRC Press, Boca Raton: 3.Google Scholar
  63. Schwarz, R. Zaczek, R., Coyle, J.T., 1978, Microinjection of kainic acid into the rat hippocampus. Eur. J. Pharmacol. 50: 209.Google Scholar
  64. Somjen, G. G., 1984, Acidification of interstitial fluid in hippocampal formation caused by seizures and by spreading depression. Brain Research, 311: 186.PubMedCrossRefGoogle Scholar
  65. Sontheimer, H., Kettenmann, H. Backus, H.K. and Schachner, M., 1988, Glutamate opens Na+/K+ channels in cultured astrocytes. Glia 1: 328.PubMedCrossRefGoogle Scholar
  66. Sykova, E. and Svoboda, J., 1990, Extracellular alkaline-acid-alkaline transients in the rat spinal cord evoked by peripheral stimulation. Brain Res. 512: 181.PubMedCrossRefGoogle Scholar
  67. Usowicz, M.M., Gallo, V., Cull-Candy, S.G., 1989, Multiple conductance channels in Type 2 cerebellar astrocytes activated by excitatory amino acids. Nature 339: 380.PubMedCrossRefGoogle Scholar
  68. Waltz, W., 1989, Role of glial cells in the regulation of the brain ion microenvironemnt. Prog. Neurobiol. 33: 309.CrossRefGoogle Scholar
  69. Watkins, J. C., Krogsgaard-Larsen, P. and Honore, T., 1990, Structure-activity relationships in the development of excitatory amino acid receptor agonists and competivitie antagonists. Trends Pharmacol. Sci. 11: 25.PubMedCrossRefGoogle Scholar
  70. Young, A. B., Dure, L.S. and J.B. Penney, 1992, Excitatory amino acids in Huntington’s disease. In: Excitatory Amino Acids. Simon, R. P (ed.) Thieme Medical, N.Y.: 217.Google Scholar
  71. Zaczek, R. and Coyle, J.T., 1982, Excitatory amino acid analogues: neurotoxicity and seizures. Neuropharmacol. 21: 15.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Ann H. Cornell-Bell
    • 1
  • Anne Williamson
    • 2
  1. 1.Department of Cell BiologyYale University School of MedicineNew HavenUSA
  2. 2.Section of NeurosurgeryYale University School of MedicineNew HavenUSA

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