Comparison of changes evoked by GABA (γ-aminobutyric acid) and anoxia in [K+](o), [Cl-](o), and [Na+](o) in stratum pyramidale and stratum radiatum of the guinea pig hippocampus

Canadian Journal of Physiology and Pharmacology

Volumn 78, Issue 5, 2000, Pages 378-391

  Obrocea, G V ^a   Morris, M E ^b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Bicuculline methiodide; Brain slices; Extracellular space shrinkage; Ion selective microelectrodes; Stratum pyramidale; Stratum radiatum

Indexed keywords

4 AMINOBUTYRIC ACID; CHLORIDE; POTASSIUM; SODIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; COMPARATIVE STUDY; GUINEA PIG; HIPPOCAMPUS; ION EXCHANGE; ION TRANSPORT; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TISSUE LEVEL;

EID: 0034122173     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/y00-001     Document Type: Article

References (105)

1. Alger, B.E., and Nicoll, R.A. 1982. Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro. J. Physiol. (London), 328: 125-141.
2. A receptors in mouse cortical neurons. Pflugers Arch. 435: 382-387.
3. Ammann, D. 1986. Ion-selective microelectrodes. Springer-Verlag, New York, N.Y. p. 346.
4. Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, I.A., and Mosfeldt Laursen, A. 1980. Two different responses of hippocampal pyramidal cells to application of gamma-aminobutyric acid. J. Physiol. (London), 305: 279-296.
5. Andiné, P., Owen, O., Jacobson, I., Sandberg, M., and Hagberg, H. 1991. Changes in extracellular amino acids and spontaneous neuronal activity during ischemia and extended reflow in the CA1 of the rat hippocampus. J. Neurochem. 57: 222-229.
6. 2+ in adult rat hippocampal slices. J. Neurophysiol. 81: 811-816.
7. A receptors causes a depolarizing potential under physiological conditions in rat hippocampal pyramidal cells. Eur. J. Neurosci. 4: 16-26.
8. Ballanyi, K., and Grafe, P. 1985. An intracellular analysis of gamma-aminobutyric-acid associated ion movements in rat sympathetic neurones. J. Physiol. (London), 365: 41-58.
9. + evoked by GABA, THIP and baclofen in the guinea-pig hippocampal slice. Exp. Brain Res. 84: 591-598.
10. Barolet, A.W., Andrews, R., and Morris, M.E. 1989. Calibration of ion-selective microelectrodes. J. Neurosci. Meth. 30: 263-266.
11. Benveniste, H., Drejer, J., Schousboe, A., and Diemer, N.H. 1984. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43: 1369-1374.
12. Böhrle, C.P., and Sonnhof, U. 1985. The ionic mechanism of postsynaptic inhibition in motoneurones of the frog spinal cord. Neuroscience, 14: 581-592.
13. Bonnet, U., Gastpar, M., and Bingmann, D. 1996. Ethacrynic acid: effects on postsynaptic GABA responses and electric activity of CA3 neurones. Neuroreport, 7: 2983-2987.
14. Bormann, J., and Kettenman, H. 1988. Patch-clamp study of gamma-aminobutyric acid receptor channels in cultured astrocytes. Proc. Natl. Acad. Sci. U.S.A. 85: 9336-9340.
15. B receptor site distribution in the rat central nervous system. Neuroscience, 20: 365-383.
16. A receptor responses by NMDA application in hippocampal neurones acutely isolated from the adult guinea-pig. J. Physiol. (London), 482: 353-362.
17. A-receptor function is regulated by phosphorylation in acutely dissociated guinea-pig hippocampal neurons. J. Physiol. (London), 420: 207-221.
18. 2+ of rat cerebellar granule cells in explant cultures. J. Neurosci. 7: 1384-1400.
19. Dietzel, I., Heinemann, U., Hofmeier, G., and Lux, H.D. 1980. Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp. Brain Res. 40: 432-439.
20. - concentration in relation to changes in the size of the extracellular space. Exp. Brain Res. 46: 73-84.
21. Djorup, A., Jahnsen, H., and Mosfeldt Laursen, A. 1981. The dendritic response to GABA in CA1 of the hippocampal slice. Brain Res. 219: 196-201.
22. Eisenman, G. 1967. Glass electrodes for hydrogen and other cations: principles and practice. Marcel Dekker, New York, N.Y. p. 367.
23. Erdo, S.L., Michler, A., and Wolff, J.R. 1991. GABA accelerates excitotoxic cell death in cortical cultures: protection by blockers of GABA-gared chloride channels. Brain Res. 542: 254-258.
24. Erecinska, M., and Silver, I.A. 1994. Ions and energy in mammalian brain. Prog. In Neurobiol. 43: 37-71.
25. Friedman, J.E., and Haddad, G.G. 1994. Anoxia induces an increase in intracellular sodium in rat central neurons in vitro. Brain Res. 663: 329-334.
26. Fujiwara, N., Higashi, H., Shimoji, K., and Yoshimura, M. 1987. Effects of hypoxia on rat hippocampal neurones in vitro. J. Physiol. (London), 384: 131-151.
27. Globus, M.Y.-T., Buston R., Martinez, E., Valdés, I., and Dietrich, W.D. 1990. Ischemia induces release of glutamate in regions spared from histopathologic damage in the rat. Stroke, 21: III-43-46.
28. Graham, S.H., Shiroishi, K., Panter, S.S., Simon, R.P., and Faden, A.I. 1990. Changes in extracellular amino acid neurotransmitters produced by focal cerebral ischemia. Neurosci. Letts. 110: 124-130.
29. Grossman, R.G., and Williams, V.F. 1971. Electrical activity and ultrastructure of cortical neurons and synapses in ischemia. In Brain hypoxia. Edited by J.B. Brierley and B.S. Meldrum. Lippincott, Philadelphia, Pa. pp. 61-75.
30. Guatteo, E., Mercuri, N.B., Bernardi, G., and Knopfel, T. 1998. Intracellular sodium and calcium homeostasis during hypoxia in dopamine neurons of rat substantia nigra pars compacta. J. Neurophysiol. 80: 2237-2243.
31. Guilbault, G.G., Durst, R.A., Frant, M.S., Freiser, H., Hansen, E.H., Light, T.S., Pungor, E., Rechnitz, G., Rice, N.M., Rohm, T.J., Simon, W., and Thomas, J.D.R. 1976. Recommendations for nomenclature of ion-selective electrodes. Pure Appl. Chem. 48: 127-145.
32. Gutnick, M.J., and Segal, M. 1981. Serotonin and GABA-induced fluctuations in extracellular ion concentration in the hippocampal slice. In Ion-selective microelectrodes and their use in excitable tissues. Edited by E. Syková, P. Hnik, and L. Vyklicky. Plenum Press, New York, N.Y. pp. 261-266.
33. Haddad, G.G. 1998. Mechanisms of anoxia tolerance. A novel approach using a Drosophila model system. Adv. Expl. Med. Biol. 454: 273-280.
34. Haddad, G.G., and Jiang, C. 1993. Mechanisms of anoxia-induced depolarization in brainstem neurons: in vitro current and voltage clamp studies in the adult rat. Brain Res. 625: 261-268.
35. Hagberg, H., Lehmann, A., Sandberg, N., Nystrom, B., Jacobson, I., and Hamberger, A. 1985. Ischemia-induced shift of inhibitory and excitatory amino acids from intra- to extracellular compartments. J. Cereb. Blood Flow Metab. 5: 413-419.
36. Hansen, A.J. 1985. Effect of anoxia on ion distribution in the brain. Physiol. Rev. 65: 101-148.
37. Hansen, A.J., and Zeuthen, T. 1981. Extracellular ion concentration during spreading depression and ischemia in rat brain cortex. Acta Physiol. Scand. 113: 437-445.
38. Hansen, A.J., Hounsgaard, J., and Jahnsen, H. 1982. Anoxia increases potassium conductance in hippocampal nerve cells. Acta Physiol. Scand. 115: 301-310.
39. - in rat hippocampal neurons. Neurosci. Lett. 143: 135-138.
40. A response under experimental ischaemia in acutely dissociated CA1 pyramidal neurones of the rat. J. Physiol. (London), 500: 673-688.
41. Heinemann, U., Lux, H.D., and Gutnick, M.J. 1977. Extracellular free calcium and potassium during paroxysmal activity in the cerebral cortex of the cat. Exp. Brain Res. 27: 237-243.
42. Hershkowitz, N., Katchman, A.N., and Veregge, S. 1993. Site of synaptic depression during anoxia: a patch-clamp analysis. J. Neurophysiol. 69: 431-441.
43. - efflux from cultured mouse oligodendrocytes. Neurosci. Letts. 97: 334-339.
44. Inagaki, C., Hara, M., and Inoue, M. 1992. Neuronal intracellular chloride ion concentrations and their regulatory mechanisms. Nippon Yakurigaku Zasshi, 99: 307-315.
45. - pump in rat brain neurons. J. Exp. Zool. 275: 262-268.
46. Inglefield, J.R., and Schwartz-Bloom, R.D. 1998a. Optical imaging of hippocampal neurons with a chloride-sensitive dye: early effects of in vitro ischemia. J. Neurochem. 70: 2500-2509.
47. - and cell volume. J. Neurochem. 71: 1396-1404.
48. +-conductance in the action of γ-aminobutyric acid in the guinea-pig hippocampus. Br. J. Pharmacol. 86: 515-524.
49. Inoue, M., Tokutomi, N., and Akaike, N. 1987. Modulation of the gamma-aminobutyric acid-gated chloride current by intracellular calcium in frog sensory neurons. Jap. J. Physiol. 37: 379-391.
50. - accumulation and depletion in cultured rat midbrain neurons. J. Neurosci. 19: 4695-4704.
51. + activity in hypoglossal neurons in vitro. J. Neurophysiol. 66: 103-111.
52. + homeostasis during anoxia in rat hypoglossal neurons: intracellular and extracellular in vitro studies J. Physiol. (London), 448: 697-708.
53. Johansen, F.F., and Diemer, N.H. 1991. Enhancement of GABA neurotransmission after cerebral ischemia in the rat reduces loss of hippocampal CA1 pyramidal cells. Acta Neurol. Scand. 84: 1-6.
54. Johansen, F.F., Christensen, T.C., Jensen, M.S., Valente, E., Jensen, C.V., Nathan, T., Lambert, J.D.C., and Diemer, N.H. 1991. Inhibition in postischemic rat hippocampus: GABA receptors, GABA release, and inhibitory postsynaptic potentials. Expl. Brain Res. 84: 529-537.
55. A receptor channel function in the nervous system. Prog. In Neurobiol. 42: 489-537.
56. Kass, I.S., and Lipton, P.J. 1982. Mechanisms involved in irreversible anoxic damage to the in vitro hippocampal slice. J. Physiol. (London), 332: 459-472.
57. Kass, I.S., Abramowicz, A.E., Cottrell, J.E., and Chambers, G. 1992. The barbiturate thiopental reduces ATP levels during anoxia but improves electrophysiological recovery and ion homeostasis in the rat hippocampal slice. Neuroscience, 49: 537-543.
58. Khazipov, R., Bregetovski, P., and Ben-Ari, Y. 1993. Hippocampal inhibitory interneurons are functionally disconnected from excitatory impacts by anoxia. J. Neurophysiol. 70: 1-9.
59. 2+ concentrations in the hippocampus. Can. J. Physiol. Pharmacol. 60: 1658-1671.
60. Lipton, P., and Whittingham, T.S. 1982. Reduced ATP concentration as a basis for synaptic transmission failure during hypoxia in the in vitro guinea-pig hippocampus. J. Physiol. (London), 325: 51-65.
61. Llano, I., Leresche, N., and Marty, A. 1991. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron, 6: 565-574.
62. Lutz, P.L. 1992. Mechanisms for anoxic survival in the vertebrate brain. Annu. Rev. Physiol. 54: 601-618.
63. Lyden, P. 1997. GABA and neuroprotection. In Neuroprotective agents and cerebral ischaemia. Edited by A.R. Green and A.J. Cross. Academic Press, New York, N.Y. pp. 233-258.
64. Martin, R.L., Lloyd, H.G.E., and Cowan, A.I. 1994. The early events of oxygen and glucose decline setting the scene for neuronal death? Trends Neurosci. 17: 251-257.
65. Morris, M.E. 1974. Hypoxia and extracellular potassium activity in the guinea-pig cortex. Can. J. Physiol. Pharmacol. 52: 872-882.
66. - in GABA (γ-aminobutyric acid)-evoked depolarization of peripheral nerve. Brain Res. 278: 127-135.
67. 2+ ion concentration activity in cat spinal neurons in situ. Neuroscience, 14: 563-580.
68. Morris, M.E., Leblond, J., Agopyan, N., and Krnjevic, K. 1991. Temperature dependence of extracellular ionic changes evoked by anoxia in hippocampal slices. J. Neurophysiol. 65: 157-167.
69. A-mediated potentials evoked by 4-aminopyridine in the adult rat hippocampus. Exp. Brain Res. 109: 71-82.
70. A receptor activation attenuates excitotoxicity but exacerbates oxygen-glucose deprivation-induced neuronal injury in vitro. J. Cereb. Blood Flow Metab. 16: 1211-1218.
71. Müller, W., Misgeld, U., and Lux, H.D. 1989. γ-Aminobutyric acid-induced ion movements in the guinea pig hippocampal slice. Brain Res. 484: 184-191.
72. i and membrane currents during impaired mitochondrial metabolism in dissociated rat hippocampal neurons. J. Physiol. (London), 507: 131-145.
73. Obrenovitch, T.P., and Urenjak, J. 1997. Altered glutamatergic transmission in neuronal disorders from high extracellular glutamate to excessive synaptic efficacy. Prog. Neurobiol. 51: 39-87.
74. o in the guinea pig hippocampus. Can. J. Physiol. Pharmacol. 71: Axviii.
75. Obrocea, G.V., and Morris, M.E. 1993b. Role of GABA (γ-aminobutyric acid) in anoxic-induced ion changes in the hippocampus. Soc. Neurosci. Abstr. 19: 1138.
76. o evoked by baclofen in guinea pig hippocampus. Can. J. Physiol. Pharmacol. 76: 148-154.
77. Obrocea, G.V., Leppanen, L., and Morris, M.E. 1994. Ion changes evoked by anoxia: osmotic shifts and role of γ-aminobutyric acid (GABA) receptors. Soc. Neurosci. Abstr. 20: 505.
78. Oehme, M., and Simon, W. 1976. Microelectrode for potassium ions based on a neutral carrier and comparison of its characteristics with a cation exchanger sensor. Anal. Chem. 86: 21-25.
79. Perkins, K.L., and Wong, R.K. 1996. Ionic basis of the postsynaptic depolarizing GABA response in hippocampal pyramidal cells. J. Neurophysiol. 76: 3886-3894.
80. Perkins, K.L., and Wong, R.K.S. 1997. The depolarizing response. Can. J. Physiol. Pharmacol. 75: 516-519.
81. A responses in hippocampal pyramidal cells. J. Neurosci. 12: 4122-4132.
82. Pumain, R., Louvel, J., and Kurcewicz, I. 1986. Long-term alterations in amino acid-induced ionic conductances in chronic epilepsy. In Excitatory amino acids and epilepsy. Edited by R. Schwarcz and Y. Ben-Ari. Plenum Press, New York, N.Y. pp. 439-447.
83. Ravindran, J., Shuaib, A., Ijaz, S., Galazka, P., Waqar, T., Ishaqzay, R., Miyashita, H., and Liu, L. 1994. High extracellular GABA levels in hippocampus as a mechanism of neuronal protection in cerebral ischemia in adrenalectomized gerbils. Neurosci. Letts. 176: 209-211.
84. Rosen, A.S., and Morris, M.E. 1991. Depolarizing effects of anoxia on pyramidal cells of rat neocortex. Neurosci. Letts. 124: 169-173.
85. Rosen, A.S., and Morris, M.E. 1993. Anoxic depression of excitatory and inhibitory postsynaptic potentials in rat neocortical slices. J. Neurophysiol. 69: 109-117.
86. Rovira, C., Ben-Ari, Y., and Cherubini, E. 1984. Somatic and dendritic actions of γ-aminobutyric acid agonists and uptake blockers in the hippocampus in vivo. Neuroscience, 12: 543-555.
87. Saransaari, P., and Oja, S.S. 1998. Release of endogenous glutamate, aspartate, GABA and taurine from hippocampal slices from adult and developing mice under cell-damaging conditions. Neurochem. Res. 23: 563-570.
88. Schatzki, A., McMillian, M., and Miller, L.G. 1990. Glutamate, kainate and quisqualate enhance GABA-dependent chloride uptake in cortex. Brain Research Bull. 25: 239-243.
89. - uptake in rat brain synaptosomes: evidence for rapid desensitization of the GABA receptor-coupled chloride ion channel. Mol. Pharmacol. 30: 419-426.
90. Schwartz, R.D., Yu, X., Katzman, M.R., Hayden-Hixson, D.M., and Perry, J.M. 1995. Diazepam, given postischemia, protects selectively vulnerable neurons in the rat hippocampus and striatum. J. Neurosci. 15: 529-539.
91. 2+] in hypoxia and ischemia in rat brain in vivo. J. Gen. Physiol. 95: 837-866.
92. +] during recovery from short-term transient ischemia. J. Cereb. Blood Flow Metab. 12: 759-772.
93. Silver, I.A., Deas, J., and Erecinska, M. 1997. Ion homeostasis in brain cells: differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. Neuroscience, 78: 589-601.
94. Sternau, L.L., Lust, W.D., Ricci, A.J., and Ratcheson, R. 1989. Role for γ-aminobutyric acid in selective vulnerability in gerbils. Stroke, 20: 281-287.
95. - cotransporter in immature cortical neurons: a role in intracellular regulation. J. Neurophysiol. 81: 1939-1948.
96. Suzdak, P.D., and Jansen, J.A. 1995. A review of the preclinical pharmacology of tiagabine: a potent and selective anticonvulsant GABA uptake inhibitor. Epilepsia, 36: 613-626.
97. Thalmann, R., Peck, E.J., and Ayala, G.F. 1981. Biphasic response of hippocampal pyramidal neurons to GABA. Neurosci. Letts. 21: 319-324.
98. Thompson, S.M. 1994. Modulation of inhibitory synaptic transmission in the hippocampus. Prog. in Neurobiol. 42: 565-609.
99. B receptor-mediated presynaptic inhibition in the hippocampus in vitro. J. Neurophysiol. 61: 524-533.
100. Torp, R., Arvin, B., Le Peillet, E., Chapman, A.G., Ottersen, O.P., and Meldrum, B.S. 1993. Effect of ischaemia and reperfusion on the extra- and intracellular distribution of glutamate, glutamine, aspartate and GABA in the rat hippocampus, with a note on the effect of the sodium channel blocker BW 1003C87. Exp. Brain Res. 96: 365-376.
101. Tossman, U., and Ungerstedt, U. 1986. Microdialysis in the study of extracellular levels of amino acids in the rat brain. Acta Physiol. Scand. 128: 9-14.
102. Tossman, U., Jensson, G., and Ungerstedt, U. 1986. Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol. Scand. 127: 533-545.
103. Yamamoto, S., Tanaka, E., and Higashi, H. 1997. Mediation by intracellular calcium-dependent signals of hypoxic hyperpolarization in rat hippocampal CA1 neurons in vitro. J. Neurophysiol. 77: 386-392.
104. +-channel blocking agents. Neuroscience, 67: 815-821.
105. Zhu, P.J., and Krnjevic, K. 1994. Anoxia selectively depresses excitatory synaptic transmission in hippocampal slices. Neurosci. Letts. 166: 27-30.