Abstract
The release of glutamate and GABA in response to K+ depolarization was determined for tissue prisms prepared from brain subregions removed from rats following 30 min of forebrain ischemia or recirculation periods up to 24 h. There were statistically significant effects of this treatment on release of both amino acids from samples of the dorsolateral striatum, an area developing selective neuronal degeneration. However, for at least the first 3 h of recirculation the calcium-dependent and calcium-independent release of both amino acids in this region were similar to pre-ischemic values. Differences were observed under some conditions at longer recirculation times. In particular there was a decrease in calcium-dependent GABA release at 24 h of recirculation and a trend towards increased release of glutamate at 6 h of recirculation and beyond. No statistically significant differences were seen in samples from the paramedian neocortex, a region resistant to post-ischemic damage. These results suggest that changes in the ability to release glutamate and GABA in response to stimulation are not necessary for the development of neurodegeneration in the striatum but rather that release of these amino acids may be modified as a result of the degenerative process.
Similar content being viewed by others
References
Kirino, T. 1982. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Research 239:57–69.
Pulsinelli, W. A., Levy, D. E., and Duffy, T. E. 1982. Regional cerebral blood flow and glucose metabolism following transient forebrain ischemia. Ann. Neurol. 11:499–509.
Smith, M. L., Auer, R. N., and Siesjö, B. K. 1984. The density and distribution of ischemic brain injury in the rat following 2–10 min of forebrain ischemia. Acta Neuropathol. (Berl.) 64:319–332.
Benveniste, H., Jorgensen, M. B., Sandberg, M., Christensen, T., Hagberg, H., and Diemer, N. H. 1989. Ischemic damage in hippocampal CA1 is dependent on glutamate release and intact innervation from CA3. J. Cereb. Blood flow Metab. 9:629–639.
Jorgensen, M. B., Johansen, F. F., and Diemer, N. H. 1987. Removal of the entorhinal cortex protects hippocampal CA1 neurons from ischemic damage. Acta Neuropathol. (Berl.) 73:189–194.
Globus, M. Y.-T., Ginsberg, M. D., and Busto, R. 1991. Excitotoxic index: A biochemical marker of selective vulnerability. Neurosci. Lett. 127:39–42.
Sheardown, M. J., Nielsen, E. O., Anker, J. H., Jacobsen, P., and Honoré, T. 1990. 2,3-Dihydroxy-6-nitro-7-sulfamoylbenzo(F)quinoxaline: A neuroprotectant for cerebral ischemia. Science 247:571–574.
Siesjö, B. K., and Bengtsson, F. 1989. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia and spereading depression: A unifying hypothesis. J. Cereb. Blood Flow Metab. 9:127–140.
Le Peillet, E., Arvin, B., Moncada, C., and Meldrum, B. S. 1992. The non-NMDA antagonists, NBQX and GYKI 52466, protect against cortical and striatal cell loss following transient global ischemia in the rat. Brain Research 571:115–120.
Globus, M. Y.-T., Ginsberg, M. D., Dietrich, W. D., Busto, R., and Scheinberg, P. 1987. Substantia nigra lesion protects against ischemic damage in the striatum. Neurosci. Lett. 80:251–256.
Wieloch, T., Miyauchi, T., and Lindvall, O. 1990. Neuronal damage in the striatum following forebrain ischemia: Lack of effect of selective lesions of mesostriatal dopamine neurons. Exp. Brain Research 83:159–163.
Baker, A. J., Zornow, M. H., Scheller, M. S., Yaksh, T. L., Skilling, S. R., Smullin, D. H., Larsen, A. A., and Kuczenski, R. 1991. Changes in extracellular concentrations of glutamate, aspartate, glycine, dopamine, serotonin, and dopamine metabolites after transient global ischemia in the rabbit brain. J. Neurochem. 57:1370–1379.
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.
Brannan, T. S., Weinberger, J., Knott, P., Taff, I., Kaufmann, H., Togasaki, D., and Nieves-Rosa, J. 1987. Direct evidence of massive striatal dopamine release in gerbils with unilateral strokes. Stroke 18:108–110.
Globus, M. Y.-T., Busto, R., Martinez, E., Valdes, I., Dietrich, W. D., and Ginsberg, M. D. 1991. Comparative effect of transient global ischemia on extracellular levels of glutamate, glycine, and gamma-aminobutyric acid in vulnerable and non-vulnerable brain regions in the rat. J. Neurochem. 57:470–478.
Hagberg, H., Lehmann, A., Sandberg, M., Nyström, B., Jacobson, I., and Hamberger, A. 1985. Ischemia-induced shift of inhibitory and excitatory amino acids from intra-to extracellular components. J. Cereb. Blood Flow Metab. 5:413–419.
Mitani, A., Andou, Y., and Kataoka, K. 1992. Selective vulnerability of hippocampal CA1 neurons cannot be explained in terms of an increase in glutamate concentration during ischemia in the gerbil: brain microdialysis study. Neuroscience 48:307–313.
Buzsaki, G., Freund, T. F., Bayardo, F., and Somogyi, P. 1989. Ischemia-induced changes in the electrical activity of the hippocampus. Exp. Brain Research 78:268–278.
Hossmann, K.-A., Sakaki, S., and Kimoto, K. 1976. Cerebral uptake of glucose and oxygen in the cat brain after prolonged ischemia. Stroke 7:301–305.
Pulsinelli, W. A., Brierley, J. B., and Plum, F. 1982. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11:491–498.
Pulsinelli, W. A., and Duffy, T. E. 1983. Regional energy balance in rat brain after transient forebrain ischemia. J. Neurochem. 40:1500–1503.
Sims, N. R., Bowen, D. M., and Davison, A. N. 1981. [14C]Acetylcholine synthesis and [14C]carbon dioxide production from [U-14C]glucose by tissue prisms from human neocortex. Biochem. J. 196:867–876.
Donzanti, B. A., and Yamamoto, B. K. 1988. An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates. Life Sci. 43:913–922.
Lowry, O. H., Rosebrough, N. J. Farr, A. L., and Randall, R. J. 1951. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193:265–275.
Nicholls, D. G. 1989. Release of glutamate, aspartate, and gamma-aminobutyric acid from isolated nerve terminals. J. Neurochem. 52:331–341.
Nicholls, D. G., Sihra, T. S., and Sanchez-Prieto, J. 1987. Calcium-dependent and-independent release of glutamate from synaptosomes monitored by continuous fluorometry. J. Neurochem. 49:50–57.
Sims, N. R. 1992. Energy metabolism and selective neuronal vulnerability following global cerebral ischemia. Neurochem. Research 17:923–931.
Sims, N. R., and Pulsinelli, W. A. 1987. Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J. Neurochem. 49:1367–1374.
Sims, N. R. 1991. Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. J. Neurochem. 56:1836–1844.
Zaidan, E., and Sims, N. R. 1993. Selective reductions in the activity of the pyruvate dehydrogenase complex in mitochondria isolated from brain subregions following forebrain ischemia in rats. J. Cereb. Blood Flow Metab. 13:98–104.
Dienel, G. A. 1984. Regional accumulation of calcium in postischemic rat brain. J. Neurochem. 43:913–925.
Suzuki, R., Yamaguchi, T., Li, C.-L., and Klatzo, I. 1983. The effects of 5-minute ischemia in Mongolian gerbils. II Changes in spontaneous neuronal activity in cerebral cortex and CA1 sector of hippocampus. Acta Neuropathol. 60:217–222.
Armstrong, D. R., Neill, K. H., Crain, B. J., and Nadler, J. V. 1989. Absence of electrographic seizures after transient forebrain ischemia in the Mongolian gerbil. Brain Research 476:174–178.
Zaidan, E., and Sims, N. R. 1990. Alterations in the production of14CO2 and [14C]acetylcholine from [U-14C]glucose in brain subregions following transient forebrain ischemia in the rat. J. Neurochem. 55:1882–1889.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sims, N.R. The stimulus-evoked release of glutamate and GABA from brain subregions following transient forebrain ischemia in the rat. Neurochem Res 18, 1073–1079 (1993). https://doi.org/10.1007/BF00966687
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00966687