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Selective vulnerability of brain: New insights from the excitatory synapse

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References

  • Auer, R. N., Wieloch, T., Olsson, Y., and Siesjo, B. K. (1984). The distribution of hypoglycemic brain damage.Acta Neuropathol. 64: 177–191.

    Google Scholar 

  • Bazan, N. G. (1970). Effects of ischemia and electroconvulsive shock on free fatty acid pool in the brain.Biochim. Biophys. Acta 218: 1–8.

    Google Scholar 

  • Ben-Ari, Y. E. (1985). Limbic seizures and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy.Neuroscience 14: 375–403.

    Google Scholar 

  • Ben-Ari, Y. E., Tremblay, E., Ottersen, O. P., and Meldrum, B. S. (1980). The role of epileptic activity in hippocampal and “remote” cerebral lesions induced by kainic acid.Brain Res. 191: 79–97.

    Google Scholar 

  • 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.

    Google Scholar 

  • Blennow, G., Brierly, J. B., Meldrum, B. S., and Siesjo, B. K. (1978). Epileptic brain damage. The role of systemic factors that modify cerebral energy metabolism.Brain 101: 687–700.

    Google Scholar 

  • Brierly, J. B., and Graham, D. I. (1984). Hypoxia and vascular disorders of the central nervous system. In Adams, J. H., Corsellis, J. A. N., and Duchen, L. W. (eds.),Greenfield's Neuropathology, John Wiley & Sons, New York, pp. 125–207.

    Google Scholar 

  • Brown, A. W., and Brierly, J. B. (1973). The earliest alterations in rat neurones after anoxia-ischaimia.Acta Neuropathol. 23: 9–22.

    Google Scholar 

  • Choi, D. W. (1985). Glutamate neurotoxicity in cortical cell cultures is calcium dependent.Neurosci. Lett. 58: 293–297.

    Google Scholar 

  • Collinridge, G. C., Kehl, S. J., and McLennan, H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus.J. Physiol. 334: 33–46.

    Google Scholar 

  • Collins, R. C. (1986). Neurotoxins and the selective vulnerability of brain. In Jenner, P. G. (ed.),Neurotoxins and Their Pharmacological Implications, Raven Press, New York (in press).

    Google Scholar 

  • Collins, R. C., Posner, J., and Plum, F. (1970). Cerebral energy metabolism during electroshock seizures in mice.Am. J. Physiol. 218: 943–950.

    Google Scholar 

  • Collins, R. C., and Olney, J. W. (1982). Focal cortical seizures cause distant thalamic lesions.Science 218: 177–179.

    Google Scholar 

  • Collins, R. C., Lothman, E. W., and Olney, J. (1983a). Status epilepticus in the limbic system: Biochemical and pathological changes. In Delgado-Escueta, A. V., Wasterlain, C. G., Treiman, D. M., and Porter, R. J. (eds.),Advances in Neurology, Vol. 34: Status Epilepticus, Raven Press, New York, pp. 277–295.

    Google Scholar 

  • Collins, R. C., Olney, J. W., and Lothman, E. W. (1983b). Metabolic and pathologic consequences of focal seizures. In Ward, A. A., Pentry, J. K., and Purpura, D. (eds.),Epilepsy, Raven Press, New York, pp. 87–107.

    Google Scholar 

  • Collins, R. C., Santori, E. S., Der, T., Toga, A. W., and Lothman, E. W. (1986). Functional metabolic mapping during forelimb movement in the rat. I. Stimulation of motor cortex.J. Neurosci. 6: 448–462.

    Google Scholar 

  • Cooper, H. K., Zalewska, T., Kawakami, S., Hossman, K. A., and Kliehus, P. (1977). The effect of ischemia and recirculation on protein synthesis in the rat brain.J. Neurochem. 28: 929–938.

    Google Scholar 

  • Croucher, M. J., Collins, J. F., and Meldrum, B. S. (1982). Anticonvulsant action of excitatory amino acid antagonist.Science 216: 889–901.

    Google Scholar 

  • Dempsey, R. J., Roy, M. W., Meyer, K., Cowen, D. E., and Hsin-Hsiung, T. (1986). Development of cyclooxygenase and lipoxygenase metabolites or arachidonic acid after transient cerebral ischemia.J. Neurosurg. 64: 118–124.

    Google Scholar 

  • Dienel, G. A., Pulsinelli, W. A., and Duffy, T. E. (1980). Regional protein synthesis in rat brain following acute hemispheric ischemia.J. Neurochem. 35: 1216–1223.

    Google Scholar 

  • Dingledine, R. (1983). N-methyl aspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells.J. Physiol. 343: 385–405.

    Google Scholar 

  • Dingledine, R. (1986). NMDA receptors: What do they do?TINS 10: 47–49.

    Google Scholar 

  • Duffy, T. E., Howse, D. C., and Plum, F. (1975). Cerebral energy metabolism during experimental status epilepticus.J. Neurochem. 24: 925–934.

    Google Scholar 

  • Earle, K. M., Baldwin, M., and Penfield, W. (1953). Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth.Arch. Neurol. Psychiat. 69: 27–42.

    Google Scholar 

  • Engelsen, B., and Fonnum, F. (1983). Effects of hypoglycemia on the transmitter pool and the metabolic pool of glutamate in rat brain.Neurosci. Lett. 42: 317–322.

    Google Scholar 

  • Evans, M., Griffiths, T., and Meldrum, B. S. (1983). Early changes in the rat hippocampus following seizures induced by bicuculline orl-allylglycine: A light and electron microscope study.Neuropathol. Appl. Neurobiol. 9: 39–52.

    Google Scholar 

  • Evans, M., Griffiths, T., and Meldrum, B. S. (1984). Kainic acid seizures and the reversibility of calcium loading in vulnerable neurons in the hippocampus.Neuropathol. Appl. Neurobiol. 10: 285–302.

    Google Scholar 

  • Fagg, G. E. (1985). L-Glutamate excitatory amino acid receptors and brain function.TINS 8: 207–210.

    Google Scholar 

  • Falconer, M. A. (1971). Genetic and related aetiological factors in temporal lobe epilepsy.Epilepsia 12: 13–31.

    Google Scholar 

  • Fonnum, F., Storm-Mathieson, J., and Divac, I. (1981). Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain.Neuroscience 6: 863–873.

    Google Scholar 

  • Foster, A. C., and Fagg, G. E. (1984). Acidic amino acid binding sites in mammalian neuronal membranes: Their characteristics and relationship to synaptic receptors.Brain Res. Rev. 7: 103–164.

    Google Scholar 

  • Greenamyre, J. T., Olson, J. M. M., Penny, J. B., and Young, A. B. (1985). Autoradiographic characterization of N-methyl-d-aspartate-, quisqualate-, and kainate-sensitive glutamate binding sites.J. Pharmacol. Exp. Ther. 233: 254–269.

    Google Scholar 

  • Griffiths. T., Evans, M. C., and Meldrum, B. S. (1982). Intracellular sites of early calcium accumulation in the rat hippocampus during status epilepticus.Neurosci. Lett. 30: 329–334.

    Google Scholar 

  • Griffiths, T., Evans, M. C., and Meldrum, B. S. (1984). Status epilepticus: the reversibility of calcium loading and acute neuronal pathological changes in the rat hippocampus.Neuroscience 12: 557–567.

    Google Scholar 

  • Hass, W. K. (1981). Beyond cerebral blood flow, metabolism and ischemic thresholds: Examination of the role of calcium in the initiation of cerebral infarction. In Meyer, J. S., Lechner, H., Reivich, M., Ott, E. O., and Arabinar, A. (eds.),Cerebral Vascular Disease, Vol. 3, Proceedings of the 10th Salzburg Conference on Cerebral Vascular Disease, Excerpta Medica, Amsterdam, pp. 3–17.

    Google Scholar 

  • House, D. C. (1983). Cerebral energy metabolism during experimental status epilepticus. In Delgado-Escueta, A. V., Wasterlain, C. G., Treiman, D. M., and Porter, R. J. (eds.),Advances in Neurology, Vol. 34. Status Epilepticus, Raven Press, New York, pp. 209–216.

    Google Scholar 

  • Ingvar, M., Soderfel, B., Folbergrova, J., Kalimo, H., Olsson, Y., and Siesjo, B. K. (1984). Metabolic, circulatory and structural alterations in the rat brain induced by sustained pentylenetetrazole seizures.Epilepsia 25(2): 191–204.

    Google Scholar 

  • Kalimo, H., Auer, R. N., and Siesjo, B. K. (1985). The temporal evolution of hypoglycemic brain damage.Acta Neuropathol. 67: 37–50.

    Google Scholar 

  • Levy, D. E., Brierly, J. B., Silverman, D. G., and Plum, F. (1975). Brief hypoxia-ischemia initially damages cerebral neurons.Arch. Neurol. 32: 450–456.

    Google Scholar 

  • Lodge, D., O'Shaughnessy, C. T., and Zeman, S. (1986). Reduction of ischemia-induced brain damage and of glutamate-induced calcium uptake by subanesthetic concentrations of ketamine.Neurosci. Lett. Suppl. 24: 535.

    Google Scholar 

  • Lothman, E. W., and Collins, R. C. (1981). Kainic acid induced limbic seizures: Metabolic, behavioral, electroencephalographic and neuropathological correlates.Brain Res. 218: 299–318.

    Google Scholar 

  • MacDermott, A. B., Mazer, M. L., Westbrook, G. L., Smith, S. J., and Barker, J. L. (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones.Nature 321: 519–522.

    Google Scholar 

  • Meldrum, B. S. (1985). Possible therapeutic applications of antagonists of excitatory amino acid neurotransmitters.Clin. Sci. 68: 113–122.

    Google Scholar 

  • Meldrum, B. S., and Brierly, J. B. (1973). Prolonged epileptic seizures in primates: Ischemic cell change and its relation to ictal physiological events.Arch. Neurol. 28: 10–17.

    Google Scholar 

  • Meldrum, B. S., and Corsellis, J. A. N. (1984). Epilepsy. In Adams, J. H., Corsellis, J. A. N., and Duchen, L. W. (eds.),Greenfield's Neuropathology, John Wiley & Sons, New York, pp. 921–950.

    Google Scholar 

  • Meldrum, B. S., Vigouroux, R. A., and Brierly, J. B. (1973). Systematic factors and epileptic brain damage. Prolonged seizures in paralyzed ventilated baboons.Arch. Neurol. 29: 82–87.

    Google Scholar 

  • Menini, C., Meldrum, B. S., Riche, D., Silva-Compte, C., and Stutzmann, J. M. (1980). Sustained limbic seizures induced by intraamygdaloid kainic acid in trhe baboon: Symptomatology and neuropathological consequences.Ann. Neurol. 8: 501–509.

    Google Scholar 

  • Meyer, A., Falconer, M. A., and Beck, E. (1954). Pathological findings in temporal lobe epilepsy.J. Neurol. Neurosurg. Psychiat. 17: 276–285.

    Google Scholar 

  • Meyers, R. E. (1979). A unitary theory of causation of anoxic and hypoxic brain pathology.Adv. Neurol. 26: 195–213.

    Google Scholar 

  • Monaghan, D. T., and Cotman, C. W. (1982). The distribution of [3H] kainic acid binding sites in rat CNS as determined by autoradiography.Brain Res. 252: 91–100.

    Google Scholar 

  • Monaghan, D. T., Holets, V. R., Toy, D. W., and Cotman, C. W. (1983). Anatomical distributions of four pharmacologically distinct H-L-glutamate binding sites.Nature 306: 176–179.

    Google Scholar 

  • Moskowitz, M. A., Kiwak, K. J., Hekimian, K., and Levine, L. (1984). Synthesis of compounds with properties of leukotrienes C4 and D4 in gerbil brains after ischemia reperfusion.Science 224: 886–888.

    Google Scholar 

  • Nadler, J. V., Perry, B. W., and Cotman, C. W. (1978). Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells.Nature 271: 676–677.

    Google Scholar 

  • Nadler, J. V., Evenson, D. A., and Cuthbertson, G. J. (1978). Comparative toxicity of kainic acid and other amino acids toward rat hippocampal neurons.Neuroscience 6: 2505–2517.

    Google Scholar 

  • Nevander, G., Ingvar, M., Auer, R., and Siesjo, B. K. (1986). Status epilepticus in well-oxygenated rats causes neuronal necrosis.Ann. Neurol. 18: 281–290.

    Google Scholar 

  • Olney, J. W. (1978). Neurotoxicity of excitatory amino acids. In McGeer, E., Olney, J. W., and McGeer, P. (eds.),Kainic Acid as a Tool in Neurobiology, Raven Press, New York, pp. 95–121.

    Google Scholar 

  • Olney, J. W. (1983). Excitotoxins: an overview. In Fuxe, K., Roberts, P., and Schwarcz, R. (eds.),Excitotoxins, Macmillan, London.

    Google Scholar 

  • Olney, J. W., Rhee, V.. and Ho, O. L. (1974). Kainic acid: A powerful neurotoxic analogue of glutamate.Brain Res. 77: 507–512.

    Google Scholar 

  • Olney, J. W., Sharpe, L. G., and deGubareff, T. (1975). Excitotoxic amino acids.Neurosci. Abstr. 1: 371.

    Google Scholar 

  • Olney, J. W., Fuller, T., and DeGubareff, T. (1979). Acute dendrotoxic changes in the hippocampus of kainate treated rats.Brain Res. 176: 91–100.

    Google Scholar 

  • Oleny, J. W., DeGubareff, T., and Sloviter, R. S. (1983). “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. II. Ultrastructural analysis of acute hippocampal pathology.Brain Res. Bull.10: 699–712.

    Google Scholar 

  • Olney, J. W., Collins, R. C., and Sloviter, R. S. (1986). Excitotoxic mechanisms of epileptic brain damage. In Delgado-Escueta, A. V., Ward, A. A., Woodbury, D. W., and Porter, R. J. (eds.),Advances in Neurology Vol. 44. Basic Mechanisms of the Epilepsies, Raven Press, New York, pp. 857–877.

    Google Scholar 

  • Peterson, D. W., Collins, J. F., and Bradford, H. F. (1984). Anticonvulsant action of amino acids antagonists against kindled hippocampal seizures.Brain Res. 311: 176–180.

    Google Scholar 

  • Pfleger, L. (1880). Beobachtungen über Schrumpfung und sclerose des Ammonshornes bei epilepsie.Allg. Z. Psychiat. 36: 359–365.

    Google Scholar 

  • Plum, F. (1983). What causes infaction in ischemie brain?Neurology 33: 22–30.

    Google Scholar 

  • Price, M. T., Olney, J. W., Samson, L., and Labruyere, J. (1985). Calcium influx accompanies but does not cause excitotoxin-induced neuronal necrosis in retina.Brain Res. Bull. 14: 369–376.

    Google Scholar 

  • Pulsinelli, W. A., Brierly, J. B., and Plum, F. (1982a). Temporal profile of neuronal damage in a model of transient forebrain ischemia.Ann. Neurol. 11: 491–498.

    Google Scholar 

  • Pulsinelli, W., Waldman, S., Rawlinson, D., and Plum, F. (1982b). Moderate hyperglycemia augments ischemie brain damage: A neuropathologic study in the rat.Neurology 32: 1239–1246.

    Google Scholar 

  • Purpura, D. P., and Gonzalez-Monteagudo, O. (1960). Acute effects of methoxypyridoxine on hippocampal end-blade neurons: An experimental study of “special pathoclisis” in the cerebral cortex.J. Neuropathol. Exp. 19: 421–432.

    Google Scholar 

  • Rehncrona, S., Rosen, I., and Siesjo, B. K. (1980). Excessive cellular acidosis: An important mechanism of neuronal damage in the brain? Acta Physiol. Scand.110: 435–437.

    Google Scholar 

  • Rothman, S. M. (1983). Synaptic activity mediates death of hypoxic neurons.Science 220: 536–537.

    Google Scholar 

  • Rothman, S. (1984). Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death.J. Neurosci. 4: 1884–1891.

    Google Scholar 

  • Rothman, S. M. (1985). The neurotoxicity of excitatory amino acids is produced by passive chloride influx.J. Neurosci. 5: 1483–1489.

    Google Scholar 

  • Rothman, S. M., and Olney, J. W. (1986). Glutamate and the pathophysiology of hypoxic-ischemic brain damage.Ann. Neurol. 19: 105–111.

    Google Scholar 

  • Rothman, S. M., Thurston, J. H., Hauhart, R. E., Clark, G. D., and Solomer, J. S. (1986). Ketamine protects hippocampal neurons from anoxiain vitro (submitted for publication).

  • Schwob, J. E., Fuller, T., Price, J. L., and Olney, J. W. (1980). Widespread patterns of neuronal damage following systemic or intracerebral injection of kainic acid: A histological study.Neuroscience 5: 991–1014.

    Google Scholar 

  • Shinozaki, H. and Konishi, S. (1970). Actions of several antihelmintics and insecticides on rat cortical neurons.Brain Res. 24: 368–371.

    Google Scholar 

  • Siesjo, B. K. (1981). Cell damage in the brain: A speculative synthesis.J. Cereb. Blood Flow Metab. 1: 155–185.

    Google Scholar 

  • Siesjo, B. K., and Wieloch, T. (1985). Cerebral metabolism in ischemia: Neurochemical basis for therapy.Br. J. Anaesth. 57: 47–62.

    Google Scholar 

  • Siesjo, B. K., and Wieloch, T. (1986). Epileptic brain damage: Pathophysiology and neurochemical pathology. In Delgado-Escueta, A. V., Ward, A. A., Woodbury, D. M., and Porter, R. J. (eds.),Basic Mechanisms of the Epilepsies, Adv. Neurol. Vol. 44, Raven Press, New York, pp. 813–847.

    Google Scholar 

  • Simon, R. P., Swan, J. H., Griffiths, T., and Meldrum, B. S. (1984). Blockade of N-methyl-d-aspartate receptors may protect against ischemic damage in brain.Science 226: 850–852.

    Google Scholar 

  • Sloviter, R. S. (1983). “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies.Brain Res. Bull. 10: 675–697.

    Google Scholar 

  • Sloviter, R. S., and Dempsey, D. F. (1985). “Epileptic” brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or asparate but not by GABA or acetylcholine.Brain Res. Bull. 15: 39–60.

    Google Scholar 

  • Sommer, W. (1880). Erkrankung des Ammonshornes als aetiologisches moment der epilepsie.Arch. Psychiat. Nervenkrauk. 10: 631–675.

    Google Scholar 

  • Spielmeyer, W. (1925). Zur pathogenese ortlich elektiven geherneuron derungen.Z. Neurol. Psychiat. 99: 756–776.

    Google Scholar 

  • Spielmeyer, W. (1928). Die pathogenese des epileptischen krampfes.Z. Neurol, Psychiat. 109: 631–675.

    Google Scholar 

  • Stringer, J. H., and Guyenet, P. G. (1983). Elimination of long-term potentiation in the hippocampus by phencyclidine and ketamine.Brain Res. 258: 159–164.

    Google Scholar 

  • Suzuki, R., Yamaguchi, T., Choh-Luh, L., and Klatzo, I. (1983). The effects of 5-minute ischemia in mongolian gerbils. II. Changes of spontaneous neuronal activity in cerebral cortex and CA1 sector of hippocampus.Acta Neuropathol.60: 217–228.

    Google Scholar 

  • Takemoto, T. (1978). Isolation and structural identification of naturally occurring excitatory amino acids. In McGeer, E., Olney, J. W., and McGeer, P. (eds.),Kainic Acid as a Tool in Neurobiology, Raven Press, New York, pp. 1–15.

    Google Scholar 

  • Taylor, D. C., and Ornsted, C. (1971). Biological mechanisms influencing the outcome of seizures in response to fever.Epilepsia 12: 33–45.

    Google Scholar 

  • Tremblay, E., Represa, A., and Ben-Ari, Y. (1985). Autoradiographic localization of kainic acid binding sites in the human hippocampus.Brain Res. 343: 378–382.

    Google Scholar 

  • Von Hanwehr, R., Smith, M. L., and Siesjo, B. K. (1986). Extra- and intracellular ph during near-complete forebrain ischemia in the rat.J. Neurochem. 46: 331–339.

    Google Scholar 

  • Wieloch, T. (1985). Hypoglycemic induced neuronal damage prevented by an N-methylsparatate antagonist.Science 230: 631–683.

    Google Scholar 

  • Wieloch, T., Engelsen, B., Westerberg, E., and Auer, R. (1985). Lesions of the glutamatergic corticostriatal projections in the rat ameliorate hypoglycemic brain damage in the striatum.Neurosci. Lett. 58: 25–30.

    Google Scholar 

  • Wooten, G. F., and Collins, R. C. (1980). Regional brain glucose utilization following intrastriatal injections of kainic acid.Brain Res. 201: 173–184.

    Google Scholar 

  • Yoshida, S., Kouichi, A., Busto, P., Watson, B. D., Kogure, K., and Ginsberg, M. D. (1982). Influence of transient ischemia on lipid-soluble antioxidants, free fatty acids and energy metabolites in rat brain.Brain Res. 245: 307–316.

    Google Scholar 

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Collins, R.C. Selective vulnerability of brain: New insights from the excitatory synapse. Metabolic Brain Disease 1, 231–240 (1986). https://doi.org/10.1007/BF00999353

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