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Glutamatergic, Cholinergic, and GABAergic Systems in Posterior Cingulate Cortex: Interactions and Possible Mechanisms of Limbic System Disease

  • John W. Olney
  • Michael A. Sesma
  • David F. Wozniak

Abstract

Glutamate and related excitatory amino acids (EAA) have become recognized as the Jekyll/Hyde molecules of the central nervous system (CNS). These agents serve vitally important metabolic, neurotrophic, and neurotransmitter roles in the mammalian brain, but also harbor treacherous neurotoxic (excitotoxic) potential. Accumulating evidence implicates endogenous excitotoxins, primarily glutamate, in the pathophysiology of various neurological disorders, and researchers have developed antagonists which, by blocking EAA receptors, can protect neurons against excitotoxic degeneration. Considerable attention has been focused on a particular subtype of EAA receptor, the N-methyl-D-aspartate (NMDA) receptor, and antagonists of this receptor have been shown to have remarkable neuroprotective properties.

Keywords

NMDA Receptor Excitatory Amino Acid GABAergic Neuron Kainic Acid NMDA Antagonist 
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References

  1. Allen HL, Iversen LL (1990): Phencyclidine, dizocilpine and cerebrocortical neurons. Science 247: 221CrossRefGoogle Scholar
  2. Benveniste H, Drejer J, Schousboe A, Diemer NM (1984): Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral micro-dialysis. J Neurochem 43: 1369–1374CrossRefGoogle Scholar
  3. Burke RF (1986): The relative selectivity of anticholinergic drugs for M1 and M2 muscarinic receptor subtypes. Movement Disorders 1: 135–144CrossRefGoogle Scholar
  4. Chicro WJ, Waters MG, Blobel G (1988): 70K heat shock related proteins stimulate protein translocation into microsomes. Nature (London) 332: 805–810CrossRefGoogle Scholar
  5. Choi DW (1988): Glutamate neurotoxicity and diseases of the nervous system. Neuron 1: 623–634CrossRefGoogle Scholar
  6. Choi DW, Koh J, Peters S (1988): Pharmacology of glutamate neurotoxicity in cortical cell culture: Attenuation by NMDA antagonists. J Neurosci 8: 185–196Google Scholar
  7. Clifford DB, Olney JW, Benz AM, Fuller TA, Zorumski CF (1990): Ketamine, phencyclidine and MK-801 protect against kainic acid induced seizure-related brain damage. Epilepsia 31: 382–390CrossRefGoogle Scholar
  8. Clifford DB, Zorumski CF, Olney JW (1989): Ketamine and MK-801 prevent degeneration of thalamic neurons induced by focal cortical seizures. Exp Neurol 105: 272–279CrossRefGoogle Scholar
  9. Collingridge GL, Kehl SJ, McLennan H (1983): Excitatory amino acids in synaptic transmission in the Shaffer collateral-commissural pathway of the rat hippocampus. J Physiol (London) 334: 33–46Google Scholar
  10. Curtis DR, Watkins JC (1960): The excitation and depression of spinal neurons by structurally related amino acids. J Neurochem 6: 117–141CrossRefGoogle Scholar
  11. Curtis DR, Watkins JC (1963): Acidic amino acids with strong excitatory actions on mammalian neurons. J Physiol (London) 166: 1–14Google Scholar
  12. Dingledine R (1983): N-Methylaspartate activates voltage-dependent calcium conductances in rat hippocampal pyramidal cells. J Physiol (London) 343: 385–405Google Scholar
  13. Dragunow M, Faull RLM (1990): MK-801 induces c-fos protein in thalamic and neocortical neurons of rat brain. Neurosci Lett 111: 39–45CrossRefGoogle Scholar
  14. Faden AI, Demediuk S, Panter S, Vink R (1989): The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244: 798–800CrossRefGoogle Scholar
  15. Faden AI, Simon RP (1987): N-Methyl-D-aspartate receptor antagonist MK-801 improves outcome following experimental spinal cord injury in rats. Neurosci Abstr 13: 1031Google Scholar
  16. Fonnum F (1984): Glutamate: A neurotransmitter in mammalian brain. J Neurochem 42: 1–11CrossRefGoogle Scholar
  17. Fonnum F, Soreide A, Kvale I, Walker J, Walaas I (1981): Glutamate in corticofugal fibers. Adv Biochem Psychopharmacol 27: 29–41Google Scholar
  18. Freedman SB, Beer MS, Harley EA (1988): Muscarinic M1, M2 receptor binding. Relationship with functional efficacy. Eur J Pharmacol 156: 133–142CrossRefGoogle Scholar
  19. Gill R, Foster AC, Woodruff GN (1987): Systemic administration of MK-801 protects against ischemia-induced hippocampal neuro-degeneration in the gerbil. J Neurosci 7: 3343–3349Google Scholar
  20. Hamos JE, Oblas B, Pulaski-Salo D, Welch WJ, Bole DG, Drachman DA (1991): Expression of heat shock proteins in Alzheimer’s disease. Neurology 41: 354–350CrossRefGoogle Scholar
  21. Hayes RL, Chapouris R, Lyeth BG, Jenkins L, Robinson SE, Young HF, Marmarou A (1987): Pretreatment with phencyclidine (PCP) attenuates long-term behavioral deficits following concussive brain injury in the rat. Neurosci Abstr 13: 1254Google Scholar
  22. Heafield MT, Fearn S, Steventon GB, Waring RH, Williams AD, Sturman SG (1990): Plasma cysteine and sulphate levels in patients with motor neurone, Parkinson’s and Alzheimer’s disease. Neurosci Lett 110: 216–220CrossRefGoogle Scholar
  23. Hubbard TJP, Sander C (1991): The role of heat-shock and chaperon proteins in protein folding: Possible molecular mechanisms. Protein Eng 4: 711–717CrossRefGoogle Scholar
  24. Hume RI, Dingledine R, Heinemann SF (1991): Identification of a site in glutamate receptor subunits that controls calcium permeability. Science 253: 1028–1031CrossRefGoogle Scholar
  25. Ikonomidou C, Price MT, Mosinger JL, Frierdich G, Labruyere J, Shahid Salles K, Olney JW (1989a): Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J Neurosci 9: 1693–1700Google Scholar
  26. Ikonomidou C, Mosinger JL, Shahid Salles K, Labruyere J, Olney JW (1989b): Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J Neurosci 9: 2809–2818Google Scholar
  27. Javits DC, Zukin SR (1991): Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148: 1301–1308Google Scholar
  28. Johnson JW, Ascher P (1987): Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature (London) 325: 529–531CrossRefGoogle Scholar
  29. Johnson JW, Ascher P (1988): The NMDA receptor and its channel. Modulation by magnesium and by glycine. In: Excitatory Amino Acids in Health and Disease, Lodge D, ed. New York: Wiley, pp 143–164Google Scholar
  30. Johnston MV, McKinney M, Coyle JT (1981): Neocortical cholinergic innervation: A description of extrinsic and intrinsic components in the rat. Exp Brain Res 43: 159–172CrossRefGoogle Scholar
  31. Jones EG (1986): Neurotransmitters in the cerebral cortex. J Neurosurg 65: 135–53CrossRefGoogle Scholar
  32. Kim JS, Claus D, Kornhuber HH (1983): Cerebral glutamate, neuroleptic drugs and schizophrenia: Increase of cerebrospinal fluid glutamate levels and decrease of striate body glutamate levels following sulpiride treatment in rats. Eur Neurol 22: 367–370CrossRefGoogle Scholar
  33. Kim JS, Kornhuber HH, Schmid-Burgk W, Holzmuller B (1980): Low cerebrospinal fluid glutamate in schizophrenic patients and a new hypothesis on schizophrenia. Neurosci Lett 20: 379–382CrossRefGoogle Scholar
  34. Kochhar A, Zivin JA, Lyden PD, Mazzarella V (1988): Glutamate antagonist therapy reduces neurologic deficits produced by focal central nervous system ischemia. Arch Neurol (Chicago) 45: 148–153CrossRefGoogle Scholar
  35. Koerner JF, Cotman CW (1981): Micromolar L-2-amino-4-phosphonobutyric acid selectively inhibits perforant path synapses from lateral entorhinal cortex. Brain Res 216: 192–198CrossRefGoogle Scholar
  36. Korttila K, Levanen J (1978): Untoward effects of ketamine combined with diazepam for supplementing conduction anaesthesia in young and middle-aged adults. Acta Anaesthesiol Scand 22: 640–648CrossRefGoogle Scholar
  37. Labruyere J, Price MT, Olney JW (1989): NMDA antagonists induce pathomorphological changes in cerebrocortical neurons. Neurosci Abstr 15: 761Google Scholar
  38. Langlais PJ, Mair RG (1990): Protective effects of the glutamate antagonist MK-801 on pyrithiamine-induced lesions and amino acid changes in rat brain. J Neurosci 10(5): 1664–1674Google Scholar
  39. Lodge D, Anis NA (1982): Effects of phencyclidine on excitatory amino acid activation of spinal interneurons in the cat. Eur J Pharmacol 77: 203–204CrossRefGoogle Scholar
  40. Lodge D, Aram JA, Church J, Davies SN, Martin D, O’Shaughnessy CT, Zeman S (1987): Excitatory amino acids and phencyclidine-like drugs. In: Excitatory Amino Acid Transmission, Hicks TP, Lodge D, McLennan H, eds. New York: Liss, pp 83–90Google Scholar
  41. Lucas DR, Newhouse JP (1957): The toxic effect of sodium L-glutamate on the inner layers of the retina. Arch Ophthalmol 58: 193–201CrossRefGoogle Scholar
  42. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986): NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature (London) 321: 519–522CrossRefGoogle Scholar
  43. MacDonald JF, Miljkovic A, Pennefather P (1987): Use-dependent block of excitatory amino acid current in cultured neurons by ketamine. J Neurophysiol 58: 251–67Google Scholar
  44. MacDonald RL, Barker JL (1978): Different actions of anticonvulsant and anesthetic barbiturates revealed by use of cultured mammalian neurons. Science 200: 775–777CrossRefGoogle Scholar
  45. Magbagbeola JAO, Thomas NA (1974): Effect of thiopentone on emergence reactions to ketamine anaesthesia. Can Anaesth Soc J 21(3): 321CrossRefGoogle Scholar
  46. Marshall BE, Longnecker DE (1990): General anesthetics. In: Goodman and Gillman, The Pharmacological Basis of Therapeutics, Rall TW, Nies AS, Taylor P, eds., New York: Pergamon Press, pp 285–310Google Scholar
  47. Mayer ML, Westbrook GL, Guthrie PB (1984): Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature (London) 309: 261–263CrossRefGoogle Scholar
  48. McDonald JW, Silverstein FS, Johnston MV (1987): MK-801 protects the neonatal brain from hypoxic-ischemic damage. Eur J Pharmacol 140: 359–361CrossRefGoogle Scholar
  49. McDonald JW, Silverstein FS, Johnston MV (1988): Neurotoxicity of N-methyl-D-aspartate is markedly enhanced in developing rat central nervous system. Brain Res 459: 200–203CrossRefGoogle Scholar
  50. Miller RF, Slaughter MM (1986): Excitatory amino acid receptors of the retina: Diversity of subtypes and conductance mechanisms. Trends Neurosci 9: 211–218CrossRefGoogle Scholar
  51. Monaghan DT, Cotman CW (1982): Distribution of [3H] kainic acid binding sites in the rat CNS as determined by autoradiography. Brain Res 252: 91–97CrossRefGoogle Scholar
  52. Monaghan DT, Cotman CW (1985): Distribution of N-methyl-D-aspartate-sensitive L-glutamate binding sites in rat brain. J Neurosci 5: 2909–2917Google Scholar
  53. Monaghan DT, Yao D, Cotman CW (1984): Distribution of [3H]-AMPA binding sites in rat brain as determined by quantitative autoradiography. Brain Res 324: 160–164CrossRefGoogle Scholar
  54. Olney JW (1969a): Brain lesions, obesity and other disturbances in mice treated with mono-sodium glutamate. Science 164: 719–721CrossRefGoogle Scholar
  55. Olney JW (1969b): Glutamate-induced retinal degeneration in neonatal mice. Electron microscopy of the acutely evolving lesion. J Neuropathol Exp Neurol 28: 455–474CrossRefGoogle Scholar
  56. Olney JW (1971): Glutamate-induced neuronal necrosis in the infant mouse hypothalamus: An electron microscopic study. J Neuropathol Exp Neurol 30: 75–90CrossRefGoogle Scholar
  57. Olney JW (1974): Toxic effects of glutamate and related amino acids on the developing central nervous system. In: Heritable Disorders of Amino Acid Metabolism, Nyhan WH, ed. New York: Wiley, pp 501–512Google Scholar
  58. Olney JW (1988): Excitatory transmitters and neuropsychiatric disorders. In: Neuronal Control of Bodily Function: Neurobiology of Amino Acids, Peptides and Trophic Factors, Ferrendelli JA, Collins RC, Johnson EM, eds. Dordrecht, Netherlands: Kluwer Acad Publ, pp 51–61CrossRefGoogle Scholar
  59. Olney JW (1989): Excitatory amino acids and neuropsychiatric disorders. Biol Psychiatry 26: 505–525CrossRefGoogle Scholar
  60. Olney JW (1990): Excitatory amino acid hypothesis of schizophrenia. Biol Psychiatry 28: 553–554CrossRefGoogle Scholar
  61. Olney JW, Collins RC, Sloviter RS (1986a): Excitotoxic mechanisms of epileptic brain damage. In: Basic Mechanisms of the Epilepsies: Molecular and Cellular Approaches, Delgado-Escueta AV, Ward AA, Woodbury DM, Porter RJ, eds. New York: Raven Press, pp 857–878Google Scholar
  62. Olney JW, deGubareff T, Labruyere J (1979): α-Aminoadipate blocks the neurotoxic action of N-methylaspartate. Life Sci 25: 537–540CrossRefGoogle Scholar
  63. Olney JW, Ho OL (1970): Brain damage in infant mice following oral intake of glutamate, aspartate or cysteine. Nature (London) 227: 609–610CrossRefGoogle Scholar
  64. Olney JW, Ho OL, Rhee V (1971): Cytotoxic effects of acidic and sulphur-containing amino acids on the infant mouse central nervous system. Exp Brain Res 14: 61–76CrossRefGoogle Scholar
  65. Olney JW, Ho OL, Rhee V, Schainker B (1972a): Cysteine-induced brain damage in infant and fetal rodents. Brain Res 45: 309–313CrossRefGoogle Scholar
  66. Olney JW, Ikonomidou C, Mosinger JL, Friedrich G (1989a): MK-801 prevents hypobaricischemic neuronal degeneration in infant rat brain. J Neurosci 9: 1701–1704Google Scholar
  67. Olney JW, Labruyere J, Collins JF, Curry K (1981): D-Aminophosphonovalerate is 100-fold more powerful than D-alpha-aminoadipate in blocking N-methyl-D-aspartate neurotoxicity. Brain Res 221: 207–210CrossRefGoogle Scholar
  68. Olney JW, Labruyere J, Price MT (1989b): Pathological changes induced in cerebrocortical neurons by phencyclidine and related drugs. Science 244: 1360–1362CrossRefGoogle Scholar
  69. Olney JW, Labruyere J, Wang G, Sesma MA, Wozniak DF, Price MT (1991): NMDA antagonist neurotoxicity: Mechanism and protection. Science 254: 1515–1518CrossRefGoogle Scholar
  70. Olney JW, Price MT, Fuller TA, Labruyere J, Samson L, Carpenter M, Mahan K (1986b): The anti-excitotoxic effects of certain anesthetics, analgesics and sedative-hypnotics. Neurosci Lett 68: 29–34CrossRefGoogle Scholar
  71. Olney JW, Price M, Shahid Salles K, Labruyere J, Friedrich G (1987a): MK-801 powerfully protects against N-methyl aspartate neurotoxicity. Eur J Pharmacol 141: 357–361CrossRefGoogle Scholar
  72. Olney JW, Price MT, Labruyere J, Shahid Salles K, Friedrich G, Mueller M, Silverman E (1987b): Anti-parkinsonian agents are phencyclidine agonists and N-methyl aspartate antagonists. Eur J Pharmacol 142: 319–320CrossRefGoogle Scholar
  73. Olney JW, Rhee V, Ilo OL (1974): Kainic acid: A powerful neurotoxic analogue of glutamate. Brain Res 77: 507–512CrossRefGoogle Scholar
  74. Olney JW, Sharpe LG, Feigin RD (1972b): Glutamate-induced brain damage in infant primates. J Neuropathol Exp Neurol 31: 464–488CrossRefGoogle Scholar
  75. Olney JW, Zorumski C, Price MT, Labruyere J (1990): L-Cysteine, a bicarbonate-sensitive endogenous excitotoxin. Science 248: 596–599CrossRefGoogle Scholar
  76. Palmer E, Monaghan DT, Cotman CW (1989): Trans-ACPD, a selective agonist to the PI-coupled excitatory amino acid receptor. Eur J Pharmacol 166: 585–587CrossRefGoogle Scholar
  77. Park CK, Nehls DG, Graham DI, Teasdale GM, McCulloch J (1988): Focal cerebral ischaemia in the cat: Treatment with the glutamate antagonist MK-801 after induction of ischaemia. J Cereb Blood Flow Metab 8: 757–762CrossRefGoogle Scholar
  78. Park CK, Nehls DG, Ozyurt E, Graham DI, McCulloch J (1987): Ischemic brain damage is reduced by systemic administration of the N-methyl-D-aspartate (NMDA) antagonist, MK-801. Neurosci Abstr 13: 1029Google Scholar
  79. Perry TL (1982): Normal cerebrospinal fluid and brain glutamate levels in schizophrenia do not support the hypothesis of glutamatergic neuronal dysfunction. Neurosci Lett 28: 81–85CrossRefGoogle Scholar
  80. Ransom RW, Stec NL (1988): Cooperative modulation of MK-801 binding to the N-methyl-D-aspartate receptor-ion channel complex by L-glutamate, glycine, and polyamines. J Neurochem 51: 830–836CrossRefGoogle Scholar
  81. Reich DL, Silvay G (1989): Ketamine: An update on the first twenty-five years of clinical experience. Can J Anaesth 36: 186–97CrossRefGoogle Scholar
  82. Reynolds IJ, Miller RJ (1989): Ifenprodil is a novel type of N-methyl-D-aspartate receptor antagonist: Interaction with polyamines. Mol Pharmacol 36: 758–765Google Scholar
  83. Richards MH (1991). Pharmacology and second messenger interactions of cloned muscarinic receptors. Biochem Pharmacol 42: 1645–1653CrossRefGoogle Scholar
  84. Robinson CS, Crooks GB, Shinkman PG, Gallagher M (1989): Behavioral effects of MK-801 mimic deficits associated with hippocampal damage. Psychobiology 17: 156–164Google Scholar
  85. Romano C, Williams K, Molinoff PB (1991): Polyamines modulate the binding of MK-801 to the solubilized N-methyl-D-aspartate receptor. J Neurochem 57: 811–818CrossRefGoogle Scholar
  86. Rothman SM (1984): Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J Neurosci 4: 1884–1891Google Scholar
  87. Rothman SM, Olney JW (1986): Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann Neurol 19: 105–111CrossRefGoogle Scholar
  88. Schoepp DD, Johnson BG (1989): Inhibition of excitatory amino acid-stimulated phosphoinositide hydrolysis in the neonatal rat hippocampus by 2-amino-3-phosphonopropionate. J Neurochem 53: 273–278CrossRefGoogle Scholar
  89. Schoepp DD, Johnson BG (1991): In vivo 2-amino-3-phosphonopropionic acid administration to neonatal rats selectively inhibits metabotropic excitatory amino acid receptors ex vivo in brain slices. Neurochem Int 18: 411–417CrossRefGoogle Scholar
  90. Schoepp DD, Johnson BG, Smith ECR, McQuaid LA (1990): Stereoselectivity and mode of inhibition of phosphoinositide-coupled excitatory amino acid receptors by 2-amino-3-phosphonopropionic acid. Mol Pharmacol 38: 222–228Google Scholar
  91. Schwarcz R, Coyle JT (1977): Neurochemical sequelae of kainate injections in corpus striatum and substantia nigra of the rat. Life Sci 20: 431–436CrossRefGoogle Scholar
  92. Sesma MA, Price MT, Olney JW (1991): Heat shock protein (HSP 72) response to NMDA antagonists is blocked by anticholinergics or GABA mimetics. Neurosci Abstr 17: 254Google Scholar
  93. Shapiro ML, Caramanos Z (1990): NMDA antagonist MK-801 impairs acquisition but not performance of spatial working and reference memory. Psychobiology 18: 231–243Google Scholar
  94. Sharp FR, Jasper P, Hall J, Noble L, Sagar SM (1991): MK-801 and ketamine induce heat shock protein HSP 72 in injured neurons in posterior cingulate and retrosplenial cortex. Ann Neurol 30: 801–809CrossRefGoogle Scholar
  95. Simon RP, Swan JH, Griffiths T, Meldrum BS (1984): Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science 226: 850–852CrossRefGoogle Scholar
  96. Sladeczek F, Pin JP, Recasens M, Bockaert J, Weiss S (1985): Glutamate stimulates inositol phosphate formation in striatal neurones. Nature (London) 317: 717–719CrossRefGoogle Scholar
  97. Sonsalla PK, Nicklas WJ, Heikkila RE (1989): Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity. Science 243: 398–400CrossRefGoogle Scholar
  98. Staubli U, Thibault O, DiLorenzo M, Lynch G (1989): Antagonism of NMDA receptors impairs acquisition but not retention of olfactory memory. Behav Neurosci 103: 54–60CrossRefGoogle Scholar
  99. Stevens JR (1992): Abnormal reinnervation as a basis for schizophrenia: A hypothesis. Arch Gen Psychiatry 49: 238–243CrossRefGoogle Scholar
  100. Stringer JL, Greenfield LJ, Hackett JT, Guyenet PG (1983): Blockade of long-term potentiation by phencyclidine and opiates in the hippocampus in vivo and in vitro. Brain Res 280: 127–138CrossRefGoogle Scholar
  101. Study RE, Barker JL (1981): Diazepam and pentobarbital: Fluctuation analysis reveals different mechanisms for potentiation of GABA responses in cultured central neurons. Proc Natl Acad Sci USA 78: 7180–7184CrossRefGoogle Scholar
  102. Sugiyama H, Ito I, Hirono C (1987): A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature (London) 3125: 531–533CrossRefGoogle Scholar
  103. Tizzano JP, Schoepp DD, Price MT, Olney JW (1991): Widespread degeneration induced in the developing rodent CNS by D,L-2-amino-3-phosphonopropionate (AP3). Soc Neurosci Abstr 17: 70Google Scholar
  104. Turski L, Bressler K, Rettig KJ, Loschmann PA, Wachtel H (1991): Protection of substantia nigra from MPP + neurotoxicity by N-methyl-D-aspartate antagonists. Nature (London) 349: 414–418CrossRefGoogle Scholar
  105. Watkins JC (1978): Excitatory amino acids. In: Kainic Acid as a Tool in Neurobiology, McGeer E, Olney JW, McGeer P, eds. New York: Raven Press, pp 37–69Google Scholar
  106. Watkins JC, Evans RH (1981): Excitatory amino acid transmitters. Annu Rev Pharmacol Toxicol 21: 165–204CrossRefGoogle Scholar
  107. Westbrook GL, Mayer ML (1987): Micromolar concentrations of Zn++ antagonize NMDA and GABA responses of hippocampal neurones. Nature (London) 328: 640CrossRefGoogle Scholar
  108. Wieloch T (1985): Hypoglycemia-induced neuronal damage prevented by an N-methyl-D-aspartate antagonist. Science 230: 681–683CrossRefGoogle Scholar
  109. Willets J, Balster RL, Leander JD (1990): The behavioral pharmacology of NMDA receptor antagonists. Trends Pharmacol Sci 11: 423–428CrossRefGoogle Scholar
  110. Wozniak DF, Olney JW, Kettinger L III, Price M, Miller JP (1990): Behavioral effects of MK-801 in the rat. Psychopharmacology 101: 47–56CrossRefGoogle Scholar
  111. Young AB, Penney JB, Cha J-H, Olson JMM, Greenamyre JT, Albin RL, Richfield E (1988): Neuronal and anatomical localization of excitatory amino acid receptor subtypes in vertebrate brain. In: Frontiers in Excitatory Amino Acid Research, Cavalheiro EA, Lehmann J, Turski L, eds. New York: Liss, pp 109–115Google Scholar

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© Springer Science+Business Media New York 1993

Authors and Affiliations

  • John W. Olney
  • Michael A. Sesma
  • David F. Wozniak

There are no affiliations available

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