Selective Neuronal Cell Death after Transient Forebrain Ischemia in the Mongolian Gerbil

  • Barbara J. Crain
  • J. Victor Nadler
Part of the Advances in Behavioral Biology book series (ABBI, volume 35)

Summary

An important feature of ischemic brain damage is the exceptional vulnerability of specific cell types. In the Mongolian gerbil, silver impregnation revealed that four brain regions are exceptionally vulnerable to 5 min of complete forebrain ischemia: (1) hippocampal areas CA1, CA2–CA3a and CA4; (2) the dorsolateral striatum; (3) the somatosensory neocortex; and (4) the dorsomedial portion of the lateral septal nucleus. The ischemic lesion evolved with time in all four regions, but at different rates. The development of argyrophilia was delayed for the longest time in hippocampal area CAlb (maximal in 3 d) and for the shortest time in hippocampal area CA4 and the striatum (maximal in 24 h or less). The mechanism for delayed neuronal death in area CAlb has been suggested to involve the activation of excitatory afferent pathways. Indeed an ipsilateral entorhinal cortical lesion partially protected CA1b pyramidal cells from ischemic cell death. However, the entorhinal cortical lesion had no protective effect in other hippocampal regions. This result suggests either that synaptic excitation is crucial for only the most delayed form of ischemic cell death or that the medial temporo-ammonic tract, and not the perforant path, is involved in the damage to area CAlb.

Keywords

Ischemia Carbon Monoxide NMDA Statin Halothane 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amaral, D.G., 1978, A Golgi study of cell types in the hilar region of the hippocampus in the rat, J. Comp. Neurol., 182:851.CrossRefGoogle Scholar
  2. Bakst, I., Avendano, C., Morrison, J.H., and Amaral, D.G., 1986, An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat, J. Neurosci., 6:1452.Google Scholar
  3. Blomqvist, P. and Wieloch, T., 1985, Ischemic brain damage in rats following cardiac arrest using a long-term recovery model, J. Cereb. Blood Flow Metab., 5:420.CrossRefGoogle Scholar
  4. Brierley, J.B., and Graham, D.I., 1984, Hypoxia and vascular disorders of the central nervous system, in: “Greenfield’s Neuropathology, 4th edition,” J.H. Adams, J.A.N. Corsellis, and L.W. Duchen, eds., Edward Arnold, London, p. 125.Google Scholar
  5. Donoghue, J.P., and Kitai, S.T., 1981, A collateral pathway to the neo-striatum from corticofugal neurons of the rat sensory-motor cortex: an intracellular HRP study, J. Comp. Neurol., 201:1.CrossRefGoogle Scholar
  6. Fält, M., Harris, E., Cotman, C., and Wieloch, T., 1986, Time course of recovery and disappearance of synaptic transmission in hippocampus following cerebral ischemia, Soc. Neurosci. Abstr., 12:868.Google Scholar
  7. Foster, A.C., Gill, R., Iversen, L.L., and Woodruff, G.N., 1987, Systemic administration of MK-801 protects against ischaemia-induced hippocampal neurodegeneration in the gerbil, Brit. J. Pharmacol., 90:9P.Google Scholar
  8. Gerhardt, S.C., Bernard, P., Pastor, G., and Boast, C.A., 1986, Effects of systemic administration of the NMDA antagonist, CPP, on ischemic brain damage in gerbils, Soc. Neurosci. Abstr., 12:59.Google Scholar
  9. Ito, U., Spatz, M., Walker, J.T., and Klatzo, I., 1975, Experimental cerebral ischemia in Mongolian gerbils. I. Light microscopic observations, Acta Neuropathol. (Berl.) 32:209.CrossRefGoogle Scholar
  10. Johansen, F.F., Jjrgensen, M.B., and Diemer, N.H., 1987a, Ischemia induced delayed neuronal death in the CA-1 hippocampus is dependent on intact glutamatergic innervation, in: “Excitatory Amino Acid Transmission, Neurology and Neurobiology Vol. 24,” T.P. Hicks, D. Lodge, and McLennan, H., eds., Alan R. Liss, New York, p. 245.Google Scholar
  11. Johansen, F.F., Zimmer, J., and Diemer, N.H., 1987b, Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA-1 pyramidal cell loss, Acta Neuropathol. (Berl.) 73:110.CrossRefGoogle Scholar
  12. Jorgensen, M.B., Johansen, F.F., and Diemer, N.H., 1987, Removal of the entorhinal cortex protects hippocampal CA-1 neurons from ischemic damage, Acta Neuropathol. (Berl.) 73:189.CrossRefGoogle Scholar
  13. Kirino, T., 1982, Delayed neuronal death in the gerbil hippocampus following ischemia, Brain Res., 239:57.CrossRefGoogle Scholar
  14. Kirino, T., and Sano, K., 1984a, Selective vulnerability in the gerbil hippocampus following transient ischemia, Acta Neuropathol. (Berl.) 62:201.CrossRefGoogle Scholar
  15. Kirino, T., and Sano, K., 1984b, Fine structural nature of delayed neuronal death following ischemia in the gerbil hippocampus, Acta Neuropathol. (Berl.) 62:209.CrossRefGoogle Scholar
  16. Kirino, T., Tamura, A., and Sano, K., 1984, Delayed neuronal death in the rat hippocampus following transient forebrain ischemia, Acta Neuropathol. (Berl.) 64:139.CrossRefGoogle Scholar
  17. Levine, S., and Sohn, D., 1969, Cerebral ischemia in infant and adult gerbils. Relation to incomplete circle of Willis, Arch. Pathol., 87:315.Google Scholar
  18. Levy, D.E., and Brierley, J.B., 1974, Communication between vertebro-basilar and carotid arterial circulations in the gerbil, Exp. Neurol., 45:503.CrossRefGoogle Scholar
  19. Levy, D.E., Brierley, J.B., and Plum, F., 1975, Ischaemic brain damage in the gerbil in the absence of “no-reflow”, J. Neurol. Neurosurg. Psychiat., 38:1197.CrossRefGoogle Scholar
  20. MacDermott, A.B., Mayer, 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.CrossRefGoogle Scholar
  21. Mouritzen Dam, A., Bajorek, J.C., and Lomax, P., 1981, Hippocampal neuron density and seizures in the Mongolian gerbil, Epilepsia 22:667.Google Scholar
  22. Monaghan, D.T., and Cotman, C.W., 1985, Distribution of N-methyl-Daspartate-sensitive L-[3H]glutamate-binding sites in rat brain, J. Neurosci., 5:2909.Google Scholar
  23. Nadler, J.V., and Evenson, D.A., 1983, Use of excitatory amino acids to make axon-sparing lesions of hypothalamus, in: “Hormone Action, Part H: Neuroendocrine Peptides, Methods in Enzymology, Vol. 103,” P.M. Conn, ed., Academic Press, New York, p. 393.CrossRefGoogle Scholar
  24. Onodera, H., Sato, G., and Kogure, K., 1986, Lesions to Schaffer collaterals prevent ischemic death of CA1 pyramidal cells, Neurosci. Lett., 68:169.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Rothman, S., 1984, Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death, J. Neurosci., 4:1884.Google Scholar
  27. Rothman, S.M., and Olney, J.W., 1986, Glutamate and the pathophysiology of hypoxic-ischemia brain damage, Ann. Neurol., 19:105.CrossRefGoogle Scholar
  28. Sakamoto, N., Kogure, K., Kato, H., and Ohtomo, H., 1986, Disturbed Ca2+ homeostasis in the gerbil hippocampus following brief transient ischemia, Brain Res., 364:372.CrossRefGoogle Scholar
  29. Simon, R.P., Griffiths, T., Evans, M.C., Swan, J.H., and Meldrum, B.S., 1984a, Calcium overload in selectively vulnerable neurons of the hippo-campus during and after ischemia: an electron microscopy study in the rat, J. Cereb. Blood Flow Metab., 4:350.CrossRefGoogle Scholar
  30. Simon, R.P., Swan, J.H., Griffiths, T., and Meldrum, B.S., 1984b, Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain, Science 226:850.CrossRefGoogle Scholar
  31. Sloviter, R.S., 1987, Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy, Science 235:73.CrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. Spielmeyer, W., 1925, Zur Pathogenese der örtlich elektiver Gehirnveränderungen, Z. Ges. Neurol. Psychiat., 99:756.CrossRefGoogle Scholar
  34. Spielmeyer, W., 1929, Über örtliche Vulnerabilität, Z. Ges. Neurol. Psychiat. 118:1.CrossRefGoogle Scholar
  35. Steward, O., 1976, Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat, J. Comp. Neurol., 167:285.CrossRefGoogle Scholar
  36. Steward, O., and Scoville, S.A., 1976, Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat, J. Comp. Neurol., 169:347.CrossRefGoogle Scholar
  37. Suzuki, R., Yamaguchi, T., Li, C.-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. (Berl.) 60:217.CrossRefGoogle Scholar
  38. Swanson, L.W., and Cowan, W.M., 1977, An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat, J. Comp. Neurol., 172:49.CrossRefGoogle Scholar
  39. Vicedomini, J.P., and Nadler, J.V., 1987, A model of status epilepticus based on electrical stimulation of hippocampal afferent pathways, Exp. Neurol., 96:681.CrossRefGoogle Scholar
  40. Webster, K.E., 1961, Cortico-striate interrelations in the albino rat, J. Anat., 95:532.Google Scholar
  41. Wieloch, T., Lindvall, O., Blomqvist, P., and Gage, F.H., 1985, Evidence for amelioration of ischaemic neuronal damage in the hippocampal formation by lesions of the perforant path, Neurol. Res., 7:24.Google Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Barbara J. Crain
    • 1
    • 2
  • J. Victor Nadler
    • 3
  1. 1.Departments of PathologyDuke University Medical CenterDurhamUSA
  2. 2.Departments of AnatomyDuke University Medical CenterDurhamUSA
  3. 3.Departments of PharmacologyDuke University Medical CenterDurhamUSA

Personalised recommendations