Skip to main content
Log in

Selective vulnerability in the gerbil hippocampus: Morphological changes after 5-min ischemia and long survival times

  • Regular Papers
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

The morphology of the hippocampus of Mongolian gerbils was investigated by light and electron microscopy after 5-min forebrain ischemia and survival times of up to 10 months. After 3 weeks recirculation only 5.8% of pyramidal neurons of the CA1 (cornu ammonis 1) sector had survived but the thickness of the inner and outer hippocampal layers did not change. After recirculation times of 6 and 10 months the number of surviving neurons declined no further but all layers of the CA1 subfield shrank markedly. Ultrastructurally, many but not all surviving CA1 neurons were altered. After 3 weeks both “dark” and “pale” type neurons were present, while after 6 and 10 months only the “pale” type of injury persisted. Axonal enlargements and myelin breakdown were observed at all survival times up to 10 months of recirculation. The astrocytes of CA1 sector contained numerous glial fibrils which were most pronounced after the longer recirculation times. The stratum radiatum presented intact presynaptic terminals densely packed with an abundance of clear vesicles even after survival of 10 months. Initially, morphologically damaged postsynaptic structures were still attached to these terminals but they disappeared after longer recirculation times. However, even after 10 months some intact synapses were observed involving dendrites which probably originated from surviving CA1 neurons. In CA3 sector and dentate gyrus no ultrastructural changes occurred at any survival time. The close association of surviving CA1 neurons with intact presynaptic terminals and reactive glial cells may be of importance for the development of epileptogenic foci which are characteristic of this particular brain region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Benveniste H, Jorgensen MB, Diemer NH, Hansen AJ (1988) Calcium accumulation by glutamate receptor activation is involved in hippocampal cell damage after ischemia. Acta Neurol Scand 78:529–536

    Google Scholar 

  2. Bodsch W, Takahashi K (1985) Molecular events associated with protein synthesis inhibition in hippocampal neurons leading to neuronal death. J Cereb Blood Flow Metab [Suppl] 5:281–282

    Google Scholar 

  3. Brierley JB, Graham DI (1984) Hypoxia and vascular disorders of the central nervous system. In: Adams JH, Corsellis JAN, Duchen LW (eds) Greenfield's neuropathology, 4th edn. John Wiley & Sons, New York, pp 125–207

    Google Scholar 

  4. Cheung JY, Bonventre JV, Malis CD, Leaf A (1986) Calcium and ischemic injury. N Engl J Med 314:1670–1676

    Google Scholar 

  5. Ito U, Spatz M, Walker JT, Klatzo I (1975) Experimental cerebral ischemia in mongolian gerbils. I. Light microscopic observations. Acta Neuropathol (Berl) 32:209–223

    Google Scholar 

  6. Johansen FF, Jorgensen MB, Diemer NH (1983) Resistance of hippocampal CA-1 interneurons to 20-min transient cerebral ischemia in the rat. Acta Neuropathol (Berl) 61:135–140

    Google Scholar 

  7. Johansen FF, Jorgensen MB, von Lubitz DKJE, Diemer NH (1984) Selective dendrite damage in hippocampal CA1 stratum radiatum with unchanged axon ultrastructure and glutamate uptake after transient cerebral ischaemia in the rat. Brain Res 291:373–377

    Google Scholar 

  8. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239:57–69

    Google Scholar 

  9. Kirino T, Sano K (1984) Fine structural nature of delayed neuronal death following ischemia in the gerbil hippocampus. Acta Neuropathol (Berl) 62:209–218

    Google Scholar 

  10. Kirino T, Tamura A, Sano K (1986) A reversible type of neuronal injury following ischemia in the gerbil hippocampus. Storke 17:455–459

    Google Scholar 

  11. Kirino T, Tamura A, Sano K (1989) Persistent presynaptic terminals in the hippocampal CA1 sector following ischemic neuronal loss. J Cereb Blood Flow Metabo [Suppl 1] 9:554

    Google Scholar 

  12. Kitagawa K, Matsumoto M, Sobue K, Niinobe M, Isaka Y, Kimura K (1989) Differential vulnerability of pre- and postsynaptic sites of neurons in cerebral ischemia: microtubule-associated protein 2 and synapsin I as specific marker proteins. J Cereb Blood Flow Metab [Suppl 1] 9:4

    Google Scholar 

  13. Meldrum B, Evanos M, Griffiths T, Simon R (1985) Ischaemic brain damage: the role of excitatory activity and of calcium entry. Br J Anaesth 57:44–46

    Google Scholar 

  14. Nishikawa Y, Takahashi T, Shimada A (1989) Morphological studies on cerebral cortical lesions induced by transient ischemia in Mongolian gerbil — Diffuse and peripheral pallor of the neuronal perikarya. Acta Neuropathol 78:1–8

    Google Scholar 

  15. Paschen W, Hallmayer J, Mies G (1987) Regional profiles of polyamines in reversible cerebral ischemia in Mongolian gerbils. Neurochem Pathol 7:143–156

    Google Scholar 

  16. Petito CK, Pulsinelli WA (1984) Sequential development of reversible and irreversible neuronal damage following cerebral ischemia. J Neuropathol Exp Neurol 43:141–153

    Google Scholar 

  17. Petito CK, Feldmann E, Pulsinelli WA, Plum F (1987) Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 37:1281–1286

    Google Scholar 

  18. Pinard E, Rigand AS, Richie D, Naquet R, Seylaz J (1987) Continuous determination of the cerebrovascular changes induced by bicuculline and kainic acid in unanesthetized spontaneously breathing rats. Neurosciences 23:943–952

    Google Scholar 

  19. Plum F, Posner JB, Troy B (1968) Cerebral metabolic and circulatory responses to induced convulsions in animals. Arch Neurol 18:1–13

    Google Scholar 

  20. Pulsinelli WA, Brierley JB (1979) A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10:267–272

    Google Scholar 

  21. Scholz W (1951) Die Krampfschädigungen des Gehirns. Springer, Berlin, S1–114

    Google Scholar 

  22. Siesjö BK (1981) Cell damage in the brain: a speculative synthesis. J Cereb Blood Flow Metab 3:38–43

    Google Scholar 

  23. Siesjö BK (1988) Historical overview: calcium, ischemia, and death of brain cells. Ann NY Acad Sci 522:638–661

    Google Scholar 

  24. Thilmann R, Xie Y, Kleihues P, Kiessling M (1986) Persistent inhibition of protein synthesis precedes delayed neuronal cell death in postischemic gerbil hippocampus. Acta Neuropathol (Berl) 71:88–93

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bonnekoh, P., Barbier, A., Oschlies, U. et al. Selective vulnerability in the gerbil hippocampus: Morphological changes after 5-min ischemia and long survival times. Acta Neuropathol 80, 18–25 (1990). https://doi.org/10.1007/BF00294217

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00294217

Key words

Navigation