Skip to main content
SpringerLink
Log in

Poor correlation between delayed neuronal death induced by transient forebrain ischemia, and immunoreactivity for parvalbumin and calbindin D-28k in developing gerbil hippocampus

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

Abstract

In the normal developing hippocampus of the gerbil, parvalbumin-immunoreactive neurons first appear in the stratum pyramidale of CA3 at postnatal day 15 (P15), and in CA2 and hilus of the dentate gyrus from P21 onwards. Immunoreactive terminals also follow the same sequence from CA3 to CA1 to reach adult patterns by the end of the 1st month. Calbindin D-28k immunoreactivity is seen in the external part of the upper blade of the dentate gyrus at P5, and progresses to the granule cell and molecular layers of the whole gyrus by P15, except for a thin band of immature cells located at the base of the granule cell layer which are calbindin negative. Calbindin immunoreactivity in mossy fibers progresses from the external to the hilar region of CA3 during the same period. A few immunoreactive cells are also found in the stratum radiatum/lacunare of the CA3, but no calbindin-immunoreactive cells are observed in the CA1 and CA2 subfields. The adult pattern of calbindin immunoreactivity is reached at P21. Vulnerability following transient forebrain ischemia for 20 min was examined in the hippocampal formation of gerbils during postnatal development. No cellular damage was seen in animals aged 7 days. Dying cells were observed at the base of the granule cell layer of the dentate gyrus in animals aged 15, 21 and 30 days. Pyramidal cells in the CA3 subfield were also sensitive to ischemia in gerbils aged 15 days, and less frequently in animals aged 21 days. The adult pattern of cellular damage, characterized by selective vulnerability of the CA1 subfield, was seen from day 30 onwards. These findings show that the pattern of selective vulnerability following transient forebrain ischemia is different in young and adult gerbils, and suggest that little, if any, correlation exists between resistance to delayed cellular damage and parvalbumin and calbindin D-28k content in the hippocampus of young gerbils.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Alcántara S, Ferrer I, Soriano E (1993) Postnatal development of parvalbumin and calbindin D-28k immunoreactivities in the cerebral cortex of the rat. Anat Embryol 188: 63–73

    Google Scholar 

  2. Araki T, Kato H, Kogure K (1990) Neuronal damage and calcium accumulation following repeated brief cerebral ischemia in the gerbil. Brain Res 528: 114–122

    Google Scholar 

  3. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15: 303–308

    Google Scholar 

  4. Bergmann I, Nitsch R, Frotscher M (1991) Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anat Embryol 184: 403–409

    Google Scholar 

  5. Bonnekoh P, Kuroiwa T, Kloiber O, Hossmann K (1992) Time profile of calcium accumulation in hippocampus, striatum and frontoparietal cortex after transient forebrain ischemia in the gerbil. Acta Neuropathol 84: 400–406

    Google Scholar 

  6. Busto R, Dietrich W, Globus MYT, Ginsberg MD (1989) Postischemic moderate hypothermia inhibits CA1 hippocampal ischemic neuronal injury. Neurosci Lett 101: 299–304

    Google Scholar 

  7. Celio MR (1990) Calbindin D-28K and parvalbumin in the rat nervous system. Neuroscience 35: 375–475

    Google Scholar 

  8. Enderlin S, Norman AW, Celio MR (1987) Ontogeny of the calcium binding protein calbindin D-28K in the rat nervous system. Anat Embryol 177: 15–28

    Google Scholar 

  9. Freund TF, Buzsáki G, Leon A, Baimbridge KG, Somogyi P. (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp Brain Res 83: 55–66

    Google Scholar 

  10. Freund TF, Ylinen A, Miettinen R, Pitkänen A, Lathinen H, Baimbridge KG, Riekkinen PJ (1991) Patterns of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res Bull 28: 27–38

    Google Scholar 

  11. Goodman JH, Wasterlain CG, Massarweh WF, Evelyn D, Sollas AL, Sloviter RS (1993) Calbindin-D28k immunoreactivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat. Brain Res 606: 309–314

    Google Scholar 

  12. Green EJ, Dietrich WD, van Dijk F, Busto R, Markgraf CG, McCabe PM, Ginsberg MD, Schneiderman N (1992) Protective effects of brain hypothermia on behavior and histopathology following global cerebral ischemia in rats. Brain Res 589: 197–204

    Google Scholar 

  13. Hara H, Sukamoto T, Kogure K (1993) Mechanisms and pathogenesis of ischemia-induced neuronal damage. Prog Neurobiol 40: 645–670

    Google Scholar 

  14. Hashimoto K, Kikuchi H, Ishikawa M, Kobayashi S (1992) Changes in cerebral energy metabolism and calcium levels in relation to delayed neuronal death after ischemia. Neurosci Lett 137: 165–168

    Google Scholar 

  15. 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 

  16. Johansen FF, Jorgensen MB, Diemer NH (1983) Resistance of hippocampal CA1 interneurons to 20 minutes of transient cerebral ischemia in the rat. Acta Neuropathol (Berl) 61: 135–140

    Google Scholar 

  17. Johansen FF, Tonder N, Zimmer J, Baimbridge KG, Diemer NH (1990) Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia. Neurosci Lett 120: 171–174

    Google Scholar 

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

    Google Scholar 

  19. Kirino T, Sano K (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol (Berl) 62: 201–208

    Google Scholar 

  20. Kirino T, Tamura A, Sano K (1984) Delayed neuronal death in the rat hippocampus following transient forebrain ischemia. Acta Neuropathol (Berl) 64: 139–147

    Google Scholar 

  21. Lang U, Frotscher M (1990) Postnatal development of nonpyramidal neurons in the rat hippocampus (areas CA1 and CA3): a combined Golgi-electron microscope study. Anat Embryol 181: 533–545

    Google Scholar 

  22. Levine S, Sohn D (1969) Cerebral ischemia in infant and adult gerbils. Arch Pathol 87: 315–317

    Google Scholar 

  23. Nitsch C (1992) Reorganization in the gerbil hippocampus after ischemia-induced delayed neuronal death: fate of parvalbumin-containing neurons. In: Ito U, Kirino T, Kuroiwa T, Klatzo I (eds) Maturation phenomenon in cerebral ischemia, Springer-Verlag, New York Berlin Heidelberg, pp 23–31

    Google Scholar 

  24. Nitsch C, Goping C, Klatzo I (1989) Preservation of GA-BAergic perikarya and boutons after transient ischemia in the gerbil hippocampal CA1 field. Brain Res 495: 243–252

    Google Scholar 

  25. Nitsch C, Scotti AL, Sommacal A, Kalt G (1989) GABAergic hippocampal neurons resistant to ischaemia induced delayed neuronal death contain the calcium-binding protein parvalbumin. Neurosci Lett 105: 263–268

    Google Scholar 

  26. Payan HM, Conar JR (1977) Carotid ligation in gerbils. Influence of age, sex and gonads. Stroke 8: 194–196

    Google Scholar 

  27. Petito CK, Pulsinelli WA (1984) Delayed neuronal recovery and neuronal death in rat hippocampus following severe cerebral ischemia: possible relationship to abnormalities in neuronal processes. J Cereb Blood Flow Metab 4: 194–205

    Google Scholar 

  28. 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 

  29. Rice JE, Vannucci RC, Brierley JB (1981) The influence of immaturity on hypoxic-ischemic brain damage. Ann Neurol 9: 131–141

    Google Scholar 

  30. Schmidt-Kastner R, Freund TF (1991) Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40: 599–636

    Google Scholar 

  31. Schwartz PH, Massarwech WF, Vinters HV, Wasterlain CG (1992) A rat model of severe neonatal hypoxic-ischemic brain injury. Stroke 23: 359–546

    Google Scholar 

  32. Scotti AL, Nitsch C (1991) The perforant path in the seizure sensitive gerbil contains the CA2+ binding protein parvalbumin. Exp Brain Res 85: 137–143

    Google Scholar 

  33. Seto-Oshima A, Aoki E, Semba R, Emson PC, Heizmann CW (1990) Appearance of parvalbumin-specific immunoreactivity in the cerebral cortex and hippocampus of the developing rat and gerbil brain. Histochemistry 94: 579–589

    Google Scholar 

  34. Sloviter RS, Sollas AL, Barbaro NM, Laxer KD (1991) Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308: 381–396

    Google Scholar 

  35. Swann JW, Brady RJ, Martin DL (1989) Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28: 551–577

    Google Scholar 

  36. Tortosa A, Ferrer I (1993) Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischaemia: a qualitative and quantitative sequential study. Neuroscience 55: 33–43

    Google Scholar 

  37. Towfighi J, Yager JY, Housman C, Vannucci RC (1991) Neuropathology of remote hypoxic-ischemic damage in the immature rat. Acta Neuropathol 81: 578–587

    Google Scholar 

  38. Tsubokawa H, Oguro K, Robinson HPC, Masuzawa T, Kirino T, Kawai N (1992) Abnormal Ca2+ homeostasis before cell death revealed by whole cell recording of ischemic CA1 hippocampal neurons. Neuroscience 49: 807–817

    Google Scholar 

  39. Welsh FA, Harris VA (1991) Postischemic hypothermia fails to reduce ischemic injury in gerbil hippocampus. J Cereb Blood Flow Metab 11: 617–620

    Google Scholar 

  40. Welsh FA, Sims RE, Harris VA (1990) Mild hypothermia prevents ischemic injury in gerbil hippocampus. J Cereb Blood Flow Metab 10: 557–563

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unidad Neuropatología, Servicio Anatomía Patológica, Hospital Príncipes de España, Universidad de Barcelona, Hospitalet de Llobregat, E-08907, Spain

    A. Tortosa & I. Ferrer

Authors
  1. A. Tortosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. Ferrer
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Supported in part by grant FIS 93-131 and a grant from the Fundacio Pi i Synyer (to A.T.)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tortosa, A., Ferrer, I. Poor correlation between delayed neuronal death induced by transient forebrain ischemia, and immunoreactivity for parvalbumin and calbindin D-28k in developing gerbil hippocampus. Acta Neuropathol 88, 67–74 (1994). https://doi.org/10.1007/BF00294361

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00294361

Key words

Search

Navigation