Abstract
Ischemic preconditioning (IPC) of the brain describes the neuroprotection induced by a short, conditioning ischemic episode (CIE) to a subsequent severe (test) ischemic episode (TIE). Most of the supporting evidence for IPC is based on histological assessment, several days after TIE. The aim of this study is to investigate if changes induced by IPC can be detected within 30 min of reperfusion following the ischemic episode. A rat model of “four‐vessel occlusion” transient global cerebral ischemia and parametric analysis of electrocorticogram were used. A control group was subjected directly to a 10 min TIE, and in a preconditioned group TIE was induced 48 h after a 3 min CIE. Quantitative histology was performed 48 h after TIE. Our key finding is that, 30 min after reperfusion, there is a significant increase in the electrocortical slow activity in the control group but not in the preconditioned group. Moreover the increase inversely correlates with the degree of electrocortical suppression during seconds 10 to 15 after the onset of the ischemic episode.
Keywords: cerebral ischemia, preconditioning, electrocorticogram, rat
References
- 1. Hossmann K.A., Experimental principles of tolerance of the brain to ischemia, Z. Kardiol, 76: 47–66, 1987. [PubMed] [Google Scholar]
- 2. Barone F.C., White R.F., Spera P.A., Ellison J., Currie R.W, Wang X., Feuerstein G.Z., Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin‐1 receptor antagonist and early gene expression, Stroke, 29: 1937–1950, 1998. [DOI] [PubMed] [Google Scholar]
- 3. Murry C.E., Jennings R.B., Reimer K.A., Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium, Circulation, 74: 1124–1136, 1986. [DOI] [PubMed] [Google Scholar]
- 4. Yellon D.M., Baxter G.F., A “second window of protection” or delayed preconditioning phenomenon: future horizons for myocardial protection?, J. Mol. Cell. Cardiol., 27: 1023–1034, 1995. [DOI] [PubMed] [Google Scholar]
- 5. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K., ‘Ischemic tolerance’ phenomenon found in the brain. Brain Res., 24: 21–24, 1990. [DOI] [PubMed] [Google Scholar]
- 6. Kitagawa K., Matsumoto M., Kuwabara K., Tagaya M., Ohtsuki T., Hata R., Ueda H., Handa N., Kimura K., Kamada T., ‘Ischemic tolerance’ phenomenon detected in various brain regions, Brain Res., 561: 203–211, 1991. [DOI] [PubMed] [Google Scholar]
- 7. Toyoda T., Kassell N.F., Lee K.S., Induction of ischemic tolerance and antioxidant activity by brief focal ischemia. Neuroreport, 8: 847–851, 1997. [DOI] [PubMed] [Google Scholar]
- 8. Stagliano N.E., Perez‐Pinzon M.A., Moskowitz M.A., Huang P.L., Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice, J. Cereb. Blood Flow Metab., 19: 757–761, 1999. [DOI] [PubMed] [Google Scholar]
- 9. Shamloo M., Wieloch T., Changes in protein tyrosine phosphorylation in the rat brain after cerebral ischemia in a model of ischemic tolerance, J. Cereb. Blood Flow Metab., 19: 173–183, 1999. [DOI] [PubMed] [Google Scholar]
- 10. Pringle A.K., Thomas S.J., Signorelli F., Iannotti F., Ischaemic pre‐conditioning in organotypic hippocampal slice cultures is inversely correlated to the induction of the 72 kDa heat shock protein (HSP72), Brain Res., 845: 152–164, 1999. [DOI] [PubMed] [Google Scholar]
- 11. Grabb M.C., Choi D.W., Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors, J. Neurosci., 19: 1657–1662, 1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Moncayo J., de Freitas G.R., Bogousslavsky J., Altieri M., van Melle G., Do transient ischemic attacks have a neuroprotective effect Neurology, 54: 2089–94, 2000. [DOI] [PubMed] [Google Scholar]
- 13. Leifer D., Kowall N.W., Imunohistochemical patterns of selective cellular vulnerability in human cerebral ischemia, J. Neurol. Sci., 119: 217–218, 1993. [DOI] [PubMed] [Google Scholar]
- 14. Smith M.L., Auer R.N., Siesjo B.K., The density and distribution of ischemic brain injury in the rat following 2–10 min of forebrain ischemia, Acta Neuropathol.(Berl.), 64: 319–332, 1984. [DOI] [PubMed] [Google Scholar]
- 15. Sinno K., Zhang L., Eubanks J.H., Carlen P.L., Wallace M.C., Transient ischemia induces an early decrease of synaptic transmission in CA1 neurons of rat hippocampus: electrophysiological study in brain slices, J. Cereb. Blood Flow Metab., 17: 955–966, 1997. [DOI] [PubMed] [Google Scholar]
- 16. Luhmann H.J., Mudrick‐Donnon L.A., Mittmann T., Heinemann U., Ischemia‐induced long‐term hyperexcitability in rat neocortex, Eur. J. Neurosci., 7: 180–191, 1995. [DOI] [PubMed] [Google Scholar]
- 17. Corsi‐Cabrera M, Juarez J, Ponce‐de‐Leon M., Ramos J., Velazquez P.N., EEG activity during estral cycle in the rat, Electroencephalogr. Clin. Neurophysiol., 83: 265–269, 1992. [DOI] [PubMed] [Google Scholar]
- 18. Sisson D.F., Sigel J., Chloral hydrate anesthesia: EEG power spectrum analysis and effects on VEPs in rat, Neurotoxicol. Teratol., 44: 61–71, 1998. [DOI] [PubMed] [Google Scholar]
- 19. Zagrean L., Vatasescu R., Oprica M., Nutiu O., Ferechide D., A comparative study of EEG suppressions induced by global cerebral ischemia and anoxia, Rom. J. Physiol., 32: 39–44, 1995. [PubMed] [Google Scholar]
- 20. Moldovan M., Munteanu A.M., Nita D.Al., Popa, D.P. , Spulber St., Zagrean, L. , Ischemic electrocortical suppression ‐ an active mechanism?, J. Med. Biochem., 4: 103–111, 2000. [Google Scholar]
- 21. Mann K., Backer P., Roschke J., Dynamical properties of the sleep EEG in different frequency bands, Int. J. Neurosci., 73: 161–169, 1993. [DOI] [PubMed] [Google Scholar]
- 22. Mabe H., Umemura S., Yoshida T., Iwayama K., Iwama M., Nagai H., Correlation between local cerebral blood flow and EEG in experimental cerebral ischemia, No To Shinkei, 34: 585–589, 1982. [PubMed] [Google Scholar]
- 23. Barzaghi F., Dragonetti M., Formento M.L., Boissier J.R., Cerebral energy metabolism and computerized EEG. Analysis following transient ischemia in the rat, J. Pharmacol., 13(4): 553–63, 1982. [PubMed] [Google Scholar]
- 24. Pulsinelli W.A., Buchan A.M., The four‐vessel occlusion rat model: method for complete occlusion of vertebral arteries and control of collateral circulation, Stroke, 19: 913–914, 1988. [DOI] [PubMed] [Google Scholar]
- 25. Sainio K., Stenberg D., Keskimaki I., Muuronen A., Kaste M., Visual and spectral EEG analysis in the evaluation of the outcome in patients with ischemic brain infarction, Electroencephalogr. Clin. Neurophysiol., 56: 117–124, 1983. [DOI] [PubMed] [Google Scholar]
- 26. Perez‐Pinzon M.A., Xu G.P., Dietrich W.D., Rosenthal M., Sick, T.J. , Rapid preconditioning protects rats against ischemic neuronal damage after 3 but not 7 days of reperfusion following global cerebral ischemia, J. Cereb. Blood Flow Metab., 17: 175–182, 1997. [DOI] [PubMed] [Google Scholar]
- 27. Kato H., Liu Y., Araki T., Kogure K., Temporal profile of the effects of pretreatment with brief cerebral ischemia on the neuronal damage following secondary ischemic insult in the gerbil: cumulative damage and protective effects, Brain Res., 553: 238–242, 1991. [DOI] [PubMed] [Google Scholar]
- 28. Tomida S., Nowak, T.S. Jr. , Vass, K. , Lohr, J.M. , Klatzo, I. , Experimental model for repetitive ischemic attacks in the gerbil: the cumulative effect of repeated ischemic insults, J. Cereb. Blood Flow Metab., 7: 773–782, 1987. [DOI] [PubMed] [Google Scholar]
- 29. Hara A., Yoshimi N., Hirose Y., Ino N., Tanaka H., Mori H., DNA fragmentation in granullar cells of human cerebellum following global ischaemia, Brain Res., 697: 247–250, 1995. [DOI] [PubMed] [Google Scholar]
- 30. Iwai T., Hara A., Niwa M., Nsozaki M., Uematsu T., Sakai N., Temporal profile of nuclear DNA fragmentation in situ in gerbil hippocampus following transient forebrain ischaemia, Brain Res., 671, 305–308, 1995. [DOI] [PubMed] [Google Scholar]