Adenosine preconditions against ouabain but not against glutamate on CA1-evoked potentials in rat hippocampal slices

European Journal of Neuroscience

Volumn 28, Issue 10, 2008, Pages 2084-2098

  Ferguson, Alexandra L ^a   Stone, Trevor W ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Adenosine; Glutamate; Ischaemia; Ouabain; Preconditioning

Indexed keywords

5 HYDROXYDECANOIC ACID; ADENOSINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; AMPA RECEPTOR; GLIBENCLAMIDE; GLUTAMIC ACID; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NITRIC OXIDE SYNTHASE INHIBITOR; OUABAIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; BRAIN ISCHEMIA; BRAIN SLICE; CELL DAMAGE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ENZYME ACTIVITY; EVOKED RESPONSE; EXCITOTOXICITY; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY;

ADENOSINE; ANIMALS; BRAIN ISCHEMIA; ENZYME INHIBITORS; EVOKED POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; ISCHEMIC PRECONDITIONING; MALE; NITRIC OXIDE SYNTHASE TYPE I; ORGAN CULTURE TECHNIQUES; OUABAIN; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 55949132874     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06490.x     Document Type: Article

References (102)

1. Alger, B.E. Williamson, A. (1988) A transient calcium-dependent potassium component of the epileptiform burst after-hyperpolarization in rat hippocampus. J. Physiol. (Lond.), 399, 191 205.
2. Alici, K., Gloveli, T., Weber-Luxenburger, G., Motine, V. Heinemann, U. (1996) Comparison of effects induced by toxic applications of kainate and glutamate by glucose deprivation on area CA1 of rat hippocampal slices. Brain Res., 738, 109 120.
3. Atochin, D.N., Clark, J., Demchenko, I.T., Moskowitz, M.A. Huang, P.L. (2003) Rapid cerebral ischemic preconditioning in mice deficient in endothelial and neuronal nitric oxide synthases. Stroke, 34, 1299 1303.
4. +)ATPase with ouabain induces spreading depression-like depolarization in hippocampal slices. Brain Res., 838, 37 44.
5. Ballard-Croft, C., Kristo, G., Yoshimura, Y., Reid, E., Keith, B.J., Mentzer, R.M. Lasley, R.D. (2005) Acute adenosine preconditioning is mediated by p38 MAPK activation in discrete subcellular compartments. Am. J. Physiol. Heart Circ. Physiol., 288, H1359 H1366.
6. Bandyopadhyay, A., Johnson, L., Chung, W. Thakor, N.V. (2002) Protection by rapid chemical preconditioning of stressed hippocampal slice: a study of cellular swelling using optical scatter imaging. Brain Res., 945, 79 87.
7. Basarsky, T.A., Feighan, D. MacVicar, B.A. (1999) Glutamate release through volume-activated channels during spreading depression. J. Neurosci., 19, 6439 6445.
8. Behan, W.M. Stone, T.W. (2002) Enhanced neuronal damage by co-administration of quinolinic acid and free radicals, and protection by adenosine A2A receptor antagonists. Br. J. Pharmacol., 135, 1435 1442.
9. Bickler, P.E. Fahlman, C.S. (2004) Moderate increases in intracellular calcium activate neuroprotective signals in hippocampal neurons. Neuroscience, 127, 673 683.
10. Blondeau, N., Plamondon, H., Richelme, C., Heurteaux, C. Lazdunski, M. (2000) K(ATP) channel openers, adenosine agonists and epileptic preconditioning are stress signals inducing hippocampal neuroprotection. Neuroscience, 100, 465 474.
11. Bond, A., Lodge, D., Hicks, C.A., Ward, M.A. O'Neill, M.J. (1999) NMDA receptor antagonism, but not AMPA receptor antagonism attenuates induced ischaemic tolerance in the gerbil hippocampus. Eur. J. Pharmacol., 380, 91 99.
12. Centeno, J.M., Orti, M., Salom, J.B., Sick, T.J. Perez-Pinzon, M.A. (1999) Nitric oxide is involved in anoxic preconditioning neuroprotection in rat hippocampal slices. Brain Res., 836, 62 69.
13. +-ATPase activity and mitochondrial functions. Basic Clin. Pharmacol. Toxicol., 101, 108 116.
14. Chiueh, C.C., Andoh, T. Chock, P.B. (2005) Roles of thioredoxin in nitric oxide-dependent preconditioning-induced tolerance against MPTP neurotoxin. Toxicol. Appl. Pharmacol., 207, 96 102.
15. Chuang, D.M., Gao, X.M. Paul, S.M. (1992) N-methyl-d-aspartate exposure blocks glutamate toxicity in cultured cerebellar granule cells. Mol. Pharmacol., 42, 210 216.
16. Cohen, M.V., Baines, C.P. Downey, J.M. (2000) Ischemic preconditioning: from adenosine receptor to K-ATP channel. Ann. Rev. Physiol., 62, 79 109.
17. Connick, J.H. Stone, T.W. (1989) Quinolinic acid neurotoxicity: protection by intracerebral phenylisopropyladenosine (PIA) and potentiation by hypotension. Neurosci. Lett., 101, 191 196.
18. Coulter, D.A., Sombati, S. DeLorenzo, R.J. (1992) Electrophysiology of glutamate neurotoxicity in vitro: induction of a calcium-dependent extended neuronal depolarization. J. Neurophysiol., 68, 362 373.
19. Cousin, M.A., Nicholls, D.G. Pocock, J.M. (1995) Modulation of ion gradients and glutamate release in cultured cerebellar granule cells by ouabain. J. Neurochem., 64, 2097 2104.
20. Cunha, G.M., Canas, P.M., Melo, C.S., Hockemeyer, J., Muller, C.E., Oliveira, C.R. Cunha, R.A. (2008) Adenosine A2A receptor blockade prevents memory dysfunction caused by beta-amyloid peptides but not by scopolamine or MK-801. Exp. Neurol., 210, 776 781.
21. Dall'Igna, O.P., Porciuncula, L.O., Souza, D.O., Cunha, R.A. Lara, D.R. (2003) Neuroprotection by caffeine and adenosine A2A receptor blockade of beta-amyloid neurotoxicity. Br. J. Pharmacol., 138, 1207 1209.
22. Dall'Igna, O.P., Fett, P., Gomes, M.W., Souza, D.O., Cunha, R.A. Lara, D.R. (2007) Caffeine and adenosine A(2a) receptor antagonists prevent beta-amyloid (25-35)-induced cognitive deficits in mice. Exp. Neurol., 203, 241 245.
23. Dave, K.R., Lange-Asschenfeldt, C., Raval, A.P., Prado, R., Busto, R., Saul, I. Perez-Pinzon, M.A. (2005) Ischemic preconditioning ameliorates excitotoxicity by shifting glutamate/gamma-aminobutyric acid release and biosynthesis. J. Neurosci. Res., 82, 665 673.
24. De Mendonca, A., Sebastiao, A.M. Ribeiro, J.A. (1995) Inhibition of NMDA receptor-mediated currents in isolated rat hippocampal-neurons by adenosine A(1) receptor activation. Neuroreport, 6, 1097 1100.
25. 2+ loading in dendrites and somata of CA1 neurons in acute slice. Hippocampus, 17, 1049 1059.
26. El-Mallakh, R.S., Schurr, A., Payne, R.S. Li, R. (2000) Ouabain induction of cycling of multiple spike responses in hippocampal slices is delayed by lithium. J. Psychiatr. Res., 34, 115 120.
27. Elmoselhi, A.B., Lukas, A., Ostadal, P. Dhalla, N.S. (2003) Preconditioning attenuates ischemia-reperfusion-induced remodeling of Na+-K+-ATPase in hearts. Amer. J. Physiol.- Heart Circ. Physiol., 285, H1055 H1063.
28. Feng, J., Sellke, M.E., Ramlawi, B., Boodhwani, M., Clements, R., Li, J., Bianchi, C. Sellke, F.W. (2006) Bradykinin induces microvascular preconditioning through the opening of calcium-activated potassium channels. Surgery, 140, 192 197.
29. +-ATPase activity in brain. Europ. J. Pharmacol., 292, 287 292.
30. Gerevich, Z., Wirkner, K. Illes, P. (2002) Adenosine A2A receptors inhibit the N-methyl-d-aspartate component of excitatory synaptic currents in rat striatal neurons. Eur. J. Pharmacol., 451, 161 164.
31. Gidday, J.M., Shah, A.R., Maceren, R.G., Wang, Q., Pelligrino, D.A., Holtzman, D.M. Park, T.S. (1999) Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J. Cereb. Blood Flow Metab., 19, 331 340.
32. Golden, W.C. Martin, L.J. (2006) Low-dose ouabain protects against excitotoxic apoptosis and up-regulates nuclear Bcl-2 in vivo. Neuroscience, 137, 133 144.
33. Grabb, M.C. Choi, D.W. (1999) Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J. Neurosci., 19, 1657 1662.
34. + channels in cerebral ischemic preconditioning. Proc. Natl Acad. Sci. USA, 92, 4666 4670.
35. Hiraide, T., Katsura, K., Muramatsu, H., Asano, G. Katayama, Y. (2001) Adenosine receptor antagonists cancelled the ischemic tolerance phenomenon in gerbil. Brain Res., 910, 94 98.
36. Hosseinzadeh, H. Stone, T.W. (1998) Tolbutamide blocks postsynaptic but not presynaptic effects of adenosine on hippocampal CA1 neurones. J. Neural Transm., 105, 161 172.
37. +-ATPase activity during early reperfusion contributes to cell death after myocardial ischemia. Circ. Res., 97, 465 473.
38. Jones, P.A., Smith, R.A. Stone, T.W. (1998) Protection against hippocampal kainate excitotoxicity by intracerebral administration of an adenosine A2A receptor antagonist. Brain Res., 800, 328 335.
39. Kato, H.L.Y., Araki, T. Kogure, K. (1991) 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.
40. Kato, H., Liu, Y., Araki, T. Kogure, K. (1992) MK-801, but not anisomycin, inhibits the induction of tolerance to ischemia in the gerbil hippocampus. Neurosci. Lett., 139, 118 121.
41. Kitagawa, K., Matsumoto, M., Tagaya, M., Hata, R., Ueda, H., Niinobe, M., Handa, N., Fukunaga, R., Kimura, K., Mikoshiba, K. Kimada, T. (1990) 'Ischemic tolerance' phenomenon found in the brain. Brain Res., 528, 21 24.
42. Kitagawa, H., Mori, A., Shimada, J., Mitsumoto, Y. Kikuchi, T. (2002) Intracerebral adenosine infusion improves neurological outcome after transient focal ischemia in rats. Neurol. Res., 24, 317 323.
43. + ATPase (alpha 1 subunit) immunoreactivity in the gerbil hippocampus after transient forebrain ischemia. Brain Res., 987, 233 239.
44. Lange-Asschenfeldt, C., Raval, A.P. Perez-Pinzon, M.A. (2005) Ischemic tolerance induction in organotypic hippocampal slices: role for the GABA(A) receptor? Neurosci. Lett., 384, 87 92.
45. Lankford, A.R., Yang, J.N., Rose'Meyer, R., French, B.A., Matherne, G.P., Fredholm, B.B. Yang, Z.Q. (2006) Effect of modulating cardiac A(1) adenosine receptor expression on protection with ischemic preconditioning. Am. J. Physiol. Heart Circ. Physiol., 290, H1469 H1473.
46. Latini, S., Bordoni, F., Pedata, F. Corradetti, R. (1999) Extracellular adenosine concentrations during in vitro ischaemia in rat hippocampal slices. Br. J. Pharmacol., 127, 729 739.
47. Lau, Y.S. Mouradian, M.M. (1993) Protection against acute MPTP-induced dopamine depletion in mice by adenosine A1 agonist. J. Neurochem., 60, 768 771.
48. Li, H. Henry, J.L. (1992) Adenosine-induced hyperpolarization is depressed by glibenclamide in rat CA1 neurones. Neuroreport, 3, 1113 1116.
49. Li, S. Stys, P.K. (2001) Na(+)-K(+)-ATPase inhibition and depolarization induce glutamate release via reverse Na(+)-dependent transport in spinal cord white matter. Neuroscience, 107, 675 683.
50. Li, F.Z., Kimura, S., Nishiyama, A., Rahman, M., Zhang, G.X. Abe, Y. (2005) Ischemic preconditioning protects post-ischemic renal function in anesthetized dogs: role of adenosine and adenine nucleotides. Acta Pharmacol. Sin., 26, 851 859.
51. Li, J., Zelenin, S., Aperia, A. Aizman, O. (2006) Low doses of ouabain protect from serum deprivation-triggered apoptosis and stimulate kidney cell proliferation via activation of NF-kappaB. J. Am. Soc. Nephrol., 17, 1848 1857.
52. Lichstein, D., Mullikinkilpatrick, D. Blume, A.J. (1982) Hyperpolarization of neuro-blastoma glioma hybrid NG108-15 by vanadium ions. Proc. Natl Acad. Sci. USA, 79, 4202 4206.
53. Liem, D.A., Hekkert, M.T.L., Manintveld, O.C., Boomsma, F., Verdouw, P.D. Duncker, D.J. (2005) Myocardium tolerant to an adenosine-dependent ischemic preconditioning stimulus can still be protected by stimuli that employ alternative signaling pathways. Am. J. Physiol. Heart Circ. Physiol., 288, H1165 H1172.
54. Liu, G.S., Thornton, J., Van Winkle, D.M., Stanley, A.W., Olsson, R.A. Downey, J.M. (1991) Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation, 84, 350 356.
55. Liu, Y., Kato, H., Nakata, N. Kogure, K. (1992) Protection of rat hippocampus against ischemic neuronal damage by pretreatment with sublethal ischemia. Brain Res., 586, 121 124.
56. Lobner, D. Lipton, P. (1993) Intracellular calcium levels and calcium fluxes in the CA1 region of the rat hippocampal slice during in-vitro ischemia - relationship to electrophysiological cell-damage. J. Neurosci., 13, 4861 4871.
57. Madl, J.E. Burgesser, K. (1993) Adenosine triphosphate depletion reverses sodium-dependent, neuronal uptake of glutamate in rat hippocampal slices. J. Neurosci., 13, 4429 4444.
58. Matsumoto, N., Komiyama, S. Akaike, N. (2002) Pre- and postsynaptic ATP-sensitive potassium channels during metabolic inhibition of rat hippocampal CA1 neurons. J. Physiol., 541, 511 520.
59. +-dependent conductance. J. Neurophysiol., 57, 496 509.
60. de Mendonca, A. Ribeiro, J.A. (2000) Long-term potentiation observed upon blockade of adenosine A1 receptors in rat hippocampus is N-methyl-d-aspartate receptor-dependent. Neurosci. Lett., 291, 81 84.
61. Miyashita, K., Abe, H., Nakajima, T., Ishikawa, A., Nishiura, M., Sawada, T. Naritomi, H. (1994) Induction of ischaemic tolerance in gerbil hippocampus by pretreatment with focal ischaemia. Neuroreport, 6, 46 48.
62. +-ATPase activities in global cerebral ischemia-exposed rats. Neurochem. Internat., 44, 585 594.
63. Murry, C.E., Jennings, R.B. Reimer, K.A. (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation, 74, 1124 1136.
64. Norenberg, W., Wirkner, K. Illes, P. (1997) Effect of adenosine and some of its structural analogues on the conductance of NMDA receptor channels in a subset of rat neostriatal neurones. Br. J. Pharmacol., 122, 71 80.
65. Norenberg, W., Wirkner, K., Assmann, H., Richter, M. Illes, P. (1998) Adenosine A2A receptors inhibit the conductance of NMDA receptor channels in rat neostriatal neurons. Amino Acids, 14, 33 39.
66. Obrenovitch, T.P., Urenjak, J., Zilkha, E. Jay, T.M. (2000) Excitotoxicity in neurological disorders - the glutamate paradox. Int. J. Dev. Neurosci., 18, 281 287.
67. + pump and endothelial cell survival: [Na+]i/[K+]i-independent necrosis triggered by ouabain, and protection against apoptosis mediated by elevation of [Na+]i. Pflugers Arch. Physiol., 448, 335 345.
68. Pasdois, P., Quinlan, C.L., Rissa, A., Tariosse, L., Vinassa, B., Costa, A.D., Pierre, S.V., Dos Santos, P. Garlid, K.D. (2007) Ouabain protects rat hearts against ischemia-reperfusion injury via pathway involving src kinase, mitoKATP, and ROS. Am. J. Physiol. Heart Circ. Physiol., 292, H1470 H1478.
69. + ATP channel and protein kinase C. Neuroscience, 89, 453 459.
70. Perez-Pinzon, M.A., Mumford, P.L., Rosenthal, M. Sick, T.J. (1996) Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience, 75, 687 694.
71. Perez-Pinzon, M.A., Born, J.G. Centeno, J.M. (1999) Calcium and increase excitability promote tolerance against anoxia in hippocampal slices. Brain Res., 833, 20 26.
72. Perkins, M.N. Stone, T.W. (1982) An iontophoretic investigation of the actions of convulsant kynurenines and their interaction with the endogenous excitant quinolinic acid. Brain Res., 247, 184 187.
73. Phillis, J.W. (1995) The effects of selective A1 and A2a adenosine receptor antagonists on cerebral ischemic injury in the gerbil. Brain Res., 705, 79 84.
74. +-ATPase signaling cascade in rat hearts. Cardiovasc. Res., 73, 488 496.
75. Poolos, N.P. Johnston, D. (1999) Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci., 19, 5205 5212.
76. Pringle, A.K., Thomas, S.J., Signorelli, F. Iannotti, F. (1999) 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.
77. Pugliese, A.M., Latini, S., Corradetti, R. Pedata, F. (2003) Brief, repeated, oxygen-glucose deprivation episodes protect neurotransmission from a longer ischemic episode in the in vitro hippocampus: role of adenosine receptors. Br. J. Pharmacol., 140, 305 314.
78. Reich, C.G., Mason, S.E. Alger, B.E. (2004) Novel form of LTD induced by transient, partial inhibition of the Na,K-pump in rat hippocampal CA1 cells. J. Neurophysiol., 91, 239 247.
79. +-ATPase inhibitor. Comparison with ouabain. Neurochem. Int., 39, 301 310.
80. Reshef, A., Sperling, O. Zoref-Shani, E. (1998) Adenosine-induced preconditioning of rat neuronal cultures against ischemia-reperfusion injury. Adv. Exp. Med. Biol., 431, 365 368.
81. Reshef, A., Sperling, O. Zoref-Shani, E. (2000a) Role of K(ATP) channels in the induction of ischemic tolerance by the 'adenosine mechanism' in neuronal cultures. Adv. Exp. Med. Biol., 486, 217 221.
82. Reshef, A., Sperling, O. Zoref-Shani, E. (2000b) Opening of K(ATP) channels is mandatory for acquisition of ischemic tolerance by adenosine. Neuroreport, 11, 463 465.
83. Rossi, D.J., Oshima, T. Attwell, D. (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature, 403, 316 321.
84. ++ exchange inhibitor KB-R7943 protects CA1 neurons in rat hippocampal slices against hypoxic/ischaemic injury. Neuropharmacology, 38, 319 321.
85. Schurr, A., Reid, K.H., Tseng, M.T., West, C. Rigor, B.M. (1986) Adaptation of adult brain tissue to anoxia and hypoxia in vitro. Brain Res., 374, 244 248.
86. Schurr, A., Payne, R.S., Tseng, M.T., Gozal, E. Gozal, D. (2001) Excitotoxic preconditioning elicited by both glutamate and hypoxia and abolished by lactate transport inhibition in rat hippocampal slices. Neurosci. Lett., 307, 151 154.
87. + channels is involved in ischemic preconditioning in canine hearts. J. Mol. Cell. Cardiol., 37, 1213 1218.
88. Soundarapandian, M.M., Zhong, X.F., Peng, L.S., Wu, D. Lu, Y.M. (2007) Role of K-ATP channels in protection against neuronal excitatory insults. J. Neurochem., 103, 1721 1729.
89. Stelmashuk, E.V., Isaev, N.K., Andreeva, N.A. Viktorov, I.V. (1996) Ouabain modulates the toxic effect of glutamate in dissociated cultures of granular cells in the rat cerebellum. Bull. Eksp. Biol. Med., 122, 163 166.
90. Stone, T.W. (2002) Purines and neuroprotection. Adv. Exp. Biol. Med., 513, 249 280.
91. Storm, J.F. (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol., 385, 733 759.
92. Tissier, R., Souktani, R., Bruneval, P., Giudicelli, J.F., Berdeaux, A. Ghaleh, B. (2002) Adenosine A(1)-receptor induced late preconditioning and myocardial infarction: reperfusion duration is critical. Am. J. Physiol. Heart Circ. Physiol., 283, H38 H43.
93. +-ATPases in the rat CA1 hippocampal region. J. Neurophysiol., 88, 2963 2978.
94. Valente, R.C., Capella, L.S., Monteiro, R.Q., Rumjanek, V.M., Lopes, A.G. Capella, M.A. (2003) Mechanisms of ouabain toxicity. FASEB J., 17, 1700 1702.
95. Virgili, M., Vandi, M. Contestabile, A. (1997) Ischemic and excitotoxic damage to brain slices from normal and microencephalic rats. Neurosci. Lett., 233, 53 57.
96. Von Lubitz, D., Beenhakker, M., Lin, R., Carter, M., Paul, I., Bischofberger, N. Jacobson, K.A. (1996) Reduction of postischemic brain damage and memory deficits following treatment with the selective adenosine A1 receptor agonist. Eur. J. Pharmacol., 302, 43 48.
97. Wallis, R.A., Panizzon, K.L. Nolan, J.P. (1994) Glycine-induced CA1 excitotoxicity in the rat hippocampal slice. Brain Res., 664, 115 125.
98. Winn, H.R., Rubio, R. Berne, R.M. (1981) Brain adenosine concentration during hypoxia in rats. Am. J. Physiol., 241, H235 H242.
99. Wirkner, K., Assmann, H., Koles, L., Gerevich, Z., Franke, H., Norenberg, W., Boehm, R. Illes, P. (2000) Inhibition by adenosine A(2A) receptors of NMDA but not AMPA currents in rat neostriatal neurons. Br. J. Pharmacol., 130, 259 269.
100. Wirkner, K., Gerevich, Z., Krause, T., Gunther, A., Koles, L., Schneider, D., Norenberg, W. Illes, P. (2004) Adenosine A2A receptor-induced inhibition of NMDA and GABAA receptor-mediated synaptic currents in a subpopulation of rat striatal neurons. Neuropharmacology, 46, 994 1007.
101. Youssef, F.F., Addae, J.I. Stone, T.W. (2006) NMDA-induced preconditioning attenuates synaptic plasticity in the rat hippocampus. Brain Res., 1073-1074, 183 189.
102. Zhan, R.Z., Fujiwara, N., Tanaka, E. Shimoji, K. (1998) Intracellular acidification induced by membrane depolarization in rat hippocampal slices: roles of intracellular Ca2+ and glycolysis. Brain Res., 780, 86 94.