Enhancement of excitatory synaptic transmission in spiny neurons after transient forebrain ischemia

Journal of Neurophysiology

Volumn 95, Issue 3, 2006, Pages 1537-1544

  Zhang, Yuchun ^a   Deng, Ping ^a   Li, Yan ^a   Xu, Zao C ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GLUTAMIC ACID; PURINE P2X RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; VOLTAGE GATED CALCIUM CHANNEL;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATORY JUNCTION POTENTIAL; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR CALCIUM; MALE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SPINAL CORD NERVE CELL; STATISTICAL SIGNIFICANCE; SYNAPTIC TRANSMISSION; TRANSIENT ISCHEMIC ATTACK; ACTION POTENTIAL; ANIMAL; FOREBRAIN; LONG TERM POTENTIATION; NEOSTRIATUM; NERVE CELL; PATHOPHYSIOLOGY; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; BRAIN ISCHEMIA; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MALE; NEOSTRIATUM; NEURONS; PROSENCEPHALON; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 33645963185     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01166.2005     Document Type: Article

References (60)

1. Abdel-Hamid KM and Tymianski M. Mechanisms and effects of intracellular calcium buffering on neuronal survival in organotypic hippocampal cultures exposed to anoxia/aglycemia or to excitotoxins. J Neurosci 17: 3538-3553, 1997.
2. Amadio S, D'Ambrosi N, Cavaliere F, Murra B, Sancesario G, Bernardi G, Burnstock G, and Volonte C. P2 receptor modulation and cytotoxic function in cultured CNS neurons. Neuropharmacology 42: 489-501, 2002.
3. Benveniste H, Drejer J, Schousboe A, and Diemer NH. Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43: 1369-1374, 1984.
4. Braun N, Zhu Y, Krieglstein J, Culmsee C, and Zimmermann H. Upregulation of the enzyme chain hydrolyzing extracellular ATP after transient forebrain ischemia in the rat. J Neurosci 18: 4891-4900, 1998.
5. Calabresi P, Centonze D, Pisani A, and Bernardi G. Endogenous adenosine mediates the presynaptic inhibition induced by aglycemia at corticostriatal synapses. J Neurosci 17: 4509-4516, 1997a.
6. Calabresi P, Centonze D, Pisani A, and Bernardi G. A possible mechanism for the aglycemia-induced depression of glutamatergic excitation in the striatum. J Cereb Blood Flow Metab 17: 1121-1126, 1997b.
7. Calabresi P, Saulle E, Centonze D, Pisani A, Marfia GA, and Bernardi G. Post-ischaemic long-term synaptic potentiation in the striatum: a putative mechanism for cell type-specific vulnerability. Brain 125: 844-860, 2002.
8. Cavaliere F, D'Ambrosi N, Sancesario G, Bernardi G, and Volonte C. Hypoglycaemia-induced cell death: features of neuroprotection by the P2 receptor antagonist basilen blue. Neurochem Int 38: 199-207, 2001.
9. Chesselet MF, Gonzales C, Lin CS, Polsky K, and Jin BK. Ischemic damage in the striatum of adult gerbils: relative sparing of somatostatinergic and cholinergic interneurons contrasts with loss of efferent neurons. Exp Neurol 110: 209-218, 1990.
10. Choi DW and Rothman SM. The role of glutamate neurotoxicity in hypoxicischemic neuronal death. Annu Rev Neurosci 13: 171-182, 1990.
11. Crépel V, Hammond C, Chinestra P, Diabira D, and Ben-Ari Y. A selective LTP of NMDA receptor-mediated currents induced by anoxia in CA1 hippocampal neurons. J Neurophysiol 70: 2045-2055, 1993.
12. Deng P, Pang ZP, Zhang Y, and Xu ZC. Increase of delayed rectifier potassium currents in large aspiny neurons in the neostriatum following transient forebrain ischemia. Neuroscience 131: 135-146, 2005.
13. Deuchars SA, Atkinson L, Brooke RE, Musa H, Milligan CJ, Batten TF, Buckley NJ, Parson SH, and Deuchars J. Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21: 7143-7152, 2001.
14. Dubyak GR and el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol Cell Physiol 265: C577-606, 1993.
15. Dutta AK, Sabirov RZ, Uramoto H, and Okada Y. Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J Physiol 559: 799-812, 2004.
16. Fowler JC, Gervitz LM, Hamilton ME, and Walker JA. Systemic hypoxia and the depression of synaptic transmission in rat hippocampus after carotid artery occlusion. J Physiol 550: 961-972, 2003.
17. Francis A and Pulsinelli W. The response of GABAergic and cholinergic neurons to transient cerebral ischemia. Brain Res 243: 271-278, 1982.
18. Franke H, Gunther A, Grosche J, Schmidt R, Rossner S, Reinhardt R, Faber-Zuschratter H, Schneider D, and Illes P. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 63: 686-699, 2004.
19. Gajendiran M, Ling GY, Pang Z, and Xu ZC. Differential changes of synaptic transmission in spiny neurons of rat neostriatum following transient forebrain ischemia. Neuroscience 105: 139-152, 2001.
20. Gao TM, Howard EM, and Xu ZC. Transient neurophysiological changes in CA3 neurons and dentate granule cells after severe forebrain ischemia in vivo. J Neurophysiol 80: 2860-2869, 1998a.
21. Gao TM, Pulsinelli WA, and Xu ZC. Prolonged enhancement and depression of synaptic transmission in CA1 pyramidal neurons induced by transient forebrain ischemia in vivo. Neuroscience 87: 371-383, 1998b.
22. Gao TM and Xu ZC. In vivo intracellular demonstration of an ischemiainduced postsynaptic potential from CA1 pyramidal neurons in rat hippocampus. Neuroscience 75: 665-669, 1996.
23. Gervitz LM, Lutherer LO, Davies DG, Pirch JH, and Fowler JC. Adenosine induces initial hypoxic-ischemic depression of synaptic transmission in the rat hippocampus in vivo. Am J Physiol Regulatory Integrative Comp Physiol 280: R639-645, 2001.
24. Globus MY, Busto R, Dietrich WD, Martinez E, Valdes I, and Ginsberg MD. Effect of ischemia on the in vivo release of striatal dopamine, glutamate, and gamma-aminobutyric acid studied by intracerebral microdialysis. J Neurochem 51: 1455-1464, 1988.
25. 2+ influx in hippocampal CA1 neurons of gerbil. J Neurosci 17: 6179-6188, 1997.
26. Hershkowitz N, Katchman AN, and Veregge S. Site of synaptic depression during hypoxia: a patch-clamp analysis. J Neurophysiol 69: 432-441, 1993.
27. Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, and Ryan AF. Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407: 11-32, 1999.
28. Khakh BS, Gittermann D, Cockayne DA, and Jones A. ATP modulation of excitatory synapses onto interneurons. J Neurosci 23: 7426-7437, 2003.
29. Khakh BS and Henderson G. ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol Pharmacol 54: 372-378, 1998.
30. Kita H. Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience 70: 925-940, 1996.
31. Lutz PL and Kabler S. Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia. Brain Res 769: 281-286, 1997.
32. Magee JC and Johnston D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301-304, 1995.
33. Mitani A, Namba S, Ikemune K, Yanase H, Arai T, and Kataoka K. Postischemic enhancements of N-methyl-D-aspartic acid (NMDA) and non-NMDA receptor-mediated responses in hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 18: 1088-1098, 1998.
34. Monyer H, Giffard RG, Hartley DM, Dugan LL, Goldberg MP, and Choi DW. Oxygen or glucose deprivation-induced neuronal injury in cortical cell cultures is reduced by tetanus toxin. Neuron 8: 967-973, 1992.
35. Mori M, Heuss C, Gahwiler BH, and Gerber U. Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 535: 115-123, 2001.
36. Neary JT, Rathbone MP, Cattabeni F, Abbracchio MP, and Burnstock G. Trophic actions of extracellular nucleotides and nucleosides on glial and neuronal cells. Trends Neurosci 19: 13-18, 1996.
37. Nieber K, Eschke D, and Brand A. Brain hypoxia: effects of ATP and adenosine. Prog Brain Res 120: 287-297, 1999.
38. Obrenovitch TP, Urenjak J, Zilkha E, and Jay TM. Excitotoxicity in neurological disorders-the glutamate paradox. Int J Dev Neurosci 18: 281-287, 2000.
39. Pang ZP, Deng P, Ruan YW, and Xu ZC. Depression of fast excitatory synaptic transmission in large aspiny neurons of the neostriatum after transient forebrain ischemia. J Neurosci 22: 10948-10957, 2002.
40. Pellegrini-Giampietro DE, Zukin RS, Bennett MV, Cho S, and Pulsinelli WA. Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc Natl Acad Sci USA 89: 10499-10503, 1992.
41. Pulsinelli WA and Brierley JB. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 10: 267-272, 1979.
42. Pulsinelli WA, Brierley JB, and Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11: 491-498, 1982.
43. Ralevic V. The involvement of smooth muscle P2X receptors in the prolonged vasorelaxation response to purine nucleotides in the rat mesenteric arterial bed. Br J Pharmacol 135: 1988-1994, 2002.
44. Ren Y, Li X, and Xu ZC. Asymmetrical protection of neostriatal neurons against transient forebrain ischemia by unilateral dopamine depletion. Exp Neurol 146: 250-257, 1997.
45. Robson SC, Kaczmarek E, Siegel JB, Candinas D, Koziak K, Millan M, Hancock WW, and Bach FH. Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med 185: 153-163, 1997.
46. Rothman SM and Olney JW. Glutamate and the pathophysiology of hypoxic -ischemic brain damage. Ann Neurol 19: 105-111, 1986.
47. Ryu JK, Kim J, Choi SH, Oh YJ, Lee YB, Kim SU, and Jin BK. ATP-induced in vivo neurotoxicity in the rat striatum via P2 receptors. Neuroreport 13: 1611-1615, 2002.
48. Sharma G and Vijayaraghavan S. Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38: 929-939, 2003.
49. 2+ entry through presynaptic P2X receptors elicits postsynaptic firing in the brainstem autonomic network. J Neurosci 24: 3125-3135, 2004.
50. Stuart G and Sakmann B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065-1076, 1995.
51. Sugahara M, Asai S, Zhao H, Nagata T, Kunimatsu T, Ishii Y, Kohno T, and Ishikawa K. Extracellular glutamate changes in rat striatum during ischemia determined by a novel dialysis electrode and conventional microdialysis. Neurochem Int 39: 65-73, 2001.
52. Takagi N, Sasakawa K, Besshoh S, Miyake-Takagi K, and Takeo S. Transient ischemia enhances tyrosine phosphorylation and binding of the NMDA receptor to the Src homology 2 domain of phosphatidylinositol 3-kinase in the rat hippocampus. J Neurochem 84: 67-76, 2003.
53. Tanaka E, Yasumoto S, Hattori G, Niiyama S, Matsuyama S, and Higashi H. Mechanisms underlying the depression of evoked fast EPSCs following in vitro ischemia in rat hippocampal CA1 neurons. J Neurophysiol 86: 1095-1103, 2001.
54. Tanaka K. Alteration of second messengers during acute cerebral ischemia - adenylate cyclase, cyclic AMP-dependent protein kinase, and cyclic AMP response element binding protein. Prog Neurobiol 65: 173-207, 2001.
55. Trussell LO, Thio LL, Zorumski CF, and Fischbach GD. Rapid desensitization of glutamate receptors in vertebrate central neurons. Proc Natl Acad Sci USA 85: 2834-2838, 1988.
56. Tsubokawa H, Oguro K, Masuzawa T, and Kawai N. Ca(2+)-dependent non-NMDA receptor-mediated synaptic currents in ischemic CA1 hippocampal neurons. J Neurophysiol 71: 1190-1196, 1994.
57. Tsubokawa H, Oguro K, Masuzawa T, and Kawai N. Spontaneous excitatory postsynaptic currents in hippocampal CA1 pyramidal neurons of the gerbil after transient ischemia. Neurosci Lett 191: 95-98, 1995.
58. Volonte C, Amadio S, Cavaliere F, D'Ambrosi N, Vacca F, and Bernardi G. Extracellular ATP and neurodegeneration. Curr Drug Targets CNS Neurol Disord 2: 403-412, 2003.
59. Wang J, Liu S, Fu Y, Wang JH, and Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat Neurosci 6: 1039-1047, 2003.
60. Zimmermann H. Signalling via ATP in the nervous system. Trends Neurosci 17: 420-426, 1994.