Irreversible impairment of inhibitory neurons and nitric oxide release in the neocortex produced by low temperature and hypoxia in vitro

Neuroscience Research

Volumn 33, Issue 4, 1999, Pages 307-316

  Fujisaki, Toshiyuki ^a,b   Wakatsuki, Hidemitsu ^a   Kudoh, Masaharu ^a   Shibuki, Katsuei ^a  

^a Niigata University   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Hyperexcitability; Hypoxia; Inhibitory neurons; Low temperature; Neocortex; Neural damage; Nitric oxide

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; BICUCULLINE; MUSCIMOL; N(G) NITROARGININE; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN NERVE CELL; BRAIN SLICE; COLD EXPOSURE; CONTROLLED STUDY; FEMALE; HYPOXIA; INTERNEURON; MALE; NEOCORTEX; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL LESION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; BICUCULLINE; CELL HYPOXIA; COLD; EVOKED POTENTIALS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABA AGONISTS; MALE; MUSCIMOL; N-METHYLASPARTATE; NEOCORTEX; NEURAL INHIBITION; NITRIC OXIDE; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 0033020189     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-0102(99)00023-1     Document Type: Article

References (59)

1. Borisy G.G., Olmsted J.B., Marcum J.M., Allen C. Microtubule assembly in vitro. Fed. Proc. 33:1974;167-174.
2. Bredt D.S., Glatt C.E., Hwang P.M., Fotuhi M., Dawson T.M., Snyder S.H. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron. 7:1991;615-624.
3. Bredt D.S., Snyder S.H. Nitric oxide, a physiological messenger molecule. Annu. Rev. Biochem. 63:1994;175-195.
4. Cellio M.R. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerrbral cortex. Science. 231:1986;995-997.
5. Choi D.W. Excitotoxic cell death. J. Neurobiol. 23:1992;1261-1276.
6. Cocito L., Favale E., Reni L. Epileptic seizures in cerebral arterial occlusive disease. Stroke. 13:1982;189-195.
7. Conger P., Khazipov R., Ben-Ari Y. Direct demonstration of functional disconnection by anoxia of inhibitory interneurons from excitatory inputs in rat hippocampus. J. Neurophysiol. 73:1995;421-426.
8. Domann R., Hagemann G., Kraemer M., Freund H.-J., Witte O.W. Electrophysiological changes in the surrounding brain tissue of photochemically induced cortical infarcts in the rat. Neurosci. Lett. 155:1993;69-72.
9. Doolette D.J., Kerr D.I.B. Hyperexcitability in CA1 of the rat hippocampal slice following hypoxia or adenosine. Brain Res. 677:1995;127-137.
10. Dunwiddie T.V. Age-related difference in the in vitro rat hippocampus. Development of inhibition and the effects of hypoxia. Dev. Neurosci. 4:1981;165-175.
11. Emery D.G., Lucas J.H. Ultrastructural damage and neuritic beading in cold-stressed spinal neurons with comparisons to NMDA and A23187 toxicity. Brain Res. 692:1995;161-173.
12. Ferry P.C. Neurologic sequalae of open-heart surgery in children. An 'irritating question'. Am. J. Dis. Child. 144:1990;369-373.
13. Freund T.F., Magloczky Z.S. Early degeneration of calretinin-containing neurons in the rat hippocampus after ischemia. Neuroscience. 56:1993;581-596.
14. +. J. Neurosci. 13:1993;63-72.
15. Fujisaki T., Kudoh M., Shibuki K. Functional brain block preparation of the rat auditory cortex. Neurosci. Res. 23:1995;321-326.
16. Fujisaki T., Kudoh M., Shibuki K. Selective impairment of inhibitory neurons in isolated rat neocortical blocks kept hypoxic at low temperature. Jpn. J. Physiol. (Suppl. 2). 47:1997;S134.
17. Fujisaki T., Kudoh M., Shibuki K. Acute neural damage in the rat neocortex in vitro induced by a combination of anoxia and mechanical stress. Neuroscience. 84:1998;591-601.
18. Fujiwara N., Higashi H., Shimoji K., Yoshimura M. Effects of hypoxia on rat hippocampal neurones in vitro. J. Physiol. (Lond). 384:1987;131-151.
19. Gabbott P.L., Dickie B.G., Vaid R.R., Headlam A.J.N., Bacon S.J. Local-circuit neurons in the medial prefrontal cortex (arias 25, 32 and 24b) in the rat: morphology and quantitative distribution. J. Comp. Neurol. 377:1997;465-499.
20. Goldberg M.P., Choi D.W. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J. Neurosci. 13:1993;3510-3524.
21. Hatashita S., Hoff J.T. Cortical tissue pressure gradients in early ischemic brain edema. J. Cereb. Blood Flow Metab. 6:1986;1-7.
22. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 75:1993;1273-1286.
23. Jung M.W., Larson J., Lynch G. Role of NMDA and non-NMDA receptors in synaptic transmission in rat piriform cortex. Exp. Brain Res. 82:1990;451-455.
24. A-mediated inhibitory postsynaptic current. J. Neurophysiol. 71:1994;1128-1138.
25. Kawaguchi Y., Katsumaru H., Kosaka T., Heizmann C.W., Hama K. Fast spiking cells in the rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416:1987;369-374.
26. Khazipov R., Bragestovski P., Ben-Ari Y. Hippocampal inhibitory interneurons are functionally disconnected from excitatory inputs by anoxia. J. Neurophysiol. 70:1993;2251-2259.
27. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239:1982;57-69.
28. Krieg W.J.S. Connections of the cerebral cortex. J. Comp. Neurol. 84:1964;221-275.
29. Kmjević K., Xu Y.Z., Zhang L. Anoxic block of GABAergic IPSPs. Neurochem. Res. 16:1991;279-284.
30. Kudoh M., Shibuki K. Long-term potentiation of supragranular outputs in the rat auditory cortex. Exp. Brain Res. 110:1996;21-27.
31. Luhmann H.J., Heinemann U. Hypoxia-induced functional alterations in adult rat neocortex. J. Neurophysiol. 67:1992;798-811.
32. Luhmann H.J., Kral T., Heinemann U. Influence of hypoxia on excitation and GABAergic inhibition in mature and developing rat neocortex. Exp. Brain Res. 97:1993;209-224.
33. Luhmann H.J., Mudrick-Donnon L.A., Mittmann T., Heinemann U. Ischemia-induced long-term hyperexcitability in rat neocortex. Eur. J. Neurosci. 7:1995;180-191.
34. Madison D., Niedermeyer E. Epileptic seizures resulting from acute cerebral anoxia. J. Neurol. Neurosurg. Psychiat. 33:1970;381-386.
35. Morris C.E. Mechanosensitive ion channels. J. Membrane Biol. 113:1990;93-107.
36. Okada Y. Recovery of neuronal activity and high-energy compound level after complete and prolonged brain ischemia. Brain Res. 72:1974;346-349.
37. Okada Y., Sakurai T., Mori M. Excitatory effect of adenosine on neurotransmission is due to increase of transmitter release in the hippocampal slices. Neurosci. Lett. 142:1992;233-236.
38. Olmsted J.B., Borisy G.G. Microtubules. Ann. Rev. Biochem. 42:1973;507-540.
39. Prieto J.J., Peterson B.A., Winer J.A. Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J. Comp. Neurol. 344:1994;349-382.
40. Quast M.J., Huang N.C., Hillman G.R., Kent T.A. The evolution of acute stroke recorded by multimodal magnetic resonance imaging. Magn. Reson. Imaging. 11:1993;465-471.
41. Rall W. Electrophysiology of a dendritic neuron model. Biophys. J. 2:1962;145-167.
42. Ribak C.E., Bradurne R.M., Harris A.B. A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex. J. Neurosci. 2:1982;1725-1735.
43. Rittenhouse E.A., Mohri H., Dillard D.H., Merendino K.A. Deep hypothermia in cardiovascular surgery. Ann. Thorac. Surg. 17:1974;63-98.
44. Romijn H.J., Ruijter J.M., Wolters P.S. Hypoxia preferentially destroys GABAergic neurons in developing rat neocortex explants in culture. Exp. Neurol. 100:1988;322-340.
45. Rosen A.S., Morris M.E. Anoxic depression of excitatory and inhibitory postsynaptic potentials in rat neocortical slices. J. Neurophysiol. 69:1993;109-117.
46. Rosenmund C., Feltz A., Westbrook G.L. Synaptic NMDA receptor channels have a low open probability. J. Neurosci. 15:1995;2788-2795.
47. Rothman S. Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J. Neurosci. 4:1984;1884-1891.
48. Schiff S.J., Somjen G.G. Hyperexcitability following moderate hypoxia in hippocampal tissue slices. Brain Res. 337:1985;337-340.
49. Schuier F.J., Hossmann K.-A. Experimental brain infarcts in cats. II. Ischemic Brain Edema. Stroke. 11:1980;593-601.
50. Shibuki K., Kimura S. Dynamic properties of nitric oxide release from parallel fibres in rat cerebellar slices. J. Physiol. (Lond.). 498:1997;443-452.
51. Sloper J.J., Johnson P., Powell T.P.S. Selective degeneration of interneurons in the motor cortex of infant monkeys following controlled hypoxia: a possible cause of epilepsy. Brain Res. 198:1980;204-209.
52. Tecoma E.S., Choi D.W. GABAergic neocortical neurons are resistant to NMDA receptor-mediated injury. Neurology. 39:1989;676-682.
53. Tsumoto T. Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex. Neurosci. Res. 9:1990;79-102.
54. Valtschanoff J.G., Weinberg R.J., Kharazia V.N., Schmidt H.H.H.W., Nakane M., Rustioni A. Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci. Lett. 157:1993;157-161.
55. A receptor function in the early period after transient forebrain ischaemia in the rat. Eur. J. Neurosci. 5:1993;955-960.
56. Wakatsuki H., Gomi H., Kudoh M., Kimura S., Takahashi K., Takeda M., Shibuki K. Layer-specific NO dependence of long-term potentiation and biased NO release in layer V in the rat auditory cortex. J. Physiol. (Lond.). 531:1998;71-81.
57. Wiche G., Cole R.D. Reversible in vitro polymerization of tubulin from a cultured cell line (rat glial cell clone C6). Proc. Natl. Acad. Sci. USA. 73:1976;1227-1231.
58. Winer J.A. Neurons accumulating [3H] gamma-aminobutyric acid (GABA) in supragranular layers of cat primary auditory cortex (AI). Neuroscience. 19:1986;771-793.
59. Wong-Riley M., Carroll E.W. Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature. 307:1984;262-264.