Soman induces ictogenesis in the amygdala and interictal activity in the hippocampus that are blocked by a GluR5 kainate receptor antagonist in vitro

Neuroscience

Volumn 159, Issue 1, 2009, Pages 380-389

  Apland, J P ^a   Aroniadou Anderjaska, V ^b   Braga, M F M ^b  

^a US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

basolateral amygdala; CA1 area; GluR5 receptors; ictogenesis; nerve agents

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; GLUTAMATE RECEPTOR 5; IONOTROPIC RECEPTOR ANTAGONIST; KAINIC ACID RECEPTOR ANTAGONIST; SOMAN; UBP 302; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; DEVELOPMENT; DRUG EXPOSURE; ELECTRIC POTENTIAL; EPILEPTIC DISCHARGE; EVOKED RESPONSE; HIPPOCAMPUS; ICTOGENESIS; IN VITRO STUDY; MALE; MEDICAL LITERATURE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REGULATORY MECHANISM; SEIZURE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ALANINE; AMYGDALA; ANIMALS; CALCIUM; EVOKED POTENTIALS; HIPPOCAMPUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; SEIZURES; SOMAN; THYMINE;

EID: 60349104146     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.11.053     Document Type: Article

References (79)

1. Abou-Donia M.B. Organophosphorus ester-induced delayed neurotoxicity. Annu Rev Pharmacol Toxicol 21 (1981) 511-548
2. Apland J. Effects of anticonvulsant drugs on soman-induced epileptiform activity in guinea pig hippocampal-entorhinal slices. USAMRICD-TR-01-02 (2001), U.S. Army Medical Research Institute of Chemical Defense, Aberdeen Proving Ground, MD
3. Aroniadou-Anderjaska V., Post R.M., Rogawski M.A., and Li H. Input-specific LTP and depotentiation in the basolateral amygdala. Neuroreport 2 (2001) 635-640
4. Aroniadou-Anderjaska V., Qashu F., and Braga M.F. Mechanisms regulating GABAergic inhibitory transmission in the basolateral amygdala: Implications for epilepsy and anxiety disorders. Amino Acids 32 (2007) 305-315
5. Aroniadou-Anderjaska V., Fritsch B., Qashu F., and Braga M.F. Pathology and pathophysiology of the amygdala in epileptogenesis and epilepsy. Epilepsy Res 78 (2008) 102-116
6. Baille V., Clarke P.G., Brochier G., Dorandeu F., Verna J.M., Four E., Lallement G., and Carpentier P. Soman-induced convulsions: the neuropathology revisited. Toxicology 215 (2005) 1-24
7. Bajgar J. Complex view on poisoning with nerve agents and organophosphates. Acta Medica (Hradec Kralove) 48 (2005) 3-21
8. Bajgar J., Sevelova L., Krejcova G., Fusek J., Vachek J., Kassa J., Herink J., de Jong L.P., and Benschop H.P. Biochemical and behavioral effects of soman vapors in low concentrations. Inhal Toxicol 16 (2004) 497-507
9. Barthold C.L., and Schier J.G. Organic phosphorus compounds: nerve agents. Crit Care Clin 21 (2005) 673-689
10. Baze W.B. Soman-induced morphological changes: an overview in the nonhuman primate. J Appl Toxicol 13 (1993) 173-177
11. Benini R., D'Antuono M., Pralong E., and Avoli M. Involvement of amygdala networks in epileptiform synchronization in vitro. Neuroscience 120 (2003) 75-84
12. Bernard A., and Khrestchatisky M. Assessing the extent of RNA editing in the TMII regions of GluR5 and GluR6 kainate receptors during rat brain development. J Neurochem 62 (1994) 2057-2060
13. Bettler B., Boulter J., Hermans-Borgmeyer I., O'Shea-Greenfield A., Deneris E.S., Moll C., Borgmeyer U., Hollmann M., and Heinemann S. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5 (1990) 583-595
14. Bortolotto Z.A., Nistico R., More J.C., Jane D.E., and Collingridge G.L. Kainate receptors and mossy fiber LTP. Neurotoxicology 26 (2005) 769-777
15. Boskovic B. The treatment of soman poisoning and its perspectives. Toxicol Sci 1 (1981) 203-213
16. Braga M.F., Aroniadou-Anderjaska V., Xie J., and Li H. Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J Neurosci 23 (2003) 442-452
17. Braga M.F., Aroniadou-Anderjaska V., and Li H. The physiological role of kainate receptors in the amygdala. Mol Neurobiol 30 (2004) 127-141
18. Brown M.A., and Brix K.A. Review of health consequences from high, intermediate, and low-level exposure to organophosphorus nerve agents. J Appl Toxicol 6 (1998) 393-408
19. Burnashev N., Villarroel A., and Sakmann B. Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J Physiol (Lond) 496 (1996) 165-173
20. Chittajallu R., Braithwaite S.P., Clarke V.R., and Henley J.M. Kainate receptors: subunits, synaptic localization and function. Trends Pharmacol Sci 20 (1999) 26-35
21. Clarke V.R., Ballyk B.A., Hoo K.H., Mandelzys A., Pellizzari A., Bath C.P., Thomas J., Sharpe E.F., Davies C.H., Ornstein P.L., Schoepp D.D., Kamboj R.K., Collingridge G.L., Lodge D., and Bleakman D. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389 (1997) 599-603
22. Cole A.E., and Nicoll R.A. Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (Lond) 352 (1984) 173-188
23. Egorov A.V., Unsicker K., and von Bohlen und Halbach O. Muscarinic control of graded persistent activity in lateral amygdala neurons. Eur J Neurosci 24 (2006) 3183-3194
24. Endres W., Spuler A., and ten Bruggencate G. Acetylcholinesterase reactivators antagonize epileptiform bursting induced by paraoxon in guinea pig hippocampal slices. Pharmacol Exp Ther 251 (1989) 1181-1186
25. Fernández de Sevilla D., and Buño W. Presynaptic inhibition of Schaffer collateral synapses by stimulation of hippocampal cholinergic afferent fibres. Eur J Neurosci 17 (2003) 555-558
26. Fukudome Y., Ohno-Shosaku T., Matsui M., Omori Y., Fukaya M., Tsubokawa H., Taketo M.M., Watanabe M., Manabe T., and Kano M. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur J Neurosci 19 (2004) 2682-2692
27. Grasshoff C., Gillessen T., Thiermann H., Wagner E., and Szinicz L. The effect of acetylcholinesterase-inhibition on depolarization-induced GABA release from rat striatal slices. Toxicology 184 (2003) 149-156
28. Gryder D.S., and Rogawski M.A. Selective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J Neurosci 23 (2003) 7069-7074
29. Hadar E.J., Yang Y., Sayin U., and Rutecki P.A. Suppression of pilocarpine-induced ictal oscillations in the hippocampal slice. Epilepsy Res 49 (2002) 61-71
30. Harrison P.K., Sheridan R.D., Green A.C., Scott I.R., and Tattersall J.E. A guinea pig hippocampal slice model of organophosphate-induced seizure activity. J Pharmacol Exp Ther 310 (2004) 678-686
31. Harrison P.K., Sheridan R.D., Green A.C., and Tattersall J.E. Effects of anticonvulsants on soman-induced epileptiform activity in the guinea-pig in vitro hippocampus. Eur J Pharmacol 518 (2005) 123-132
32. Hayes J., Li S., Anwyl R., and Rowan M.J. A role for protein kinase A and protein kinase M zeta in muscarinic acetylcholine receptor-initiated persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 151 (2008) 604-612
33. Hayward I.J., Wall H.G., Jaax N.K., Wade J.V., Marlow D.D., and Nold J.B. Decreased brain pathology in organophosphate-exposed rhesus monkeys following benzodiazepine therapy. Neurol Sci 98 (1990) 99-106
34. Huettner J.E. Kainate receptors and synaptic transmission. Prog Neurobiol 70 (2003) 387-407
35. Kadar T., Shapira S., Cohen G., Sahar R., Alkalay D., and Raveh L. Sarin-induced neuropathology in rats. Hum Exp Toxicol 14 (1995) 252-259
36. Kaminski R.M., Banerjee M., and Rogawski M.A. Topiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist. Neuropharmacology 46 (2004) 1097-1104
37. Lallement G., Carpentier P., Collet A., Pernot-Marino I., Baubichon D., Sentenac-Roumanou H., and Blanchet G. Involvement of glutamatergic system of amygdala in generalized seizures induced by soman: comparison with the hippocampus. C R Acad Sci III 313 (1991) 421-426
38. Lallement G., Carpentier P., Collet A., Pernot-Marino I., Baubichon D., and Blanchet G. Effects of soman-induced seizures on different extracellular amino acid levels and on glutamate uptake in rat hippocampus. Brain Res 563 (1991) 234-240
39. Lallement G., Carpentier P., Pernot-Marino I., Baubichon D., Collet A., and Blanchet G. Involvement of the different rat hippocampal glutamatergic receptors in development of seizures induced by soman: an autoradiographic study. Neurotoxicology 12 (1991) 655-664
40. Lallement G., Carpentier P., Collet A., Baubichon D., Pernot-Marino I., and Blanchet G. Extracellular acetylcholine changes in rat limbic structures during soman-induced seizures. Neurotoxicology 13 (1992) 557-567
41. Layish I., Krivoy A., Rotman E., Finkelstein A., Tashma Z., and Yehezkelli Y. Pharmacologic prophylaxis against nerve agent poisoning. Isr Med Assoc J 7 (2005) 182-187
42. Lebeda F., Ton T., and Rutecki P. Synaptic inhibition and soman-induced epileptiform activity in the hippocampus. Proceedings of the Workshop on Convulsions and Related Brain Damage Induced by Organophosphorus Agents (1990), U.S. Army Medical Research Institute of Chemical Defense, Aberdeen Proving Ground, MD
43. Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4 (2003) 481-495
44. Li H., Chen A., Xing G., Wei M.L., and Rogawski M.A. Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 4 (2001) 612-620
45. Li S., Cullen W.K., Anwyl R., and Rowan M.J. Muscarinic acetylcholine receptor-dependent induction of persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 144 (2007) 754-761
46. Madison D.V., Lancaster B., and Nicoll R.A. Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7 (1987) 733-741
47. McCormick D.A., and Contreras D. On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63 (2001) 815-846
48. McDonald A.J. Is there an amygdala and how far does it extend?. An anatomical perspective. Ann N Y Acad Sci 985 (2003) 1-21
49. McDonough Jr. J.H., Smith R.F., and Smith C.D. Behavioral correlates of soman-induced neuropathology: deficits in DRL acquisition. Toxicol Teratol 8 (1986) 179-187
50. McDonough Jr. J.H., McLeod Jr. C.G., and Nipwoda M.T. Direct microinjection of soman or VX into the amygdala produces repetitive limbic convulsions and neuropathology. Brain Res 435 (1987) 123-137
51. McDonough Jr. J.H., and Shih T.M. Pharmacological modulation of soman-induced seizures. Neurosci Biobehav Rev 17 (1993) 203-215
52. McDonough Jr. J.H., and Shih T.M. Neuropharmacological mechanisms of nerve agent-induced seizure and neuropathology. Neurosci Biobehav Rev 21 (1997) 559-579
53. McDonough Jr. J.H., Zoeffel L.D., McMonagle J., Copeland T.L., Smith C.D., and Shih T.M. Anticonvulsant treatment of nerve agent seizures: anticholinergics versus diazepam in soman-intoxicated guinea pigs. Epilepsy Res 38 (2000) 1-14
54. Mohapel P., Dufresne C., Kelly M.E., and McIntyre D.C. Differential sensitivity of various temporal lobe structures in the rat to kindling and status epilepticus induction. Epilepsy Res 23 (1996) 179-187
55. More J.C., Nistico R., Dolman N.P., Clarke V.R., Alt A.J., Ogden A.M., Buelens F.P., Troop H.M., Kelland E.E., Pilato F., Bleakman D., Bortolotto Z.A., Collingridge G.L., and Jane D.E. Characterisation of UBP296: a novel, potent and selective kainate receptor antagonist. Neuropharmacology 47 (2004) 46-64
56. B receptors. Neuropharmacology 51 (2006) 1030-1037
57. Pitkänen A., Tuunanen J., Kalviainen R., Partanen K., and Salmenpera T. Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 32 (1998) 233-253
58. Pitkänen A. Connectivity of the rat amygdaloid complex. In: Aggleton J.P. (Ed). The amygdala: a functional analysis (2000), Oxford UP, New York, NY 31-115
59. Reed D.J., Withrow C.D., and Woodbury D.M. Electrolyte and acid-base parameters of rat cerebrospinal fluid. Exp Brain Res 3 (1967) 212-219
60. Rogawski M.A., Gryder D., Castaneda D., Yonekawa W., Banks M.K., and Lia H. GluR5 kainate receptors, seizures, and the amygdala. Ann N Y Acad Sci 985 (2003) 150-162
61. Rutecki P.A., and Yang Y. Ictal epileptiform activity in the CA3 region of hippocampal slices produced by pilocarpine. J Neurophysiol 79 (1998) 3019-3029
62. Rutecki P.A., Sayin U., Yang Y., and Hadar E. Determinants of ictal epileptiform patterns in the hippocampal slice. Epilepsia 43 (2002) 179-183
63. Sah P., Faber E.S., Lopez De Armentia M., and Power J. The amygdaloid complex: anatomy and physiology. Physiol Rev 83 (2003) 803-834
64. 2+-dependent PKC. J Neurophysiol 98 (2007) 952-965
65. Sang C.N., Ramadan N.M., Wallihan R.G., Chappell A.S., Freitag F.G., Smith T.R., Silberstein S.D., Johnson K.W., Phebus L.A., Bleakman D., Ornstein P.L., Arnold B., Tepper S.J., and Vandenhende F. LY293558, a novel AMPA/GluR5KR antagonist, is efficacious and well-tolerated in acute migraine. Cephalalgia 24 (2004) 596-602
66. Santos M.D., Pereira E.F., Aracava Y., Castro N.G., Fawcett W.P., Randall W.R., and Albuquerque E.X. Low concentrations of pyridostigmine prevent soman-induced inhibition of GABAergic transmission in the central nervous system: involvement of muscarinic receptors. J Pharmacol Exp Ther 304 (2003) 254-265
67. Savidge J.R., Bleakman D., and Bristow D.R. Identification of kainate receptor-mediated intracellular calcium increases in cultured rat cerebellar granule cells. J Neurochem 69 (1997) 1763-1766
68. Shih T.M., and McDonough J.H. Efficacy of biperiden and atropine as anticonvulsant treatment for organophosphorus nerve agent intoxication. Arch Toxicol 74 (2000) 165-172
69. Shih T.M., Duniho S.M., and McDonough J.H. Control of nerve agent induced seizures is critical for neuroprotection and survival. Toxicol Applied Pharmacol 188 (2003) 69-80
70. Singh S., and Sharma N. Neurological syndromes following organophosphate poisoning. Neurol India 48 (2000) 308-313
71. Smolders I., Bortolotto Z.A., Clarke V.R., Warre R., Khan G.M., O'Neill M.J., Ornstein P.L., Bleakman D., Ogden A., Weiss B., Stables J.P., Ho K.H., Ebinger G., Collingridge G.L., Lodge D., and Michotte Y. Antagonists of GLU(K5)-containing kainate receptors prevent pilocarpine-induced limbic seizures. Nat Neurosci 5 (2002) 796-804
72. Traub R.D., and Jefferys J.G. Are there unifying principles underlying the generation of epileptic afterdischarges in vitro?. Prog Brain Res 102 (1994) 383-394
73. Wade J.V., Samson F.E., Nelson S.R., and Pazdernik T.L. Changes in extracellular amino acids during soman- and kainic acid-induced seizures. J Neurochem 49 (1987) 645-650
74. Washburn M.S., and Moises H.C. Muscarinic responses of rat basolateral amygdaloid neurons recorded in vitro. J Physiol 449 (1992) 121-154
75. White L.E., and Price J.L. The functional anatomy of limbic status epilepticus in the rat. I. Patterns of 14C-2-deoxyglucose uptake and Fos immunocytochemistry. J Neurosci 13 (1993) 4787-4809
76. White L.E., and Price J.L. The functional anatomy of limbic status epilepticus in the rat. II. The effects of focal deactivation. J Neurosci 13 (1993) 4810-4830
77. Williamson A.M., and Sarvey J.M. Effects of cholinesterase inhibitors on evoked responses in field CA1 of the rat hippocampus. J Pharmacol Exp Ther 235 (1985) 448-455
78. Womble M.D., and Moises H.C. Muscarinic inhibition of M-current and a potassium leak conductance in neurones of the rat basolateral amygdala. J Physiol 457 (1992) 93-114
79. Yajeya J., De La Fuente A., Criado J.M., Bajo V., Sánchez-Riolobos A., and Heredia M. Muscarinic agonist carbachol depresses excitatory synaptic transmission in the rat basolateral amygdala in vitro. Synapse 38 (2000) 151-160