Multiple kainic acid seizures in the immature and adult brain: Ictal manifestations and long-term effects on learning and memory

Epilepsia

Volumn 38, Issue 11, 1997, Pages 1157-1166

  Sarkisian, Matthew R ^a   Tandon, Pushpa ^a   Liu, Zhao ^a   Yang, Yili ^a   Hori, Ariyuki ^a   Holmes, Gregory L ^a   Stafstrom, Carl E ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

Immature brain; Kainic acid; Learning; Seizures; Water maze

Indexed keywords

KAINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROCARDIOGRAM; EPILEPTIC DISCHARGE; LATENT PERIOD; LEARNING DISORDER; MALE; MAZE TEST; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; RAT; SEIZURE;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; KAINIC ACID; MALE; MAZE LEARNING; MEMORY; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SPATIAL BEHAVIOR;

EID: 0030808854     PISSN: 00139580     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1528-1157.1997.tb01211.x     Document Type: Article

References (54)

1. Nadler JV. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 1981;29:2031-42.
2. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985;14:375-403.
3. Albala BJ, Moshe SL, Okada R. Kainic acid-induced seizures: A developmental study. Dev Brain Res 1984;13:139-48.
4. Nitecka L, Tremblay E, Charton G, Bouillot JP, Berger ML, BenAri Y. Maturation of kainic acid seizure-brain damage syndrome in the rat: II. Histopathological sequelae. Neuroscience 1984;13: 1073-94.
5. Sperber EF, Haas KZ, Stanton PK, Moshé SL. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Dev Brain Res 1991;60:88-93.
6. Stafstrom CE, Holmes GL, Chronopoulos A, Thurber S. Thompson JL. Age-dependent cognitive and behavioral deficits following kainic acid-induced seizures. Epilepsia 1993;34:420-32.
7. Thurber S, Chronopoulos A, Stafstrom CE, Holmes GL. Behavioral effects of continuous hippocampal stimulation in the developing rat. Dev Brain Res 1992;68:35-40.
8. Liu Z, Gatt A, Werner SJ, Mikati MA, Holmes GL. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 1994;19:191-204.
9. Stafstrom CE, Thompson JL, Holmes GL. Kainic acid seizures in the developing brain: Status epilepticus and spontaneous recurrent seizures. Dev Brain Res 1992;65:227-36.
10. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. Place navigation is impaired in rats with hippocampal lesions. Nature 1982;297: 681-3.
11. Sutherland RJ, Whishaw IQ, Kolb B. A behavioral analysis of spatial localization following electrolytic, kainate or colchicine-induced damage to the hippocampus. Behav Brain Res 1983;7: 133-53.
12. Sherwood NM, Timiras PS. A Stereotaxic Atlas of the Developing Rat Brain. Berkeley, CA: University of California Press, 1970.
13. Tremblay E, Nitecka L, Berger ML, Ben-Ari Y. Maturation of kainic acid seizure brain damage syndrome in the rat: I. Clinical, electrographic and metabolic observations. Neuroscience 1984;13: 1051-72.
14. Sperk G. Kainic acid seizures in the rat. Progr Neurobiol 1994; 42:1-32.
15. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997;17:3727-38.
16. Holmes GL, Thompson JL. Effects of serial administration of kainic acid on the developing brain. Neuropharmacology 1988;27: 209-12.
17. Vosu H, Wise RA. Cholinergic seizure kindling in the rat: Comparison of caudate, amygdala and hippocampus. Behav Biol 1975; 13:491-4.
18. Diehl RG, Smialowski A, Gotwo T. Development and persistence of kindled seizures after repeated injections of pentylenetetrazole in rats and guinea pigs. Epilepsia 1984;25:506-10.
19. Ribak CE, Navetta MS. An immature mossy fiber innervation of hilar neurons may explain their resistance to kainate-induced cell death in 15-day-old rats. Dev Brain Res 1994;79:47-62.
20. Miller LP, Johnson AE, Gelhard RE, Insel TR. The ontogeny of excitatory amino acid receptors in rat forebrain: II. Kainic acid receptors. Neuroscience 1990;35:45-51.
21. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, Henley JM. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 1996;379:78-81.
22. Liu Z, Stafstrom CE, Sarkisian M, et al. Age-dependent effects of glutamate toxicity in the hippocampus. Dev Brain Res 1996;97: 178-84.
23. Gould E, Cameron HA, McEwen BS. Blockade of NMDA receptors increases cell death and birth in developing rat dentate gyrus. J Comp Neurol 1994;340:551-65.
24. Balazs R, Jorgensen OS, Hack N. N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 1988;27:437-51.
25. Yan GM, Ni B, Weller M, Wood KA, Paul SM. Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res 1994;656:43-52.
26. Bambrick LL, Yarowski PL, Krueger BK. Glutamate as a hippocampal neuronal survival factor: An inherited defect in the trisomy 16 mouse. Proc Natl Acad Sci USA 1995;92:9692-6.
27. Suzuki F, Junier M-P, Guilhem D, Sorenson J-C, Onteniente B. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience 1995;64:665-74.
28. A receptor subunit mRNA concentrations following chronic lorazepam administration. Br J Pharmacol 1991;103:1285-7.
29. Temple A. Visualization of mu opiate receptor downregulation following morphine treatment in neonatal rat brain. Brain Res 1991;64:19-26.
30. B receptors. J Neurosci 1996;16:4250-60.
31. Bushnell PJ, Padilla SS, Ward T, Pope CN, Olszyk VB. Behavioral and neurochemical changes in rats dosed repeatedly with diisopropylfluorophosphate. J Pharmacol Exp Ther 1991;256:741-50.
32. Clement JG. Effect of a single dose of acetylcholinesterase inhibitor on oxotremorine-and nicotine-induced hypothermia in mice. Pharmacol Biochem Behav 1991;39:929-34.
33. Tandon P, Sarkisian MR, Stafstrom CE, Yang Y, Holmes GL. Repeated exposure to kainic acid in developing rats does not cause repeated seizures, neuronal loss or behavioral deficits later in life. Epilepsia 1996;37[Suppl. 5]:66.
34. Ballarin M, Ernfors P, Lindefors N, Persson H. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp Neurol 1991;114:35-43.
35. Riva MA, Gale K, Mocchetti I. Basic fibroblast growth factor mRNA increases in specific brain regions following convulsive seizures. Molec Brain Res 1992;15:311-8.
36. Follesa P, Gale K, Mocchetti I. Regional and temporal pattern of expression of nerve growth factor and basic fibroblast growth factor mRNA in rat brain following electroconvulsive shock. Exp Neurol 1994;127:37-44.
37. Dugich-Djordjevic MM, Tocco G, Willoughby DA et al. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron 1992;8:1127-38.
38. Larmet Y, Reibel S, Carnahan J, Nawa H, Marescaux C, Depaulis A. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport 1995;6:1937-41.
39. Kaisho Y, Shintani A, Ono Y, Kato K, Igarashi K. Regional expression of the nerve growth factor gene family in rat brain during development. Biochem Biophys Res Commun 1991;174:379-85.
40. Nonner D, Barrett JN. Changes in the response of cultured septal cholinergic neurons to nerve growth factor exposure and deprivation during the first postnatal month. Dev Brain Res 1994;79:219-28.
41. Zhou J, Bradford HF, Stern G. The stimulatory effect of brain-derived neurotrophic factor on dopaminergic phenotype expression of embryonic rat cortical neurons in vitro. Dev Brain Res 1994; 81:318-24.
42. Thoenen H. Neurotrophins and neuronal plasticity. Science 1995; 270:593-8.
43. Zhou X-F, Rush RA. Sympathetic neurons in neonatal rats require endogenous neurotrophin-3 for survival. J Neurosci 1995;15: 6521-30.
44. Zafra F, Hengerer B, Leibrock J, Thoenen H, Lindholm D. Activity-dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by nonNMDA glutamate receptors. EMBO J 1990;9:3545-50.
45. Wetmore C, Olson L, Bean AJ. Regulation of brain derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J Neurosci 1994;14:1688-700.
46. Tandon P, Sarkisian M, Yang Y, et al. The neuroprotective role of BDNF in seizure induced neuronal loss during development. Neurology 1997;48:A151.
47. Kelly ME, McIntyre DC. Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Res 1994;634:245-56.
48. Najm I, Schreiber SS, Bruce A, Tocco G, Baudry M. A short episode of seizure activity protects CA3 neurons from prolonged seizure activity-induced death. Soc Neurosci Abstr 1992;18:1146.
49. Holmes GL. Do seizures cause brain damage? Epilepsia 1991;32[Suppl. 5]:S14-28.
50. Frank JE, Schwartzkroin PA. Immature rabbit hippocampus is damaged by systemic but not intraventricular kainic acid. Dev Brain Res 1984;13:219-27.
51. Babb TL, Pereira-Leite J, Mathern GW, Pretorius JK. Kainic acid-induced hippocampal seizures in rats: Comparisons of acute and chronic seizures using intrahippocampal versus systemic injections. Ital J Neurol Sci 1995;16:39-44.
52. Neill JC, Liu Z, Sarkisian M, et al. Recurrent seizures in immature rats: Effect on auditory and visual discrimination. Dev Brain Res 1996;95:283-92.
53. Moshé SL, Albala BJ. Kindling in developing rats: Persistence of seizures into adulthood. Dev Brain Res 1982;4:67-71.
54. Moshé SL, Albala BJ. Maturational changes in postictal refractoriness and seizure susceptibility in developing rats. Ann Neurol 1983;13:552-7.