Skip to main content
The Yale Journal of Biology and Medicine logoLink to The Yale Journal of Biology and Medicine
. 1987 May-Jun;60(3):255–272.

Experimental models of chronic focal epilepsy: a critical review of four models.

E D Louis, P D Williamson, T M Darcey
PMCID: PMC2590100  PMID: 3111109

Abstract

A number of experimental (i.e., animal) models have been developed to induce chronic focal epilepsy. Three of the most commonly employed are the alumina cream, kainic acid, and the electrical kindling techniques. A fourth approach involving the application of minute quantities of tetanus toxin to discrete brain sites, although relatively under-utilized, may be favorably compared to the aforementioned models.

Full text

PDF
255

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Araki H., Aihara H., Watanabe S., Ohta H., Yamamoto T., Ueki S. The role of noradrenergic and serotonergic systems in the hippocampal kindling effect. Jpn J Pharmacol. 1983 Feb;33(1):57–64. doi: 10.1254/jjp.33.57. [DOI] [PubMed] [Google Scholar]
  2. BLUM B., LIBAN E. Experimental basotemporal epilepsy in the cat: discrete epileptogenic lesions produced in the hippocampus or amygdaloid by tungstic acid. Neurology. 1960 Jun;10:546–554. doi: 10.1212/wnl.10.6.546. [DOI] [PubMed] [Google Scholar]
  3. BLUM B., MAGNES J., BENTAL E., LIBAN E. Electroencephalographic studies in cats with experimentally produced hippocampal epilepsy. Electroencephalogr Clin Neurophysiol. 1961 Jun;13:340–353. doi: 10.1016/0013-4694(61)90002-5. [DOI] [PubMed] [Google Scholar]
  4. BROOKS V. B., ASANUMA H. Action of tetanus toxin in the cerebral cortex. Science. 1962 Aug 31;137(3531):674–676. doi: 10.1126/science.137.3531.674-a. [DOI] [PubMed] [Google Scholar]
  5. Ben-Ari Y., Lagowska J., Tremblay E., Le Gal La Salle G. A new model of focal status epilepticus: intra-amygdaloid application of kainic acid elicits repetitive secondarily generalized convulsive seizures. Brain Res. 1979 Mar 9;163(1):176–179. doi: 10.1016/0006-8993(79)90163-x. [DOI] [PubMed] [Google Scholar]
  6. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 1985 Feb;14(2):375–403. doi: 10.1016/0306-4522(85)90299-4. [DOI] [PubMed] [Google Scholar]
  7. Ben-Ari Y., Tremblay E., Ottersen O. P. Injections of kainic acid into the amygdaloid complex of the rat: an electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience. 1980;5(3):515–528. doi: 10.1016/0306-4522(80)90049-4. [DOI] [PubMed] [Google Scholar]
  8. Ben-Ari Y., Tremblay E., Ottersen O. P., Meldrum B. S. The role of epileptic activity in hippocampal and "remote" cerebral lesions induced by kainic acid. Brain Res. 1980 Jun 2;191(1):79–97. doi: 10.1016/0006-8993(80)90316-9. [DOI] [PubMed] [Google Scholar]
  9. Ben-Ari Y., Tremblay E., Ottersen O. P., Naquet R. Evidence suggesting secondary epileptogenic lesion after kainic acid: pre treatment with diazepam reduces distant but not local brain damage. Brain Res. 1979 Apr 13;165(2):362–365. doi: 10.1016/0006-8993(79)90571-7. [DOI] [PubMed] [Google Scholar]
  10. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., Naquet R. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience. 1981;6(7):1361–1391. doi: 10.1016/0306-4522(81)90193-7. [DOI] [PubMed] [Google Scholar]
  11. CARREA R., LANARI A. Chronic effect of tetanus toxin applied locally to the cerebral cortex of the dog. Science. 1962 Aug 3;137(3527):342–343. doi: 10.1126/science.137.3527.342. [DOI] [PubMed] [Google Scholar]
  12. Cavalheiro E. A., Riche D. A., Le Gal La Salle G. Long-term effects of intrahippocampal kainic acid injection in rats: a method for inducing spontaneous recurrent seizures. Electroencephalogr Clin Neurophysiol. 1982 Jun;53(6):581–589. doi: 10.1016/0013-4694(82)90134-1. [DOI] [PubMed] [Google Scholar]
  13. Cepeda C., Tanaka T., Riche D., Naquet R. Limbic status epilepticus: behaviour and sleep alterations after intra-amygdaloid kainic acid microinjections in Papio Papio baboons. Electroencephalogr Clin Neurophysiol. 1982 Dec;54(6):603–613. doi: 10.1016/0013-4694(82)90114-6. [DOI] [PubMed] [Google Scholar]
  14. Curtis D. R., Felix D., Game C. J., McCulloch R. M. Tetanus toxin and the synaptic release of GABA. Brain Res. 1973 Mar 15;51:358–362. doi: 10.1016/0006-8993(73)90389-2. [DOI] [PubMed] [Google Scholar]
  15. FAETH W. H., WALKER A. E., KAPLAN A. D., WARNER W. A. Threshold studies on production of experimental epilepsy with alumina cream. Proc Soc Exp Biol Med. 1955 Mar;88(3):329–331. doi: 10.3181/00379727-88-21579. [DOI] [PubMed] [Google Scholar]
  16. FAETH W. H., WALKER A. E. Studies on effect of the injection of alumina (aluminum oxide) cream into the basal ganglia. AMA Arch Neurol Psychiatry. 1957 Dec;78(6):562–567. doi: 10.1001/archneurpsyc.1957.02330420022003. [DOI] [PubMed] [Google Scholar]
  17. Feria-Velasco A., Olivares N., Rivas F., Velasco M., Velasco F. Alumina cream-induced focal motor epilepsy in cats. IV. Thickness and cellularity of layers in the perilesional motor cortex. Arch Neurol. 1980 May;37(5):287–290. doi: 10.1001/archneur.1980.00500540065008. [DOI] [PubMed] [Google Scholar]
  18. French E. D., Aldinio C., Schwarcz R. Intrahippocampal kainic acid, seizures and local neuronal degeneration: relationships assessed in unanesthetized rats. Neuroscience. 1982 Oct;7(10):2525–2536. doi: 10.1016/0306-4522(82)90212-3. [DOI] [PubMed] [Google Scholar]
  19. GASTAUT H., NAQUET R., MEYER A., CAVANAGH J. B., BECK E. Experimental psychomotor epilepsy in the cat; electro-clinical and anatomo-pathological correlations. J Neuropathol Exp Neurol. 1959 Apr;18(2):270–293. doi: 10.1097/00005072-195904000-00004. [DOI] [PubMed] [Google Scholar]
  20. Goddard G. V. Development of epileptic seizures through brain stimulation at low intensity. Nature. 1967 Jun 3;214(5092):1020–1021. doi: 10.1038/2141020a0. [DOI] [PubMed] [Google Scholar]
  21. Goddard G. V., McIntyre D. C., Leech C. K. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol. 1969 Nov;25(3):295–330. doi: 10.1016/0014-4886(69)90128-9. [DOI] [PubMed] [Google Scholar]
  22. Harris A. B., Lockard J. S. Absence of seizures or mirror foci in experimental epilepsy after excision of alumina and astrogliotic scar. Epilepsia. 1981 Feb;22(1):107–122. doi: 10.1111/j.1528-1157.1981.tb04337.x. [DOI] [PubMed] [Google Scholar]
  23. Harris A. B. Ultrastructure and histochemistry of alumina in cortex. Exp Neurol. 1973 Jan;38(1):33–63. doi: 10.1016/0014-4886(73)90006-x. [DOI] [PubMed] [Google Scholar]
  24. Hauser W. A., Kurland L. T. The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia. 1975 Mar;16(1):1–66. doi: 10.1111/j.1528-1157.1975.tb04721.x. [DOI] [PubMed] [Google Scholar]
  25. KOPELOFF L. M., CHUSID J. G., KOPELOFF N. Chronic experimental epilepsy in Macaca mulatta. Neurology. 1954 Mar;4(3):218–227. doi: 10.1212/wnl.4.3.218. [DOI] [PubMed] [Google Scholar]
  26. KOPELOFF L. M., CHUSID J. G., KOPELOFF N. Epilepsy in Macaca mulatta after cortical or intracerebral alumina. AMA Arch Neurol Psychiatry. 1955 Nov;74(5):523–526. doi: 10.1001/archneurpsyc.1955.02330170057010. [DOI] [PubMed] [Google Scholar]
  27. KOPELOFF N., CHUSID J. G., KOPELOFF L. M. Epilepsy produced in Macaca mulatta with commercial aluminum hydroxide. Electroencephalogr Clin Neurophysiol. 1954 May;6(2):303–306. doi: 10.1016/0013-4694(54)90032-2. [DOI] [PubMed] [Google Scholar]
  28. KOPELOFF N., WHITTIER J. R., PACELLA B. L., KOPELOFF L. M. The epileptogenic effect of subcortical alumina cream in the rhesus monkey. Electroencephalogr Clin Neurophysiol. 1950 May;2(2):163–168. doi: 10.1016/0013-4694(50)90029-0. [DOI] [PubMed] [Google Scholar]
  29. Leech C. K., McIntyre D. C. Kindling rates in inbred mice: an analog to learning? Behav Biol. 1976 Apr;16(4):439–452. doi: 10.1016/s0091-6773(76)91603-5. [DOI] [PubMed] [Google Scholar]
  30. Lockard J. S., Congdon W. C., DuCharme L. L., Huntsman B. J. Prophylaxis with diphenylhydantoin and phenobarbital and alumina-gel monkey model. I. Twelve months of treatment: seizure, EEG, blood, and behavioral data. Epilepsia. 1976 Mar;17(1):37–47. doi: 10.1111/j.1528-1157.1976.tb03380.x. [DOI] [PubMed] [Google Scholar]
  31. Lothman E. W., Collins R. C., Ferrendelli J. A. Kainic acid-induced limbic seizures: electrophysiologic studies. Neurology. 1981 Jul;31(7):806–812. doi: 10.1212/wnl.31.7.806. [DOI] [PubMed] [Google Scholar]
  32. Lothman E. W., Collins R. C. Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res. 1981 Aug 10;218(1-2):299–318. doi: 10.1016/0006-8993(81)91308-1. [DOI] [PubMed] [Google Scholar]
  33. MORRELL F., BRADLEY W., PTASHNE M. Effect of drugs on discharge characteristics of chronic epileptogenic lesions. Neurology. 1959 Jul;9(7):492–498. doi: 10.1212/wnl.9.7.492. [DOI] [PubMed] [Google Scholar]
  34. MORRELL F., ROBERTS L., JASPER H. H. Effect of focal epileptogenic lesions and their ablation upon conditioned electrical responses of the brain in the monkey. Electroencephalogr Clin Neurophysiol. 1956 May;8(2):217–236. doi: 10.1016/0013-4694(56)90115-8. [DOI] [PubMed] [Google Scholar]
  35. Mayanagi Y. Alumina cream-induced temporal lobe epilepsy in the monkey as an experimental model. Folia Psychiatr Neurol Jpn. 1979;33(3):457–462. doi: 10.1111/j.1440-1819.1979.tb00787.x. [DOI] [PubMed] [Google Scholar]
  36. Mayanagi Y. Experimental studies on the pathogensis of temporal lobe epilepsy. Folia Psychiatr Neurol Jpn. 1976;30(3):415–424. doi: 10.1111/j.1440-1819.1976.tb02278.x. [DOI] [PubMed] [Google Scholar]
  37. Mayanagi Y., Walker A. E. Experimental temporal lobe epilepsy. Brain. 1974 Sep;97(3):423–446. doi: 10.1093/brain/97.1.423. [DOI] [PubMed] [Google Scholar]
  38. McGeer P. L., McGeer E. G., Campbell J. J. Rotatory effects of intracerebral tetanus toxin injections. Exp Neurol. 1980 Feb;67(2):363–367. doi: 10.1016/0014-4886(80)90235-6. [DOI] [PubMed] [Google Scholar]
  39. McNamara J. O., Byrne M. C., Dasheiff R. M., Fitz J. G. The kindling model of epilepsy: a review. Prog Neurobiol. 1980;15(2):139–159. doi: 10.1016/0301-0082(80)90006-4. [DOI] [PubMed] [Google Scholar]
  40. Mellanby J., George G., Robinson A., Thompson P. Epileptiform syndrome in rats produced by injecting tetanus toxin into the hippocampus. J Neurol Neurosurg Psychiatry. 1977 Apr;40(4):404–414. doi: 10.1136/jnnp.40.4.404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mellanby J., George G. Tetanus toxin and experimental epilepsy in rats. Adv Cytopharmacol. 1979;3:401–408. [PubMed] [Google Scholar]
  42. Mellanby J., Hawkins C., Mellanby H., Rawlins J. N., Impey M. E. Tetanus toxin as a tool for studying epilepsy. J Physiol (Paris) 1984;79(4):207–215. [PubMed] [Google Scholar]
  43. Menini C., Meldrum B. S., Riche D., Silva-Comte C., Stutzmann J. M. Sustained limbic seizures induced by intraamygdaloid kainic acid in the baboon: Symptomatology and neuropathological consequences. Ann Neurol. 1980 Nov;8(5):501–509. doi: 10.1002/ana.410080507. [DOI] [PubMed] [Google Scholar]
  44. Morrell F., Tsuru N. Kindling in the frog: development of spontaneous epileptiform activity. Electroencephalogr Clin Neurophysiol. 1976 Jan;40(1):1–11. doi: 10.1016/0013-4694(76)90174-7. [DOI] [PubMed] [Google Scholar]
  45. Mutani R. Cobalt experimental hippocampal epilepsy in the cat. Epilepsia. 1967 Dec;8(4):223–240. doi: 10.1111/j.1528-1157.1967.tb04439.x. [DOI] [PubMed] [Google Scholar]
  46. Muñoz C., Grossman S. P. Some behavioral effects of selective neuronal depletion by kainic acid in the dorsal hippocampus of rats. Physiol Behav. 1980 Oct;25(4):581–587. doi: 10.1016/0031-9384(80)90125-0. [DOI] [PubMed] [Google Scholar]
  47. Nadler J. V. Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 1981 Nov 16;29(20):2031–2042. doi: 10.1016/0024-3205(81)90659-7. [DOI] [PubMed] [Google Scholar]
  48. Nadler J. V., Perry B. W., Cotman C. W. Intraventricular kainic acid preferentially destroys hippocampal pyramidal cells. Nature. 1978 Feb 16;271(5646):676–677. doi: 10.1038/271676a0. [DOI] [PubMed] [Google Scholar]
  49. Nadler J. V., Shelton D. L., Perry B. W., Cotman C. W. Regional distribution of [3H]kainic acid after intraventricular injection. Life Sci. 1980 Jan 14;26(2):133–138. doi: 10.1016/0024-3205(80)90057-0. [DOI] [PubMed] [Google Scholar]
  50. Nelson M. F., Zaczek R., Coyle J. T. Effects of sustained seizures produced by intrahippocampal injection of kainic acid on noradrenergic neurons: evidence for local control of norepinephrine release. J Pharmacol Exp Ther. 1980 Sep;214(3):694–702. [PubMed] [Google Scholar]
  51. Nitecka L., Tremblay E., Charton G., Bouillot J. P., Berger M. L., Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. II. Histopathological sequelae. Neuroscience. 1984 Dec;13(4):1073–1094. doi: 10.1016/0306-4522(84)90289-6. [DOI] [PubMed] [Google Scholar]
  52. Olney J. W., Fuller T. A., de Gubareff T. Kainate-like neurotoxicity of folates. Nature. 1981 Jul 9;292(5819):165–167. doi: 10.1038/292165a0. [DOI] [PubMed] [Google Scholar]
  53. Olney J. W., Fuller T., de Gubareff T. Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res. 1979 Oct 26;176(1):91–100. doi: 10.1016/0006-8993(79)90872-2. [DOI] [PubMed] [Google Scholar]
  54. Olney J. W., Rhee V., Ho O. L. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 1974 Sep 13;77(3):507–512. doi: 10.1016/0006-8993(74)90640-4. [DOI] [PubMed] [Google Scholar]
  55. Papavasilious P. S., Kutt H., Miller S. T., Rosal V., Wang Y. Y., Aronson R. B. Seizure disorders and trace metals: manganese tissue levels in treated epileptics. Neurology. 1979 Nov;29(11):1466–1473. doi: 10.1212/wnl.29.11.1466. [DOI] [PubMed] [Google Scholar]
  56. Pei Y., Zhao D., Huang J., Cao L. Zinc-induced seizures: a new experimental model of epilepsy. Epilepsia. 1983 Apr;24(2):169–176. doi: 10.1111/j.1528-1157.1983.tb04876.x. [DOI] [PubMed] [Google Scholar]
  57. Pisa M., Sanberg P. R., Corcoran M. E., Fibiger H. C. Spontaneously recurrent seizures after intracerebral injections of kainic acid in rat: a possible model of human temporal lobe epilepsy. Brain Res. 1980 Nov 3;200(2):481–487. doi: 10.1016/0006-8993(80)90938-5. [DOI] [PubMed] [Google Scholar]
  58. Racine R. J. Modification of seizure activity by electrical stimulation. I. After-discharge threshold. Electroencephalogr Clin Neurophysiol. 1972 Mar;32(3):269–279. doi: 10.1016/0013-4694(72)90176-9. [DOI] [PubMed] [Google Scholar]
  59. Racine R. J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972 Mar;32(3):281–294. doi: 10.1016/0013-4694(72)90177-0. [DOI] [PubMed] [Google Scholar]
  60. Remler M. P., Marcussen W. H. Systemic focal epileptogenesis. Epilepsia. 1986 Jan-Feb;27(1):35–42. doi: 10.1111/j.1528-1157.1986.tb03498.x. [DOI] [PubMed] [Google Scholar]
  61. Rial R. V., González J. Kindling effect in the reptilian brain: motor and electrographic manifestations. Epilepsia. 1978 Dec;19(6):581–589. doi: 10.1111/j.1528-1157.1978.tb05038.x. [DOI] [PubMed] [Google Scholar]
  62. SERVIT Z., STERC J. Audiogenic epileptic seizures evoked in rats by artificial epileptogenic foci. Nature. 1958 May 24;181(4621):1475–1476. doi: 10.1038/1811475b0. [DOI] [PubMed] [Google Scholar]
  63. STAMM J. S., PRIBRAM K. H. Effects of epileptogenic lesions of inferotemporal cortex on learning and retention in monkeys. J Comp Physiol Psychol. 1961 Dec;54:614–618. doi: 10.1037/h0042752. [DOI] [PubMed] [Google Scholar]
  64. SVENNERHOLM L. CHROMATOGRAPHIC SEPARATION OF HUMAN BRAIN GANGLIOSIDES. J Neurochem. 1963 Sep;10:613–623. doi: 10.1111/j.1471-4159.1963.tb08933.x. [DOI] [PubMed] [Google Scholar]
  65. Scherer-Singler U., McGeer E. G. Distribution and persistence of kainic acid in brain. Life Sci. 1979 Mar 12;24(11):1015–1022. doi: 10.1016/0024-3205(79)90321-7. [DOI] [PubMed] [Google Scholar]
  66. Schwarcz R., Coyle J. T. Neurochemical sequelae of kainate injections in corpus striatum and substantia nigra of the rat. Life Sci. 1977 Feb 1;20(3):431–436. doi: 10.1016/0024-3205(77)90384-8. [DOI] [PubMed] [Google Scholar]
  67. Schwarcz R., Zaczek R., Coyle J. T. Microinjection of kainic acid into the rat hippocampus. Eur J Pharmacol. 1978 Aug 1;50(3):209–220. doi: 10.1016/0014-2999(78)90353-9. [DOI] [PubMed] [Google Scholar]
  68. Schwob J. E., Fuller T., Price J. L., Olney J. W. Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: a histological study. Neuroscience. 1980;5(6):991–1014. doi: 10.1016/0306-4522(80)90181-5. [DOI] [PubMed] [Google Scholar]
  69. Shinozaki H., Konishi S. Actions of several anthelmintics and insecticides on rat cortical neurones. Brain Res. 1970 Dec 1;24(2):368–371. doi: 10.1016/0006-8993(70)90122-8. [DOI] [PubMed] [Google Scholar]
  70. Soloway S. S., Williamson P. D., Spencer D. D., Mattson R. H. Surgery for epilepsy: role of depth electroencephalography. Conn Med. 1980 Feb;44(2):70–75. [PubMed] [Google Scholar]
  71. Soper H. V., Strain G. M., Babb T. L., Lieb J. P., Crandall P. H. Chronic alumina temporal lobe seizures in monkeys. Exp Neurol. 1978 Oct;62(1):99–121. doi: 10.1016/0014-4886(78)90044-4. [DOI] [PubMed] [Google Scholar]
  72. Sperk G., Lassmann H., Baran H., Kish S. J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience. 1983 Dec;10(4):1301–1315. doi: 10.1016/0306-4522(83)90113-6. [DOI] [PubMed] [Google Scholar]
  73. Tanaka T., Kaijima M., Daita G., Ohgami S., Yonemasu Y., Riche D. Electroclinical features of kainic acid-induced status epilepticus in freely moving cats. Microinjection into the dorsal hippocampus. Electroencephalogr Clin Neurophysiol. 1982 Sep;54(3):288–300. doi: 10.1016/0013-4694(82)90178-x. [DOI] [PubMed] [Google Scholar]
  74. Tremblay E., Nitecka L., Berger M. L., Ben-Ari Y. Maturation of kainic acid seizure-brain damage syndrome in the rat. I. Clinical, electrographic and metabolic observations. Neuroscience. 1984 Dec;13(4):1051–1072. doi: 10.1016/0306-4522(84)90288-4. [DOI] [PubMed] [Google Scholar]
  75. Tremblay E., Ottersen O. P., Rovira C., Ben-Ari Y. Intra-amygdaloid injections of kainic acid: regional metabolic changes and their relation to the pathological alterations. Neuroscience. 1983;8(2):299–315. doi: 10.1016/0306-4522(83)90068-4. [DOI] [PubMed] [Google Scholar]
  76. Velasco M., Velasco F., Estrada-Villanueva F., Olvera A. Alumina cream-induced focal motor epilepsy in cats. 1. Lesion size and temporal course. Epilepsia. 1973 Mar;14(1):3–14. doi: 10.1111/j.1528-1157.1973.tb03937.x. [DOI] [PubMed] [Google Scholar]
  77. Velasco M., Velasco F., Lozoya X., Feria A., Gonzàlez Licea A. Alumina cream-induced focal motor epilepsy in cats. 2. Thickness and cellularity of cerebral cortex adjacent to epileptogenic lesions. Epilepsia. 1973 Mar;14(1):15–27. doi: 10.1111/j.1528-1157.1973.tb03938.x. [DOI] [PubMed] [Google Scholar]
  78. Velasco M., Velasco F., Márquez I., Cepeda C., Estrada-Villanueva F. Alumina cream induced focal motor epilepsy in cats. VI. Excision of the perilesional cortex. Electroencephalogr Clin Neurophysiol. 1985 Jun;60(6):548–557. doi: 10.1016/0013-4694(85)91116-2. [DOI] [PubMed] [Google Scholar]
  79. Velasco M., Velasco F., Pacheco M. T., Azpeitia E., Saldívar L., Estrada-Villanueva F. Alumina cream-induced focal motor epilepsy in cats. Part 5. Excision and transplant of the epileptogenic granuloma. Epilepsia. 1984 Dec;25(6):752–758. doi: 10.1111/j.1528-1157.1984.tb03487.x. [DOI] [PubMed] [Google Scholar]
  80. WESTRUM L. E., WHITE L. E., Jr, WARD A. A., Jr MORPHOLOGY OF THE EXPERIMENTAL EPILEPTIC FOCUS. J Neurosurg. 1964 Dec;21:1033–1046. doi: 10.3171/jns.1964.21.12.1033. [DOI] [PubMed] [Google Scholar]
  81. Wada J. A., Mizoguchi T., Komai S. Kindling epileptogenesis in orbital and mesial frontal cortical areas of subhuman primates. Epilepsia. 1985 Sep-Oct;26(5):472–479. doi: 10.1111/j.1528-1157.1985.tb05683.x. [DOI] [PubMed] [Google Scholar]
  82. Wada J. A., Sato M., Corcoran M. E. Persistent seizure susceptibility and recurrent spontaneous seizures in kindled cats. Epilepsia. 1974 Dec;15(4):465–478. doi: 10.1111/j.1528-1157.1974.tb04022.x. [DOI] [PubMed] [Google Scholar]
  83. Wauquier A., Ashton D., Melis W. Behavioral analysis of amygdaloid kindling in beagle dogs and the effects of clonazepam, diazepam, phenobarbital, diphenylhydantoin, and flunarizine on seizure manifestation. Exp Neurol. 1979 Jun;64(3):579–586. doi: 10.1016/0014-4886(79)90233-4. [DOI] [PubMed] [Google Scholar]
  84. Wuerthele S. M., Lovell K. L., Jones M. Z., Moore K. E. A histological study of kainic acid-induced lesions in the rat brain. Brain Res. 1978 Jun 30;149(2):489–497. doi: 10.1016/0006-8993(78)90491-2. [DOI] [PubMed] [Google Scholar]
  85. YOUMANS J. R. Experimental production of seizures in the Macaque by temporal lobe lesions. Neurology. 1956 Mar;6(3):179–186. doi: 10.1212/wnl.6.3.179. [DOI] [PubMed] [Google Scholar]
  86. Zaczek R., Nelson M. F., Coyle J. T. Effects of anaesthetics and anticonvulsants on the action of kainic acid in the rat hippocampus. Eur J Pharmacol. 1978 Dec 1;52(3-4):323–327. doi: 10.1016/0014-2999(78)90285-6. [DOI] [PubMed] [Google Scholar]
  87. Zaczek R., Simonton S., Coyle J. T. Local and distant neuronal degeneration following intrastriatal injection of kainic acid. J Neuropathol Exp Neurol. 1980 May;39(3):245–264. doi: 10.1097/00005072-198005000-00003. [DOI] [PubMed] [Google Scholar]
  88. van Heyningen S. Tetanus toxin. Pharmacol Ther. 1980;11(1):141–157. doi: 10.1016/0163-7258(80)90070-4. [DOI] [PubMed] [Google Scholar]

Articles from The Yale Journal of Biology and Medicine are provided here courtesy of Yale Journal of Biology and Medicine

RESOURCES