Animal models of status epilepticus and temporal lobe epilepsy: a narrative review

References

Anderson, A.E., Hrachovy, R.A., Antalffy, B.A., Armstrong, D.L., and Swann, J.W. (1999). A chronic focal epilepsy with mossy fiber sprouting follows recurrent seizures induced by intrahippocampal tetanus toxin injection in infant rats. Neuroscience 92, 73–82.10.1016/S0306-4522(98)00746-5Suche in Google Scholar

Babb, T.L. (1999). Synaptic reorganizations in human and rat hippocampal epilepsy. Adv. Neurol. 79, 763–779.Suche in Google Scholar

Bagetta, G., Corasaniti, M.T., Nistico, G., and Bowery, N.G. (1990). Behavioural and neuropathological effects produced by tetanus toxin injected into the hippocampus of rats. Neuropharmacology 29, 765–770.10.1016/0028-3908(90)90130-JSuche in Google Scholar

Baldelli, E., Leo, G., Andreoli, N., Fuxe, K., Biagini, G., and Agnati, L.F. (2010). Homocysteine potentiates seizures and cell loss induced by pilocarpine treatment. Neuromol. Med. 12, 248–259.10.1007/s12017-009-8110-1Suche in Google Scholar

Baram, T.Z., Gerth, A., and Schultz, L. (1997). Febrile seizures: an appropriate-aged model suitable for long-term studies. Brain Res. Dev. Brain Res. 98, 265–270.10.1016/S0165-3806(96)00190-3Suche in Google Scholar

Barnes, G., Puranam, R.S., Luo, Y., and McNamara, J.O. (2003). Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus 13, 1–20.10.1002/hipo.10041Suche in Google Scholar

Ben-Ari, Y. and Cossart, R. (2000). Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23, 580–587.10.1016/S0166-2236(00)01659-3Suche in Google Scholar

Ben-Ari, Y., Tremblay, E., Riche, D., Ghilini, G., and Naquet, R. (1981). 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 6, 1361–1391.10.1016/0306-4522(81)90193-7Suche in Google Scholar

Bertram, E.H. and Lothman, E.W. (1990). NMDA receptor antagonists and limbic status epilepticus: a comparison with standard anticonvulsants. Epilepsy Res. 5, 177–184.10.1016/0920-1211(90)90036-USuche in Google Scholar

Bertram, E.H., Lothman, E.W., and Lenn, N.J. (1990). The hippocampus in experimental chronic epilepsy: a morphometric analysis. Ann. Neurol. 27, 43–48.10.1002/ana.410270108Suche in Google Scholar PubMed

Bumanglag, A.V. and Sloviter, R.S. (2008). Minimal latency to hippocampal epileptogenesis and clinical epilepsy after perforant pathway stimulation-induced status epilepticus in awake rats. J. Comp. Neurol. 510, 561–580.10.1002/cne.21801Suche in Google Scholar PubMed PubMed Central

Carriero, G., Arcieri, S., Cattalini, A., Corsi, L., Gnatkovsky, V., and de Curtis, M. (2012). A guinea pig model of mesial temporal lobe epilepsy following nonconvulsive status epilepticus induced by unilateral intrahippocampal injection of kainic acid. Epilepsia 53, 1917–1927.10.1111/j.1528-1167.2012.03669.xSuche in Google Scholar

Cavazos, J.E., Jones, S.M., and Cross, D.J. (2004). Sprouting and synaptic reorganization in the subiculum and CA1 region of the hippocampus in acute and chronic models of partial-onset epilepsy. Neuroscience 126, 677–688.10.1016/j.neuroscience.2004.04.014Suche in Google Scholar

Clifford, D.B., Olney, J.W., Maniotis, A., Collins, R.C., and Zorumski, C.F. (1987). The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience 23, 953–968.10.1016/0306-4522(87)90171-0Suche in Google Scholar

Coulter, D.A., Rafiq, A., Shumate, M., Gong, Q.Z., DeLorenzo, R.J., and Lyeth, B.G. (1996). Brain injury-induced enhanced limbic epileptogenesis: anatomical and physiological parallels to an animal model of temporal lobe epilepsy. Epilepsy Res. 26, 81–91.10.1016/S0920-1211(96)00044-7Suche in Google Scholar

Curia, G., Longo, D., Biagini, G., Jones, R.S.G., and Avoli, M. (2008). The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 172, 143–157.10.1016/j.jneumeth.2008.04.019Suche in Google Scholar

D’Ambrosio, R. and Perucca, E. (2004). Epilepsy after head injury. Curr Opin Neurol. 17, 731–735.10.1097/00019052-200412000-00014Suche in Google Scholar

De Araujo Furtado, M., Braga, G.K., Oliveira, J.A.C., Del Vecchio, F., and Garcia-Cairasco, N. (2002). Behavioral, morphologic, and electroencephalographic evaluation of seizures induced by intrahippocampal microinjection of pilocarpine. Epilepsia 43, 37–39.10.1046/j.1528-1157.43.s.5.41.xSuche in Google Scholar

De Araujo Furtado, M., Lumley, L.A., Robison, C., Tong, L.C., Lichtenstein, S., and Yourick, D.L. (2010). Spontaneous recurrent seizures after status epilepticus induced by soman in Sprague-Dawley rats. Epilepsia 51, 1503–1510.10.1111/j.1528-1167.2009.02478.xSuche in Google Scholar

De Deyn, P.P., D’Hooge, R., Marescau, B., and Pei, Y.-Q. (1992). Chemical models of epilepsy with some reference to their applicability in the development of anticonvulsants. Epilepsy Res. 12, 87–110.10.1016/0920-1211(92)90030-WSuche in Google Scholar

Deshpande, L.S., Carter, D.S., Blair, R.E., and DeLorenzo, R.J. (2010). Development of a prolonged calcium plateau in hippocampal neurons in rats surviving status epilepticus induced by the organophosphate diisopropylfluorophosphate. Toxicol. Sci. 116, 623–631.10.1093/toxsci/kfq157Suche in Google Scholar PubMed PubMed Central

Deshpande, L.S., Carter, D.S., Phillips, K.F., Blair, R.E., and DeLorenzo, R.J. (2014). Development of status epilepticus, sustained calcium elevations and neuronal injury in a rat survival model of lethal paraoxon intoxication. Neurotoxicology 44, 17–26.10.1016/j.neuro.2014.04.006Suche in Google Scholar

Doheny, H.C., Whittington, M.A., Jefferys, J.G., and Patsalos, P.N. (2002). A comparison of the efficacy of carbamazepine and the novel anti-epileptic drug levetiracetam in the tetanus toxin model of focal complex partial epilepsy. Br. J. Pharmacol. 135, 1425–1434.10.1038/sj.bjp.0704606Suche in Google Scholar

Doretto, M.C., Fonseca, C.G., Lobo, R.B., Terra, V.C., Oliveira, J.A., and Garcia-Cairasco, N. (2003). Quantitative study of the response to genetic selection of the Wistar audiogenic rat strain (WAR). Behav. Genet. 33, 33–42.10.1023/A:1021099432759Suche in Google Scholar

Drexel, M., Preidt, A.P., and Sperk, G. (2012). Sequel of spontaneous seizures after kainic acid-induced status epilepticus and associated neuropathological changes in the subiculum and entorhinal cortex. Neuropharmacology 63, 806–817.10.1016/j.neuropharm.2012.06.009Suche in Google Scholar

Dube, C., Chen, K., Eghbal-Ahmadi, M., Brunson, K., Soltesz, I., and Baram, T.Z. (2000). Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term. Ann. Neurol. 47, 336–344.10.1002/1531-8249(200003)47:3<336::AID-ANA9>3.0.CO;2-WSuche in Google Scholar

Dube, C., Yu, H., Nalcioglu, O., and Baram, T.Z. (2004). Serial MRI after experimental febrile seizures: altered T2 signal without neuronal death. Ann. Neurol. 56, 709–714.10.1002/ana.20266Suche in Google Scholar

Dutra Moraes, M.F., Galvis-Alonso, O.Y., and Garcia-Cairasco, N. (2000). Audiogenic kindling in the Wistar rat: a potential model for recruitment of limbic structures. Epilepsy Res. 39, 251–259.10.1016/S0920-1211(00)00107-8Suche in Google Scholar

Engel, J. Jr. (1996). Surgery for seizures. N. Engl. J. Med. 334, 647–652.10.1056/NEJM199603073341008Suche in Google Scholar

Fisher, R., Salanova, V., Witt, T., Worth, R., Henry, T., Gross, R., Oommen, K., Osorio, I., Nazzaro, J., Labar, D., et al. (2010). Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia 51, 899–908.10.1111/j.1528-1167.2010.02536.xSuche in Google Scholar

Fisher, R.S., Eggleston, K.S., and Wright, C.W. (2015). Vagus nerve stimulation magnet activation for seizures: a critical review. Acta. Neurol. Scand. 131, 1–8.10.1111/ane.12288Suche in Google Scholar

French, E.D., Aldinio, C., and Schwarcz, R. (1982). Intrahippocampal kainic acid, seizures and local neuronal degeneration: relationships assessed in unanesthetized rats. Neuroscience 7, 2525–2536.10.1016/0306-4522(82)90212-3Suche in Google Scholar

French, J.A., Williamson, P.D., Thadani, V.M., Darcey, T.M., Mattson, R.H., Spencer, S.S., and Spencer, D.D. (1993). Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann. Neurol. 34, 774–780.10.1002/ana.410340604Suche in Google Scholar

Giavina-Bianchi, P., Giavina-Bianchi, M., Tanno, L.K., Ensina, L.F.C., Motta, A.A., and Kalil, J. (2009). Epileptic seizure after treatment with thiocolchicoside. Ther. Clin. Risk Management 5, 635–637.10.2147/TCRM.S4823Suche in Google Scholar

Goffin, K., Nissinen, J., Van Laere, K., and Pitkanen, A. (2007). Cyclicity of spontaneous recurrent seizures in pilocarpine model of temporal lobe epilepsy in rat. Exp. Neurol. 205, 501–505.10.1016/j.expneurol.2007.03.008Suche in Google Scholar

Goldberg, E.M. and Coulter, D.A. (2013). Mechanisms of epileptogenesis: a convergence on neural circuit dysfunction. Nat. Rev. Neurosci. 14, 337–349.10.1038/nrn3482Suche in Google Scholar

Goodman, J. (1998). Experimental models of status epilepticus. Neuropharmacology Methods in Epilepsy Research (New York, NY, USA: CRB Press).Suche in Google Scholar

Gorter, J.A., van Vliet, E.A., Aronica, E., and Lopes da Silva, F.H. (2001). Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur. J. Neurosci. 13, 657–669.10.1046/j.1460-9568.2001.01428.xSuche in Google Scholar

Groticke, I., Hoffmann, K., and Loscher, W. (2007). Behavioral alterations in the pilocarpine model of temporal lobe epilepsy in mice. Exp. Neurol. 207, 329–349.10.1016/j.expneurol.2007.06.021Suche in Google Scholar

Hamilton, S.E., Loose, M.D., Qi, M., Levey, A.I., Hille, B., McKnight, G.S., Idzerda, R.L., and Nathanson, N.M. (1997). Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc. Natl. Acad. Sci. USA 94, 13311–13316.10.1073/pnas.94.24.13311Suche in Google Scholar

Hattiangady, B., Kuruba, R., and Shetty, A.K. (2011). Acute seizures in old age leads to a greater loss of CA1 pyramidal neurons, an increased propensity for developing chronic TLE and a severe cognitive dysfunction. Aging Dis. 2, 1–17.Suche in Google Scholar

Hawkins, C.A. and Mellanby, J.H. (1987). Limbic epilepsy induced by tetanus toxin: a longitudinal electroencephalographic study. Epilepsia 28, 431–444.10.1111/j.1528-1157.1987.tb03669.xSuche in Google Scholar

Holmes, G.L. and Weber, D.A. (1985). Effects of hypoxic-ischemic encephalopathies on kindling in the immature brain. Exp. Neurol. 90, 194–203.10.1016/0014-4886(85)90052-4Suche in Google Scholar

Jehi, L.E. (2015). The risk-benefit ratio for temporal lobe resection in patients with bilateral mesial temporal lobe epilepsy. Epilepsy Curr. 15, 78–79.10.5698/1535-7597-15.2.78Suche in Google Scholar

Jensen, F.E., Applegate, C.D., Holtzman, D., Belin, T.R., and Burchfiel, J.L. (1991). Epileptogenic effect of hypoxia in the immature rodent brain. Ann. Neurol. 29, 629–637.10.1002/ana.410290610Suche in Google Scholar

Jobe, P.C., Picchioni, A.L., and Chin, L. (1973). Role of brain norepinephrine in audiogenic seizure in the rat. J. Pharmacol. Exp. Ther. 184, 1–10.10.1016/S0022-3565(25)29378-8Suche in Google Scholar

Jope, R.S., Morrisett, R.A., and Snead, O.C. (1986). Characterization of lithium potentiation of pilocarpine-induced status epilepticus in rats. Exp. Neurol. 91, 471–480.10.1016/0014-4886(86)90045-2Suche in Google Scholar

Kharatishvili, I., Nissinen, J.P., McIntosh, T.K., and Pitkanen, A. (2006). A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 140, 685–697.10.1016/j.neuroscience.2006.03.012Suche in Google Scholar PubMed

Kienzler-Norwood, F., Costard, L., Sadangi, C., Müller, P., Neubert, V., Bauer, S., Rosenow, F., and Norwood, B.A. (2017). A novel animal model of acquired human temporal lobe epilepsy based on the simultaneous administration of kainic acid and lorazepam. Epilepsia 58, 222–230.10.1111/epi.13579Suche in Google Scholar PubMed

Kiesmann, M., Marescaux, C., Vergnes, M., Micheletti, G., Depaulis, A., and Warter, J.M. (1988). Audiogenic seizures in Wistar rats before and after repeated auditory stimuli: clinical, pharmacological, and electroencephalographic studies. J. Neural Transm. 72, 235–244.10.1007/BF01243422Suche in Google Scholar PubMed

Klee, R., Brandt, C., Tollner, K., and Loscher, W. (2017). Various modifications of the intrahippocampal kainate model of mesial temporal lobe epilepsy in rats fail to resolve the marked rat-to-mouse differences in type and frequency of spontaneous seizures in this model. Epilepsy Behav. 68, 129–140.10.1016/j.yebeh.2016.11.035Suche in Google Scholar PubMed

Kruman, I.I., Culmsee, C., Chan, S.L., Kruman, Y., Guo, Z., Penix, L., and Mattson, M.P. (2000). Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J. Neurosci. 20, 6920–6926.10.1523/JNEUROSCI.20-18-06920.2000Suche in Google Scholar

Lánský, P., Velíŝková, J., and Velíŝek, L. (1997). An indirect method for absorption rate estimation: flurothyl-induced seizures. Bull. Math. Biol. 59, 569–579.10.1007/BF02459466Suche in Google Scholar PubMed

Lapin, I.P. (1978). Stimulant and convulsive effects of kynurenines injected into brain ventricles in mice. J. Neural. Transm. 42, 37–43.10.1007/BF01262727Suche in Google Scholar PubMed

Lévesque, M. and Avoli, M. (2013). The kainic acid model of temporal lobe epilepsy. Neurosci. Biobehav. Rev. 37, 2887–2899.10.1016/j.neubiorev.2013.10.011Suche in Google Scholar

Loscher, W., Cramer, S., and Ebert, U. (1998). Differences in kindling development in seven outbred and inbred rat strains. Exp. Neurol. 154, 551–559.10.1006/exnr.1998.6948Suche in Google Scholar

Lothman, E.W., Bertram, E.H., Bekenstein, J.W., and Perlin, J.B. (1989). Self-sustaining limbic status epilepticus induced by ‘continuous’ hippocampal stimulation: electrographic and behavioral characteristics. Epilepsy Res. 3, 107–119.10.1016/0920-1211(89)90038-7Suche in Google Scholar

Lowenstein, D.H., Simon, R.P., and Sharp, F.R. (1990). The pattern of 72-kDa heat shock protein-like immunoreactivity in the rat brain following flurothyl-induced status epilepticus. Brain Res. 531, 173–182.10.1016/0006-8993(90)90771-3Suche in Google Scholar

Marchi, N., Oby, E., Batra, A., Uva, L., De Curtis, M., Hernandez, N., Van Boxel-Dezaire, A., Najm, I., and Janigro, D. (2007). In vivo and in vitro effects of pilocarpine: relevance to ictogenesis. Epilepsia 48, 1934–1946.10.1111/j.1528-1167.2007.01185.xSuche in Google Scholar

McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.L. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233–244.10.1016/0306-4522(89)90247-9Suche in Google Scholar

Mellanby, J. (1993). Tetanus toxin as a tool for investigating the consequences of excessive neuronal excitation. Botulinum and tetanus neurotoxins: neurotransmission and biomedical aspects. (Boston, MA, USA: DasGupta, B.R. Springer US), pp. 291–297.10.1007/978-1-4757-9542-4_31Suche in Google Scholar

Mellanby, J., George, G., Robinson, A., and Thompson, P. (1977). Epileptiform syndrome in rats produced by injecting tetanus toxin into the hippocampus. J. Neurol. Neurosurg. Psychiatry 40, 404–414.10.1136/jnnp.40.4.404Suche in Google Scholar

Mello, L.E. and Covolan, L. (1996). Spontaneous seizures preferentially injure interneurons in the pilocarpine model of chronic spontaneous seizures. Epilepsy Res. 26, 123–129.10.1016/S0920-1211(96)00048-4Suche in Google Scholar

Mü;ller, C.J., Bankstahl, M., Groticke, I., and Loscher, W. (2009). Pilocarpine vs. lithium-pilocarpine for induction of status epilepticus in mice: development of spontaneous seizures, behavioral alterations and neuronal damage. Eur. J. Pharmacol. 619, 15–24.10.1016/j.ejphar.2009.07.020Suche in Google Scholar PubMed

Owens, J., Robbins, C.A., Wenzel, H.J., and Schwartzkroin, P.A. (1997). Acute and chronic effects of hypoxia on the developing hippocampus. Ann. Neurol. 41, 187–199.10.1002/ana.410410210Suche in Google Scholar

Pitkanen, A. and McIntosh, T.K. (2006). Animal models of post-traumatic epilepsy. J. Neurotrauma 23, 241–261.10.1089/neu.2006.23.241Suche in Google Scholar

Poletaeva, I.I., Surina, N.M., Kostina, Z.A., Perepelkina, O.V., and Fedotova, I.B. (2017). The Krushinsky-Molodkina rat strain: the study of audiogenic epilepsy for 65 years. Epilepsy Behav. 71, 130–141.10.1016/j.yebeh.2015.04.072Suche in Google Scholar

Prilopko, L. (2005). Epilepsy Care in the World. Epilepsy Health Atlas (Geneva, Switzerland: World Health Organization).Suche in Google Scholar

Racine, R.J. (1972). Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281–294.10.1016/0013-4694(72)90177-0Suche in Google Scholar

Rao, M.S., Hattiangady, B., Reddy, D.S., and Shetty, A.K. (2006). Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. J. Neurosci. Res. 83, 1088–1105.10.1002/jnr.20802Suche in Google Scholar

Reddy, D.S. and Kuruba, R. (2013). Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions. Int. J. Mol. Sci. 14, 18284–18318.10.3390/ijms140918284Suche in Google Scholar

Rejdak, K., Nieoczym, D., Czuczwar, M., Kis, J., Wlaz, P., and Turski, W.A. (2011). Orphenadrine induces secondarily generalized convulsive status epilepticus in rats. Brain Res. Bull. 84, 389–393.10.1016/j.brainresbull.2011.01.014Suche in Google Scholar

Rejdak, K., Nieoczym, D., Czuczwar, M., Kis, J., Wlaz, P., and Turski, W.A. (2014). Orphenadrine-induced convulsive status epilepticus in rats responds to the NMDA antagonist dizocilpine. Pharmacol. Rep. 66, 399–403.10.1016/j.pharep.2013.12.007Suche in Google Scholar

Ross, K.C. and Coleman, J.R. (2000). Developmental and genetic audiogenic seizure models: behavior and biological substrates. Neurosci. Biobehav. Rev. 24, 639–653.10.1016/S0149-7634(00)00029-4Suche in Google Scholar

Rubio, C., Rubio-Osornio, M., Retana-Marquez, S., Veronica Custodio, M.L., and Paz, C. (2010). In vivo experimental models of epilepsy. Cent. Nerv. Syst. Agents Med. Chem. 10, 298–309.10.2174/187152410793429746Suche in Google Scholar PubMed

Schauwecker, P.E. (2011). The relevance of individual genetic background and its role in animal models of epilepsy. Epilepsy Res. 97, 1–11.10.1016/j.eplepsyres.2011.09.005Suche in Google Scholar

Schmidt, A.P., Lara, D.R., de Faria Maraschin, J., da Silveira Perla, A., and Onofre Souza, D. (2000). Guanosine and GMP prevent seizures induced by quinolinic acid in mice. Brain Res. 864, 40–43.10.1016/S0006-8993(00)02106-5Suche in Google Scholar

Schwarcz, R., Brush, G.S., Foster, A.C., and French, E.D. (1984). Seizure activity and lesions after intrahippocampal quinolinic acid injection. Exp. Neurol. 84, 1–17.10.1016/0014-4886(84)90001-3Suche in Google Scholar

Sechi, G., De Riu, P., Mameli, O., Deiana, G.A., Cocco, G.A., and Rosati, G. (2003). Focal and secondarily generalised convulsive status epilepticus induced by thiocolchicoside in the rat. Seizure 12, 508–515.10.1016/S1059-1311(03)00053-0Suche in Google Scholar

Serikawa, T., Mashimo, T., Kuramoto, T., Voigt, B., Ohno, Y., and Sasa, M. (2015). Advances on genetic rat models of epilepsy. Exp. Animals 64, 1–7.10.1538/expanim.14-0066Suche in Google Scholar

Sharma, A.K., Reams, R.Y., Jordan, W.H., Miller, M.A., Thacker, H.L., and Snyder, P.W. (2007). Mesial temporal lobe epilepsy: pathogenesis, induced rodent models and lesions. Toxicol. Pathol. 35, 984–999.10.1080/01926230701748305Suche in Google Scholar

Shetty, A.K. (2010). Neural stem cell therapy for temporal lobe epilepsy. Epilepsia 51, 92.10.1093/med/9780199746545.003.0085Suche in Google Scholar

Sloviter, R.S. (1983). “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain. Res. Bull. 10, 675–697.10.1016/0361-9230(83)90037-0Suche in Google Scholar

Sloviter, R.S. (1987). Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235, 73–76.10.1126/science.2879352Suche in Google Scholar

Sloviter, R.S., Dean, E., Sollas, A.L., and Goodman, J.H. (1996). Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J. Comp. Neurol. 366, 516–533.10.1002/(SICI)1096-9861(19960311)366:3<516::AID-CNE10>3.0.CO;2-NSuche in Google Scholar

Sperber, E.F. and Moshé, S.L. (1988). Age-related differences in seizure susceptibility to flurothyl. Dev. Brain Res. 39, 295–297.10.1016/0165-3806(88)90033-8Suche in Google Scholar

Sutula, T.P. (2004). Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res. 60, 161–171.10.1016/j.eplepsyres.2004.07.001Suche in Google Scholar

Todorovic, M.S., Cowan, M.L., Balint, C.A., Sun, C., and Kapur, J. (2012). Characterization of status epilepticus induced by two organophosphates in rats. Epilepsy Res. 101, 268–276.10.1016/j.eplepsyres.2012.04.014Suche in Google Scholar

Turski, W.A., Cavalheiro, E.A., Schwarz, M., Czuczwar, S.J., Kleinrok, Z., and Turski, L. (1983a). Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 9, 315–335.10.1016/0166-4328(83)90136-5Suche in Google Scholar

Turski, W.A., Czuczwar, S.J., Kleinrok, Z., and Turski, L. (1983b). Cholinomimetics produce seizures and brain damage in rats. Experientia 39, 1408–1411.10.1007/BF01990130Suche in Google Scholar

Vale, F.L., Vivas, A.C., Manwaring, J., Schoenberg, M.R., and Benbadis, S.R. (2015). Temporal lobe epilepsy and cavernous malformations: surgical strategies and long-term outcomes. Acta Neurochir. (Vienna) 157, 1887–1895; discussion 1895.10.1007/s00701-015-2592-4Suche in Google Scholar

van Luijtelaar, E.L. and Coenen, A.M. (1986). Two types of electrocortical paroxysms in an inbred strain of rats. Neurosci. Lett. 70, 393–397.10.1016/0304-3940(86)90586-0Suche in Google Scholar

Vicedomini, J.P. and Nadler, J.V. (1987). A model of status epilepticus based on electrical stimulation of hippocampal afferent pathways. Exp. Neurol. 96, 681–691.10.1016/0014-4886(87)90229-9Suche in Google Scholar

Vincent, P. and Mulle, C. (2009). Kainate receptors in epilepsy and excitotoxicity. Neuroscience 158, 309–323.10.1016/j.neuroscience.2008.02.066Suche in Google Scholar

Walton, N.Y. and Treiman, D.M. (1988). Experimental secondarily generalized convulsive status epilepticus induced by D,L-homocysteine thiolactone. Epilepsy Res. 2, 79–86.10.1016/0920-1211(88)90023-XSuche in Google Scholar

White, H.S. (2002). Animal models of epileptogenesis. Neurology 59, S7–S14.10.1212/WNL.59.9_suppl_5.S7Suche in Google Scholar

Williams, P.A., Dou, P., and Dudek, F.E. (2004). Epilepsy and synaptic reorganization in a perinatal rat model of hypoxia–ischemia. Epilepsia 45, 1210–1218.10.1111/j.0013-9580.2004.60403.xSuche in Google Scholar

Yang, J., Houk, B., Shah, J., Hauser, K.F., Luo, Y., Smith, G., Schauwecker, E., and Barnes, G.N. (2005). Genetic background regulates semaphorin gene expression and epileptogenesis in mouse brain after kainic acid status epilepticus. Neuroscience 131, 853–869.10.1016/j.neuroscience.2004.09.064Suche in Google Scholar

Zhao, D.Y., Wu, X.R., Pei, Y.Q., and Zuo, Q.H. (1985). Kindling phenomenon of hyperthermic seizures in the epilepsy-prone versus the epilepsy-resistant rat. Brain Res. 358, 390–393.10.1016/0006-8993(85)90991-6Suche in Google Scholar