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Epilepsy and Seizures: Excitotoxicity or Excitotrophicity?

  • Karen Gale

Abstract

Excitotoxic neuronal death has been clearly documented in the adult brain following status epilepticus (SE), a state of uninterrupted seizure activity that may last for hours. The severity and duration of SE determine the extent of neuronal injury; in most animal models damage is observed with durations of one hour or longer. Severity, duration and rate of onset may also influence the extent to which the neuronal death is mediated by apoptotic or necrotic processes. In contrast to the adult brain, the immature brain is resistant to SE-induced damage; nevertheless long-term deleter ious effects of SE have been observed in animals that experienced SE in infancy without exhibiting neuronal loss. Likewise, in adult animals, long-term abnormalities such as spontaneous seizures have been documented following SE even under conditions in which the brain was protected from damage. This suggests that SE-induced excitotoxic injury is not required for the development of long-term disrupt ion of neuronal function in the aftermath of SE. In contrast to SE, recurrent intermittent brief seizures such as those typically associated with epilepsy, do not necessar ily cause neuronal inj ury. In patients with epilepsy it is often difficult to determine whether brain lesions are a cause or consequence of the seizure condition; little or no injury has been observed with chronic brief seizures in several animal models. In fact, exposure to repeated brief noninjurious seizures has been shown to exert a neuroprotective action, possibly as a consequence of induction of expression of neurotrophic factors. This “excitotrophic” effect of seizures extends beyond protection against SE-induced injury to include protection in models such as adrenalectomy-induced granule cell death. It is therefore possible that seizures may serve to protect against neurodegeneration and promote regrowth and remodeling in the face of insults to the nervous system. Thus, seizures can span a spectrum from trophic and adaptive to toxic and maladaptive, depending upon the conditions of their occurrence and the extent to which they are regulated. In this context, seizures may be analogous to fever: adaptive and protective in specific settings, with the capacity to become maladaptive and injurious in their own right if they develop into SE or a long lasting epileptic condition.

Keywords

seizures limbic system status epilepticus neuroprotection neurotrophic factors apoptosis electroconvulsive shock immature brain 

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References

  1. Abrams R. ECT for Parkinson’s disease. Am J Psychiatry 1989; Nov; 146(11):1391–3PubMedGoogle Scholar
  2. Akbar M.T., Lundberg A.M., Liu K., Vidyadaran S., Wells K.E., Dolatshad H., Wynn S., Wells D.J., Latchman D.S., de Belleroche J. The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem 2003; May 30;278(22):19956–65PubMedCrossRefGoogle Scholar
  3. Andre V., Ferrandon A., Marescaux C., Nehlig A. Electroshocks delay seizures and subsequent epileptogenesis but do not prevent neuronal damage in the lithium-pilocarpine model of epilepsy. Epilepsy Res 2000; Nov;42(1):7–22PubMedCrossRefGoogle Scholar
  4. Angelucci F., Aloe L., Jimenez-Vasquez P., Mathe A.A. Electroconvulsive stimuli alter the regional concentrations of nerve growth factor, brain-derived neurotrophic factor, and glial cell line-derived neurotrophic factor in adult rat brain. J ECT 2002; Sep; 18(3):138–43PubMedCrossRefGoogle Scholar
  5. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton SA, Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995; 15:961–973PubMedCrossRefGoogle Scholar
  6. Araki T., Simon R.P., Taki W., Lan J.Q., Henshall D.C. Characterization of neuronal death induced by focally evoked limbic seizures in the C57BL/6 mouse. J Neurosci Res 2002; Sep 1;69(5):614–21PubMedCrossRefGoogle Scholar
  7. Aronica E.M., Gorter J.A., Paupard M.C., Grooms S.Y., Bennett M.Y., Zukin R.S. Status epilepticus-induced alterations in metabotropic glutamate receptor expression in young and adult rats. J Neurosci 1997; Nov 1;17(21):8588–95PubMedGoogle Scholar
  8. Babb T.L., Brown W.J., Pretorius J., Davenport C., Lieb J.P., Crandall P.H. Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 1990; 25:729–740.CrossRefGoogle Scholar
  9. Balldin J., Eden S., Granerus A.K, Modigh K., Svanborg A., Walinder J., Wallin L. Electroconvulsive therapy in Parkinson’s syndrome with “on-off” phenomenon. J Neural Transm 1980; 47(1):11–21PubMedCrossRefGoogle Scholar
  10. Baram T.Z., Eghbal-Ahmadi M., Bender R.A. Is neuronal death required for seizureinduced epileptogenesis in the immature brain? Prog Brain Res 2002; 135:365–75PubMedCrossRefGoogle Scholar
  11. Beale M.D., Kellner C.H., Gurecki P., Pritchett J.T. ECT for the treatment of Huntington’s disease: a case study. Convuls Ther 1997; Jun;13(2):108–12PubMedGoogle Scholar
  12. Becker A.J., Gillardon F., Blumcke I., Langendorfer D., Beck H., Wiestler O.D. Differential regulation of apoptosis-related genes in resistant and vulnerable subfields of the rat epileptic hippocampus. Brain Res Mol Brain Res 1999; Apr 6;67(1):172–6PubMedCrossRefGoogle Scholar
  13. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985; 14:375–403PubMedCrossRefGoogle Scholar
  14. Berger M., de Soto D.A. The use of ECT for Parkinson symptoms in a nondepressed patient. Psychosomatics 1990; Fall;31(4):465–6PubMedCrossRefGoogle Scholar
  15. Bernasconi N., Bernasconi A., Caramanos Z., Dubeau F., Richardson J., Andermann F., Arnold D.L. Entorhinal cortex atrophy in epilepsy patients exhibiting normal hippocampal volumes. Neurology 2001; May 22;56(10):1335–9PubMedCrossRefGoogle Scholar
  16. Bertram E.H. 3rd, Lothman E.W. Morphometric effects of intermittent kindled seizures and limbic status epilepticus in the dentate gyrus of the rat. Brain Res 1993; Feb 12;603(1):2531Google Scholar
  17. Berzaghi M. P., Cooper J., Castren E., Zafra F., Sofroniew M., Thoenen H., and Lindholm D. Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus. J Neurosci 1993; 13:3818–3826Google Scholar
  18. Birkett D.P. Use of ECT in Parkinson’s disease. Am J Psychiatry 1990; Jul;147(7):952Google Scholar
  19. Bittigau P., Sifringer M., Ikonomidou C. Antiepileptic drugs and apoptosis in the developing brain. Ann N Y Acad Sci 2003; May;993: 103–14; discussion 123-4PubMedCrossRefGoogle Scholar
  20. Bittigau P., Sifringer M., Genz K., Reith E., Pospischil D., Govindarajalu S., Dzietko M., Pesditschek S., Mai L., Dikranian K., Olney J., and Ikonomidou C. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. PNAS 2002; 99(23):15089–15094PubMedCrossRefGoogle Scholar
  21. Blennow G., Brierley J.B., Meldrum B.S., Siesjo B.K. Epileptic brain damage: the role of systemic factors that modify cerebral energy metabolism. Brain 1978; Dec;101(4):687–700PubMedCrossRefGoogle Scholar
  22. Blumcke I., Becker A.J., Klein C., Scheiwe C., Lie A.A., Beck H., Waha A., Friedl M.G., Kuhn R., Emson P., Elger C., Wiestler O.D. Temporal lobe epilepsy associated upregulation of metabotropic glutamate receptors: correlated changes in mGluR1 mRNA and protein expression in experimental animals and human patients. J Neuropathol Exp Neurol 2000; Jan;59(1):1–10PubMedGoogle Scholar
  23. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 1995; Aug 1;92(16):7162–6PubMedCrossRefGoogle Scholar
  24. Briellmann R.S., Newton M.R., Wellard R.M., Jackson G.D. Hippocampal sclerosis following brief generalized seizures in adulthood. Neurology 2001; 57:315–7PubMedCrossRefGoogle Scholar
  25. Browning R.A., Nelson D.K. Modification of electroshock and pentylenetetrazol seizure patterns in rats after precollicular transections. Exp Neurol 1986; Sep;93(3):546–56PubMedCrossRefGoogle Scholar
  26. Browning R.A., Nelson D.K. Variation in threshold and pattern of electroshock-induced seizures in rats depending on site of stimulation. Life Sci 1985; Dec 9;37(23):2205–11PubMedCrossRefGoogle Scholar
  27. Browning R.A., Wang C., Lanker M.L., Jobe P.C. Electroshock-and pentylenetetrazol-induced seizures in genetically epilepsy-prone rats (GEPRs): differences in threshold and pattern. Epilepsy Res 1990; May–Jun;6(1):1–11PubMedCrossRefGoogle Scholar
  28. Bruce A.J., M. Baudry. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Rad Biol Med 1995; 18:993–1002PubMedCrossRefGoogle Scholar
  29. Buckmaster P.S., Dudek F.E. Neuronal loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 1997; 385:385–404PubMedCrossRefGoogle Scholar
  30. Cassidy R.M., Gale K. Mediodorsal thalamus plays a critical role in the development of limbic motor seizures. J Neurosci 1998; Nov 1; 18(21):9002–9PubMedGoogle Scholar
  31. Cavalheiro E.A., Silva D.F., Turski W.A., Calderazzo-Filho L.S., Bortolotto Z.A., Turski L. The susceptibility of rats to pilocarpine is age-dependent. Exp Brain Res 1987; 37:43–58Google Scholar
  32. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 1991; 32:778–782PubMedCrossRefGoogle Scholar
  33. Cendes F., Andermann F., Carpenter S., Zatorre R.J., Cashman N.R. Temporal lobe epilepsy caused by domoic acid intoxication: evidence for glutamate receptor-mediated excitotoxicity in humans. Ann Neurol 1995; Jan;37(1):123–6PubMedCrossRefGoogle Scholar
  34. Cendes F., Andermann F., Dubeau F., Gloor P., Evans A., Jones-Gotman M., Olivier A., Andermann E., Robitaille Y., Lopes-Cendes I., et al. Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study. Neurology 1993; Jun;43(6):1083–7PubMedCrossRefGoogle Scholar
  35. Cheng B., Mattson M.P. NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res 1994; Mar 21;640(1–2):56–67PubMedCrossRefGoogle Scholar
  36. Cilio M.R., Sogawa Y., Cha B.H., Liu X., Huang L.T., Holmes G.L. Long-term effects of status epilepticus in the immature brain are specific for age and model. Epilepsia 2003; Apr;44(4):518–28PubMedCrossRefGoogle Scholar
  37. Clifford D.B., Olney J.W., Maniotis A., Collins R.C., Zorumski C.F. The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience 1987; 23:953–968PubMedCrossRefGoogle Scholar
  38. Covolan L., Ribeiro L.T.C., Longo B.M., Mello L. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine or kainate induced status epilepticus. Hippocampus 2000; 10:169–180PubMedCrossRefGoogle Scholar
  39. Dalby N.O., Tonder N., Wolby D.P., West M., Finsen B., Bolwig T.G. No loss of hippocampal hilar somatostatinergic neurons after repeated electroconvulsive shock: a combined stereological and in situ hybridization study. Biol Psychiatry 1996; Jul 1;40(1):54–60PubMedCrossRefGoogle Scholar
  40. Davies K.G., Hermann B.P., Dohan F.C. Jr., Foley K.T., Bush A.J., Wyler A.R. Relationship of hippocampal sclerosis to duration and age of onset of epilepsy, and childhood febrile seizures in temporal lobectomy patients. Epilepsy Res 1996; Jun;24(2):119–26PubMedCrossRefGoogle Scholar
  41. DeGiorgio C.M., Tomiyasu U., Gott P.S., Treiman D.M. Hippocampal pyramidal cell loss in human status epilepticus. Epilepsia 1992; 33:23–7PubMedCrossRefGoogle Scholar
  42. DeLorenzo R.J., Hauser W.A., Towne A.R., Boggs J.G., Pellock J.M., Penberthy L., et al. A prospective, population-based epidemiologic study of status epilepticus in Richmond, Virginia. Neurology 1996; 46:1029–35PubMedCrossRefGoogle Scholar
  43. DeLorenzo R.J., Towne A.R., Pellock J.M., Ko D. Status epilepticus in children, adults, and the elderly. Epilepsia 1992; 33 Suppl 4:S15–25PubMedCrossRefGoogle Scholar
  44. Dirnagl U., Simon R.P., Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 2003; May;26(5):248–54PubMedCrossRefGoogle Scholar
  45. Druga R., Kubova H., Suchomelova L., Haugvicova R. Lithium/pilocarpine status epilepticus-induced neuropathology of piriform cortex and adjoining structures in rats is age-dependent. Physiol Res 2003; 52(2):251–64PubMedGoogle Scholar
  46. Dzhala V., Ben-Ari Y., Khazipov R. Seizures accelerate anoxia-induced neuronal death in the neonatal rat hippocampus. Ann Neurol 2000; Oct;48(4):632–40PubMedCrossRefGoogle Scholar
  47. Ebert U., Brandt C., Loscher W. Delayed sclerosis, neuroprotection, and limbic epileptogenesis after status epilepticus in the rat. Epilepsia 2002; 43 Suppl 5:86–95PubMedCrossRefGoogle Scholar
  48. Emerson M.R., Nelson S.R., Samson F.E., Pazdernik T.L. A global hypoxia preconditioning model: neuroprotection against seizure-induced specific gravity changes (edema) and brain damage in rats. Brain Res Brain Res Protoc 1999; Dec;4(3):360–6PubMedCrossRefGoogle Scholar
  49. Ende G., Braus D.F., Walter S., Weber-Fahr W., Henn F.A. The hippocampus in patients treated with electroconvuls ive therapy: a proton magnetic resonance spectroscopic imaging study. Arch Gen Psychiatry 2000; 57(10):937–943PubMedCrossRefGoogle Scholar
  50. Faber R., Trimble M.R. Electroconvulsive therapy in Parkinson’s disease and other movement disorders. Mov Disord 1991; 6(4):293–303PubMedCrossRefGoogle Scholar
  51. Faherty C.J., Xanthoudakis S., Smeyne R.J. Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment. Brain Res Mol Brain Res 1999; Jun 18;70(1):159–63PubMedCrossRefGoogle Scholar
  52. Farwell J. R., Dodrill C. B., Batzel L. W. Neuropsychological abilities of children with epilepsy. Epilepsia 1985; 26:395–400PubMedCrossRefGoogle Scholar
  53. Fernandez G., Effenberger O., Vinz B., Steinlein O., Elger C.E., Dohring W., Heinze H.J. Hippocampal malformation as a cause of familial febrile convulsions and subsequent hippocampal sclerosis. Neurology 1998; Apr;50(4):909–17Google Scholar
  54. Fernandez-Sanchez M.T., Novelli A. Basic fibroblast growth factor protects cerebellar neurons in primary culture from NMDA and non-NMDA receptor mediated neurotoxicity. FEBS Lett 1993; Nov 29;335(1):124–31PubMedCrossRefGoogle Scholar
  55. Finklestein S.P., Kemmou A., Caday C.G., Berlove D.J. Basic fibroblast growth factor protects cerebrocortical neurons against excitatory amino acid toxicity in vitro. Stroke 1993; Dec;24(12 Suppl):I141–3Google Scholar
  56. 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; May;127(1):37–44PubMedCrossRefGoogle Scholar
  57. Fountain N.B., Lothman E.W. Pathophysiology of status epilepticus. J Clin Neurophysiol 1995; Jul;12(4):326–42PubMedGoogle Scholar
  58. Freese A., Finklestein S.P., DiFiglia M. Basic fibroblast growth factor protects striatal neurons in vitro from NMDA-receptor mediated excitotoxicity. Brain Res 1992; Mar 20;575(2):351–5PubMedCrossRefGoogle Scholar
  59. Friedman L.K. Selective reduction of GluR2 protein in adult hippocampal CA3 neurons following status epilepticus but prior-to cell loss. Hippocampus 1998; 8(5):511–25PubMedCrossRefGoogle Scholar
  60. Fuerst D., Shah J., Kupsky W.I., Johnson R., Shah A., Hayman-Abello B., et al. Volumetric MRI, pathological, and neuropsychological progression in hippocampal sclerosis. Neurology 2001; 57:184–8PubMedCrossRefGoogle Scholar
  61. Fujikawa D.G., Itabashi H.H., Wu A., Shinmei S.S. Status epilepticus-induced neuronal loss in humans without systemic complications or epilepsy. Epilepsia 2000; Aug;41(8):981–91PubMedCrossRefGoogle Scholar
  62. Fujikawa D.G., Ke X., Trinidad R.B., Shinmei S.S., Wu A. Caspase-3 is not activated in seizure-induced neuronal necrosis with internucleosomal DNA cleavage. J Neurochem 2002; Oct;83(1):229–40PubMedCrossRefGoogle Scholar
  63. Fujikawa D.G., Shinmei S.S., Cai B. Kainic acid-induced seizures produce necrotic, not apoptotic, neurons with internucleosomal DNA cleavage: implications for programmed cell death mechanisms. Neuroscience 2000c; 98(1):41–53PubMedCrossRefGoogle Scholar
  64. Fujikawa D.G., Shinmei S.S., Cai B. Lithium-pilocarpineinduced status epilepticus produces necrotic neurons with internucleosomal DNA fragmentation in adult rats. Eur J Neurosci 1999; 11:1605–14Google Scholar
  65. Fujikawa D.G., Shinmei S.S., Cai B. Seizure-induced neuronal necrosis: implications for programmed cell death mechanisms. Epilepsia 2000d; 41 Suppl 6:S9–13PubMedCrossRefGoogle Scholar
  66. Fujikawa D.G. Confusion between neuronal apoptosis and activation of programmed cell death mechanisms in acute necrot ic insults. Trends Neurosci 2000; Sep;23(9):410–1PubMedCrossRefGoogle Scholar
  67. Galanopoulou A.S., Vidaurre J., Moshe S.L. Under what circumstances can seizures produce hippocampal injury: evidence for age-specific effects. Dev Neurosci 2002; 24(5):355–63PubMedCrossRefGoogle Scholar
  68. Gilbert D.L., Gantside P.S., Glauser T.A. Efficacy and mortality in treatment of refractory generalized convulsive status epilepticus in children: a meta-analysis. J Child Neurol 1999; 14:602–609PubMedCrossRefGoogle Scholar
  69. Glass M., Dragunow M. Neurochemical and morphological changes associated with human epilepsy. Brain Res Brain Res Rev 1995; Jul;21(1):29–41PubMedCrossRefGoogle Scholar
  70. Glazner G.W., Mattson M.P. Differential effects of BDNF, ADNF9, and TNFalpha on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Exp Neurol 2000; Feb;161(2):442–52PubMedCrossRefGoogle Scholar
  71. Gombos Z., Spiller A., Cottrell G.A., Racine R.I., Mcintyre Burnham W. Mossy fiber sprout ing induced by repeated electroconvulsive shock seizures. Brain Res 1999; Oct 9;844(1–2):28–33PubMedCrossRefGoogle Scholar
  72. Goodman J.H. “Experimental models of status epilepticus.” In Neuropharmacological Methods in Epilepsy Research, S.L. Peterson and T.E. Albertson, eds. Boca Raton: CRC Press, 1998.Google Scholar
  73. Gordon T. Fatigue in adapted systems. Overuse and underuse paradigms. Adv Exp Med Biol 1995; 384:429–56PubMedGoogle Scholar
  74. Gorter J.A., Van Vliet E.A., Proper E.A., De Graan P.N., Ghijsen W.E., Lopes Da Silva F.H., Aronica E. Glutamate transporters alterations in the reorganizing dentate gyrus are associated with progressive seizure activity in chronic epileptic rats. J Comp Neurol 2002; Jan 21;442(4):365–77PubMedCrossRefGoogle Scholar
  75. Gould E., Woolley C.S., McEwen B.S. Short-term glucocort icoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience 1990; 37(2):367–75PubMedCrossRefGoogle Scholar
  76. Gould E., Woolley C.S., McEwen B.S. Naturally occurring cell death in the developing dentate gyrus of the rat. J Comp Neurology 1991; 304:408–418CrossRefGoogle Scholar
  77. Gray N.A., Zhou R., Du J., Moore G.J., Manji H.K. The use of mood stabilizers as plasticity enhancers in the treatment of neuropsychiatric disorders. J Clin Psychiatry 2003; 64 Suppl 5:3–17PubMedGoogle Scholar
  78. Grunewald R.A., Farrow T., Vaughan P., Rittey C.D., Mundy J. A magnetic resonance study of complicated early childhood convulsion. J Neurol Neurosurg Psychiatry 2001; Nov;71(5):638–42PubMedCrossRefGoogle Scholar
  79. Gunderson V.M., Dubach M., Szot P., Born D.E., Wenzel H.J., Maravilla K.R., Zierath D.K., Robbins C.A., Schwartzkroin P.A. Development of a model of status epilepticus in pigtailed macaque infant monkeys. Dev Neurosci 1999; Nov;21(3–5):352–64PubMedCrossRefGoogle Scholar
  80. Gwinn R.P., Kondratyev A., Gale K. Time-dependent increase in basic fibroblast growth factor protein in limbic regions following electroshock seizures. Neuroscience 2002; 114(2):403–9PubMedCrossRefGoogle Scholar
  81. Haas K.Z., Sperber E.F., Opanashuk L.A., Staton P.K., Moshe S.L. Resistance of immature hippocampus to morphologic and physiologic alteration following status epilepticus or kindling. Hippocampus 2001; 11(6):615–625PubMedCrossRefGoogle Scholar
  82. Hamm R.J., Pike B.R., Temple M.D., O’Dell D.M., Lyeth B.G. The effect of postinjury kindled seizures on cognitive performance of traumatically brain-injured rats. Exp Neurol 1995; Dec;136(2):143–8PubMedCrossRefGoogle Scholar
  83. Hauser W.A. Status epilepticus: epidemiologic considerations. Neurology 1990; 40(suppl 2):9–13.PubMedGoogle Scholar
  84. Henshall D.C., Chen J., Simon R.P. Involvement of caspase-3 like protease in the mechanism of cell death following focally evoked limbic seizures. J Neurochem 2000; 74:1215–1223PubMedCrossRefGoogle Scholar
  85. Hermann B. Neurodevelopmental and Progressive Adverse Effects of Epilepsy on Higher Cognitive Functioning 2002 http://www.aesnet.org/edu_pub/PresidentiaISymposium.cfm
  86. Hernandez T.D., Holling L.C. Disruption of behavioral recovery by the anti-convulsant phenobarbital. Brain Res 1994; Jan 28; 635(1–2):300–6PubMedCrossRefGoogle Scholar
  87. Hernandez T.D., Schallert T. Seizures and recovery from experimental brain damage. Exp Neurol 1988; Dec; 102(3):318–24PubMedCrossRefGoogle Scholar
  88. Holmes G. L. Do seizures cause brain damage? Epilepsia 1991; 32:(suppl. 5) S14–S28PubMedGoogle Scholar
  89. Holmes G. L. The long term effects of seizures on the developing brain: clinical and laboratory issues. Brain Dev 1991; 13:393–409PubMedCrossRefGoogle Scholar
  90. Holmes G.L., Khazipov R., Ben-Ari Y. New concepts in neonatal seizures. Neuroreport 2002; 13:A3–8PubMedCrossRefGoogle Scholar
  91. Holmes G.L., Ben-Ari Y. Seizures in the developing brain: perhaps not so benign after all. Neuron 1998; Dec;21(6):1231–4PubMedCrossRefGoogle Scholar
  92. Holmes G.L. Seizure-induced neuronal injury: animal data. Neurology 2002; Nov 12;59(9 Suppl 5):S3–6PubMedCrossRefGoogle Scholar
  93. Houser C.R. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv Neurol 1999; 79:743–761PubMedGoogle Scholar
  94. Huang L., Cilio M. R., Silveira D.C., McCabe B.K., Sogawa Y., Stafstrom C.E., Holmes G.L. Long-term effects of neonatal seizures: a behavioral, electrophysiological, and histological study, Dev Brain Res 1999; 118:99–107CrossRefGoogle Scholar
  95. Hughes P.E., Alexi T., Walton M., Williams C.E., Dragunow M., Clark R.G., Gluckman P.D. Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog Neurobiol 1999; Feb;57(4):421–50PubMedCrossRefGoogle Scholar
  96. Husseini M.K., Jorge Q.A., Sporn J., Payne J.L., Denicoff K., Gray N.A., Zarate Jr. C.A., Charney D.S. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 2003; Apr 15; 53(8): 707–742CrossRefGoogle Scholar
  97. Huttenlocher P.R., Hapke R.J. A follow-up study of intractable seizures in childhood. Ann. Neurol 1990; 28:699–705PubMedCrossRefGoogle Scholar
  98. Ikononomidou C., Bosch F., Miksa M., Bittigua P., Vockler J., Dikranian K., Tenkova T., Stefovska V., Turski L., Olney J. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999; 283:74CrossRefGoogle Scholar
  99. Jefferys J.G., Evans B.J., Hughes S.A., Williams S.F. Neuropathology of the chronic epileptic syndrome induced by intrahippocampal tetanus toxin in rat: preservation of pyramidal cells and incidence of dark cells. Neuropathol Appl Neurobiol 1992; Feb;18(1):53–70PubMedCrossRefGoogle Scholar
  100. Jensen F.E., Baram T.Z. Developmental seizures induced by common early-life insults: short-and long-term effects on seizure susceptibility. Ment Retard Dev Disabil Res Rev 2000; 6(4):253–7.PubMedCrossRefGoogle Scholar
  101. Jones P.A., Smith R.A., Stone T.W. Nitric oxide synthase inhibitors L-NAME and 7-nitroindazole protect rat hippocampus against kainate-induced excitotoxicity, Neurosci Lett 1998; Jun 19;249(2–3):75–8PubMedCrossRefGoogle Scholar
  102. Jope R.S., Morrisett R.A., Snead D.C. Characterization of lithium potentiation of pilocarpine-induced status epilepticus in rats. Exp Neurol 1986; Mar;91(3):471–80PubMedCrossRefGoogle Scholar
  103. Kant R., Bogyi A.M., Carosella N.W., Fishman E., Kane V., Coffey C.E. ECT as a therapeutic option in severe brain injury. Convuls Ther 1995; Mar; 11(1):45–50PubMedGoogle Scholar
  104. Kellner C.H., Beale M.D., Pritchett J.T., Bernstein H.J., Bums C.M. Electroconvulsive therapy and Parkinson’s disease: the case for further study. Psychopharmacol Bull 1994; 30(3):495–500PubMedGoogle Scholar
  105. Kelly M.E., McIntyre D.C. Hippocampal kindling protects several structures from the neuronal damage resulting from kainic acid-induced status epilepticus. Brain Res 1994; Jan 21;634(2):245–56PubMedCrossRefGoogle Scholar
  106. Kempermann G., Van Praag H., Gage F. H. Activity-dependent regulation of neuronal plasticity and self repair. Prog. Brain Res 2000; 127:35–48PubMedCrossRefGoogle Scholar
  107. Klitgaard H., Matagne A., Vanneste-Goemaere J., Margineanu D.G. Pilocarpine-induced epileptogenesis in the rat: impact of initial duration of status epilepticus on electrophysiological and neuropathological alterations. Epilepsy Res 2002; Sep;51(1–2):93–107PubMedCrossRefGoogle Scholar
  108. Kobayashi E., Li L.M., Lopes-Cendes I., Cendes F. Magnetic resonance imaging evidence of hippocampal sclerosis in asymptomatic, first-degree relatives of patients with familial mesial temporal lobe epilepsy. Arch Neurol 2002; Dec;59(12): 1891–4PubMedCrossRefGoogle Scholar
  109. Kondratyev A., Ved R., Gale K. The effects of repeated minimal electroconvulsive shock exposure on levels of mRNA encoding fibroblast growth factor-2 and nerve growth factor in limbic regions. Neuroscience 2002; 114(2):411–6PubMedCrossRefGoogle Scholar
  110. Kondratyev A., Gale K. Temporal and spatial patterns of DNA fragmentation following focally or systemically-evoked status epilepticus in rats. Neurosci Lett 2001; 310:13–16PubMedCrossRefGoogle Scholar
  111. Kondratyev A., Sahibzada N., Gale K. Electroconvulsive shock exposure prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Mol Brain Res 2001; 91: 1–13PubMedCrossRefGoogle Scholar
  112. Kondratyev A., Gale K. Intracerebral injection of caspase-3 inhibitor prevents neuronal apoptosis after kainic acid-evoked status epilepticus. Brain Res Mol Brain Res 2000; 75: 216–224PubMedCrossRefGoogle Scholar
  113. Kornblum H.I., Sankar R., Shin D.H., Wasterlain CG., Gall C.M. Induction of brain derived neurotrophic factor mRNA by seizures in neonatal and juvenile rat brain. Mol Brain Res 1997; 44:219–228PubMedCrossRefGoogle Scholar
  114. Kotloski R., Lynch M., Lauersdorf S., Sutula T. Repeated brief seizures induce progressive hippocampal neuron loss and memory deficits. Prog Brain Res 2002; 135:95–110PubMedCrossRefGoogle Scholar
  115. Kuan C.Y., Roth K.A., Flavell R.A., Rakic P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci 2000; 23:291–297PubMedCrossRefGoogle Scholar
  116. Kudryashov I.E., Onufriev M.V., Kudryashova I.V., Gulyaeva N.V. Periods of postnatal maturation of hippocampus: synaptic modifications and neuronal disconnection. Dev Brain Res 2001; 132:113–120CrossRefGoogle Scholar
  117. Kuks J.B., Cook M.J., Fish D.R., Stevens J.M., Shorvon S.D. Hippocampal sclerosis in epilepsy and childhood febrile seizures. Lancet 1993; Dec 4;342(8884): 1391–4PubMedCrossRefGoogle Scholar
  118. Kunz W.S., Goussakov I.V., Beck H., Elger C.E. Altered mitochondrial oxidative phosphorylation in hippocampal slices of kainate-treated rats. Brain Res 1999; 826:236–242PubMedCrossRefGoogle Scholar
  119. Kunz W.S., Kudin A.P., Vielhaber S., Blumcke I., Zuschratter W., Schramm J., Beck H., Elger C.E. Mitochondrial complex I deficiency in the epileptic focus of patients with temporal lobe epilepsy. Ann. Neurol 2000; 48:766–773PubMedCrossRefGoogle Scholar
  120. Lado F.A., Sankar R., Lowenstein D., Moshe S.L. Age-dependent consequences of seizures: relationship to seizure frequency, brain damage, and circuitry reorganization. Ment Retard Dev Disabil Res Rev 2000; 6(4):242–52PubMedCrossRefGoogle Scholar
  121. Lewis D.V., Barboriak D.P., MacFall J.R., Provenzale J.M., Mitchell T.V., VanLandingham K.E. Do prolonged febrile seizures produce medial temporal sclerosis? Hypotheses, MRI evidence and unanswered questions. Prog Brain Res 2002; 135:263–78PubMedCrossRefGoogle Scholar
  122. Lewis D.V. Febrile convulsions and mesial temporal sclerosis. Curr Opin Neurol 1999; Apr; 12(2):197–201PubMedCrossRefGoogle Scholar
  123. Liang L.P., Ho Y.S., Patel M. Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience 2000; 101(3):563–70PubMedCrossRefGoogle Scholar
  124. Liou A.K., Clark R.S., Henshall D.C., Yin X.M., Chen J. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 2003; Feb;69(2):103–42PubMedCrossRefGoogle Scholar
  125. Liposits Z., Kallo I., Hrabovszky E., Gallyas F. Ultrastructural pathology of degenerating “dark” granule cells in the hippocampal dentate gyrus of adrenalectomized rats. Acta Biol Hung 1997; 48(2):173–87PubMedGoogle Scholar
  126. Liu Z., D’Amore P.A., Mikati M., Gatt A., Holmes G.L. Neuroprotective effect of chronic infusion of basic fibroblast growth factor on seizure-associated hippocampal damage. Brain Res 1993; Oct 29;626 (1–2):335–8PubMedCrossRefGoogle Scholar
  127. Liu Z., Holmes G.L. Basic fibroblast growth factor is highly neuroprotective against seizure-induced long-term behavioural deficits. Neuroscience 1997; Feb;76(4):1129–38PubMedCrossRefGoogle Scholar
  128. Liu Z., Yang Y., Silveira D.C., Sarkisian M.R., Tandon P., Huang L.T., Stafstrom C.E., Holmes G.L. Consequences of recurrent seizures during early brain development. Neuroscience 1999; 92:1443–1454PubMedCrossRefGoogle Scholar
  129. Lothman E.W., Bertram E.H. 3rd. Epileptogenic effects of status epilepticus. Epilepsia 1993; 34 Suppl 1:S59–70PubMedCrossRefGoogle Scholar
  130. Lowenstein D.H., Arsenault L. The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons. J Neurosci 1996; 16:1759–1769PubMedGoogle Scholar
  131. Lumme A., Soinila S., Sadeniemi M., Halonen T., Vanhatalo S. Nitric oxide synthase immunoreactivity in the rat hippocampus after status epilepticus induced by perforant pathway stimulation. Brain Res 2000; 871:303–310PubMedCrossRefGoogle Scholar
  132. Lynch M., Sayin U., Bownds J., Janumpalli S., Sutula T. Long-term consequences of early postnatal seizures on hippocampal learning and plasticity. Eur J Neurosci 2000; Jul;12(7):2252–64PubMedCrossRefGoogle Scholar
  133. Maggio R., Liminga U., Gale K. Selective stimulation of kainate but not quisqualate or NMDA receptors in substantia nigra evokes limbic motor seizures. Brain Res 1990; Oct 1;528(2):223–30PubMedCrossRefGoogle Scholar
  134. Maher J., McLachlan R.S. Febrile convulsions. Is seizure duration the most important predictor of temporal lobe epilepsy? Brain 1995; Dec;118 (Pt 6):1521–8PubMedCrossRefGoogle Scholar
  135. Maher J., McLachlan R.S. Febrile convulsions. Is seizure duration the most important predictor of temporal lobe epilepsy? Brain 1995; Dec;118 (Pt 6):1521–8PubMedCrossRefGoogle Scholar
  136. Manji H.K., Quiroz J.A., Sporn J., Payne J.L., Denicoff K.A., Gray N., Zarate C.A. Jr., Charney D.S. Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 2003; Apr 15;53(8):707–42PubMedCrossRefGoogle Scholar
  137. Masco D., Sahibzada N., Switzer R., Gale K. Electroshock seizures protect against apoptotic hippocampal cell death induced by adrenalectomy. Neuroscience 1999; 91(4):1315–1319PubMedCrossRefGoogle Scholar
  138. Mathern G.W., Adelson P.D., Cahan L.D., Leite J.P. Hippocampal neuron damage in human epilepsy: Meyer’s hypothesis revisited. Prog Brain Res 2002; 135:237–51PubMedCrossRefGoogle Scholar
  139. Mattson M.P., Kumar K.N., Wang H., Cheng B., Michaelis E.K. Basic FGF regulates the expression of a functional 71 kDa NMDA receptor protein that mediates calcium influx and neurotoxicity in hippocampal neurons. J Neurosci 1993; Nov;13(11):4575–88PubMedGoogle Scholar
  140. Mattson M.P., Lovell M.A., Furukawa K., Markesbery W.R. Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 1995; Oct;65(4):1740–51Google Scholar
  141. Mayat E., Lerner-Natoli M., Rondouin G., Lebrun F., Sassetti I., Reasens M. Kainate-induced status epilepticus leads to a delayed increase in various specific glutamate metabotropic receptor responses in the hippocampus. Brain Res 1994; May 9;645(1–2):186–200PubMedCrossRefGoogle Scholar
  142. McIntyre D.C., Nathanson D., Edson N. A new model of partial status epilepticus based on kindling. Brain Res 1982; Oct 28;250(1):53–63PubMedCrossRefGoogle Scholar
  143. McIntyre D.C., Poulter M.O., Gilby K. Kindling: some old and some new. Epilepsy Res 2002; Jun;50(1–12):79–92PubMedCrossRefGoogle Scholar
  144. Meier P, Finch A., Evan G. Apoptosis in development. Nature 2000; 407: 797–801CrossRefGoogle Scholar
  145. Meldrum B.S., Horton R.W., Brierley J.B. Epileptic brain damage in adolescent baboons following seizures induced by allylgycine. Brain 1974; Jun;97(2):407–18PubMedCrossRefGoogle Scholar
  146. Meldrum B.S., Papy J.J., Toure M.F., Brierley J.B. Four models for studying cerebral lesions secondary to epileptic seizures. Adv Neurol 1975; 10:147–61PubMedGoogle Scholar
  147. Meldrum B.S., Vigouroux R.A., Brierley J.B. Systemic factors and epileptic brain damage. Prolonged seizures in paralyzed artificially ventilated baboons. Arch Neurol 1973a; Aug;29(2):82–7PubMedCrossRefGoogle Scholar
  148. Meldrum B.S., Vigouroux R.A., Rage P., Brierley J.B. Hippocampal lesions produced by prolonged seizures in paralyzed artificially ventilated baboons. Experientia 1973b; May 15;29(5):561–3PubMedCrossRefGoogle Scholar
  149. Meldrum B.S. Metabolic factors during prolonged seizures and their relation to nerve cell death. Adv Neurol 1983; 34:261–75PubMedGoogle Scholar
  150. Meldrum B.S. Excitotoxicity and epileptic brain damage. Epilepsy Res 1991; 10:55–61PubMedCrossRefGoogle Scholar
  151. Meletti S., Benuzzi F., Rubboli G., Cantalupo G., Stanzani Maserati M., Nichelli P., Tassinari C.A. Impaired facial emotion recognition in early-onset right mesial temporal lobe epilepsy. Neurology 2003; Feb 11;60(3):426–31PubMedCrossRefGoogle Scholar
  152. Milatovic D., Gupta R.C., Dettbam W.D. Involvement of nitric oxide in kainic acid-induced excitotoxicity in rat brain. Brain Research 2002; 957:330–337PubMedCrossRefGoogle Scholar
  153. Mizrahi E.M., Clancy R.R. Neonatal seizures: early-onset seizure syndromes and their consequences for development. Ment Retard Dev Disabil Res Rev 2000; 6(4):229–41PubMedCrossRefGoogle Scholar
  154. Mody I. Synaptic plasticity in kindling. Adv Neurol 1999; 79:631–43PubMedGoogle Scholar
  155. Mohapel P., Dufresne C., Kelly M.E., McIntyre D.C. Differential sensitivity of various temporal lobe structures in the rat to kindling and status epilepticus induction. Epilepsy Res 1996; Apr;23(3):179–87PubMedCrossRefGoogle Scholar
  156. Montecot C., Rondi-Reig L., Springhetti V., Seylaz J., Pinard E. Inhibition of neuronal (type 1) nitric oxide synthase prevents hyperaemia and hippocampal lesions resulting from kainate-induced seizures. Neuroscience 1998; Jun;84(3):791–800PubMedCrossRefGoogle Scholar
  157. Morrisett R.A., Jope R.S., Snead O.C. III. Status epilepticus is produced by administration of cholinergic agonists to lithiumtreated rats: comparison with kainic acid. Exp Neurol 1987; 98:594–605PubMedCrossRefGoogle Scholar
  158. Morrison R.S., Wenzel H.J., Kinoshita Y., Robbins C.A., Donehower L.A., Schwartzkroin P. A. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 1996; Feb 5;16(4):1337–45PubMedGoogle Scholar
  159. Moshe S.L. Brain injury with prolonged seizures in children and adults. J Child Neurol 1998; Oct;13 Suppl 1:S3–6PubMedCrossRefGoogle Scholar
  160. Najm I.M., Hadam J., Ckakraverty D., Mikuni N., Penrod C., Sopa C., Markarian G., Luders H.O., Babb T., Baudry M. A short episode of seizure activity protects from status epilepticus-induced neuronal damage in rat brain. Brain Res 1998; Nov 9;81O(1–12):72–5CrossRefGoogle Scholar
  161. Narkilahti S., Nissinen J., Pitkanen A. Administration of caspase 3 inhibitor during and after status epilepticus in rat: effect on neuronal damage and epileptogenesis. Neuropharmacology 2003; Jun;44(8):1068–88PubMedCrossRefGoogle Scholar
  162. Naruse I., Keino H. Apoptosis in the developing CNS. Prog Neurobiol 1995; 47:135–155PubMedCrossRefGoogle Scholar
  163. Naylor P., Stewart C.A., Wright S.R., Pearson R.C., Reid I.C. Repeated ECS induces GluRI mRNA but not NMDARIA-G mRNA in the rat hippocampus. Brain Res Mol Brain Res 1996; Jan;35(1–2):349–53PubMedCrossRefGoogle Scholar
  164. Nevander G., Ingvar M., Auer R., Siesjo B.K. Status epilepticus in well-oxygenated rats causes neuronal necrosis. Ann Neurol 1985; 18:281–90PubMedCrossRefGoogle Scholar
  165. Nibuya M., Morinobu S., Duman R.S. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995; Nov;15(11):7539–47PubMedGoogle Scholar
  166. Olney J.W., Wozniak D.F., Jevtovic-Todorovic Y., Farber N.B., Bittigau P., Ikonomidou C. Drug-induced apoptotic neurodegeneration in the developing brain. Brain Pathol 2002; Oct;12(4):488–98PubMedCrossRefGoogle Scholar
  167. Oppenheim R W. Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14:453–501PubMedCrossRefGoogle Scholar
  168. Pekary A.E., Meyerhoff J.L, Sattin A. Electroconvulsive seizures modulate levels of thyrotrop in releasing hormone and related peptides in rat hypothalamus, cingulate and lateral cerebellum. Brain Res 2000; Nov 24;884(1–2):174–83CrossRefGoogle Scholar
  169. Pelletier M.R., Wadia J.S., Mills L.R., Carlen P.L. Seizure-induced cell death produced by repeated tetanic stimulation in vitro: possible role of endoplasmic reticulum calcium stores. J Neurophysiol 1999; 81:3054–3064PubMedGoogle Scholar
  170. Penner M.R., Pinaud R., Robertson H.A. Rapid kindling of the hippocampus protects against neural damage resulting from status epilepticus. NeuroReport 2001; 12(3): 453–457PubMedCrossRefGoogle Scholar
  171. Pinard E., Tremblay E., Ben-Ari Y., Seylaz J. Blood flow compensates oxygen demand in the vulnerable CA3 regions of the hippocampus during kainate-induced seizures. Neuroscience 1984; 13:1039–1049PubMedCrossRefGoogle Scholar
  172. Plamondon H., Blondeau N., Heurteaux C., Lazdunski M. Mutually protective actions of kainic acid epileptic preconditioning and sublethal global ischemia on hippocampal neuronal death: involvement of adenosine A1 receptors and K(ATP) channels. J Cereb Blood Flow Metab 1999; Dec;19(12):1296–308PubMedCrossRefGoogle Scholar
  173. Pollard H., Cantagrel S., Charriaut-Marlangue C., Moreau J., Ben-Ari Y. Apoptosis associated DNA fragmentation in epileptic brain damage. NeuroReport 1994; 5:1053–1055PubMedCrossRefGoogle Scholar
  174. Portera-Cailliau C., Price D.L., Martin L.J. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997; Feb 3;378(1):70–87PubMedGoogle Scholar
  175. Portera-Cailliau C., Price D.L., Martin L.J. Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J Comp Neurol 1997; Feb 3;378(1):88–104PubMedCrossRefGoogle Scholar
  176. Pridmore S., Pollard C. Electroconvulsive therapy in Parkinson’s disease: 30 month follow up. J Neurol Neurosurg Psychiatry 1996; Jun;60(6):693PubMedCrossRefGoogle Scholar
  177. Puig B., Ferrer I. Caspase-3-associated apoptotic cell death in excitotoxic necrosis of the entorhinal cortex following intraperitoneal injection of kainic acid in the rat. Neurosci Lett 2002; Mar 22;321(3):182–6PubMedCrossRefGoogle Scholar
  178. Racine R.J., Adams B., Osehobo P., Fahnestock M. Neural growth, neural damage and neurotroph ins in the kindling model of epilepsy. Adv Exp Med Biol 2002; 497:149–70PubMedCrossRefGoogle Scholar
  179. Rasmussen K., Abrams R. Treatment of Parkinson’s disease with electroconvulsive therapy. Psychiatr Clin North Am 1991; Dec;14(4):925–33PubMedGoogle Scholar
  180. Reti I.M., Baraban J.M. Sustained increase in Narp protein expression foIlowing repeated electroconvulsive seizure. Neuropsychopharmacology 2000; Oct;23(4):439–43PubMedCrossRefGoogle Scholar
  181. Roy M., Sapolsky R. Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? Trends Neurosci 1999; Oct;22(10):419–22PubMedCrossRefGoogle Scholar
  182. Sakhi S., Sun N., Wing L.L., Mehta P., Schreiber S.S. Nuclear accumulation of p53 protein following kainic acid-induced seizures. NeuroReport 1996; 7:493–496PubMedCrossRefGoogle Scholar
  183. Sandyk R. Mechanisms of action of ECT in Parkinson’s disease: possible role of pineal melatonin. Int J Neurosci 1990; Jan;50(1–2):83–94PubMedCrossRefGoogle Scholar
  184. Sankar R., Shin D.H., Liu H., Mazarati A., Pereira de Vasconcelos A., Wasterlain C.G. Patterns of status epilepticus-induced neuronal injury during development and long-term consequences. J Neurosci 1998; 18:8382–93PubMedGoogle Scholar
  185. Sasahira M., Lowry T., Simon R.P., Greenberg D.A. Epileptic tolerance: prior seizures protect against seizure-induced neuronal injury. Neurosci Lett 1995; Feb 9;185(2):95–8PubMedCrossRefGoogle Scholar
  186. Sasahira M., Simon R.P., Greenberg D.A. Neuronal injury in experimental status epilepticus in the rat: role of hypoxia. Neurosci Lett 1997; Feb 7;222(3):207–9PubMedCrossRefGoogle Scholar
  187. Sasahira M., Lowry T., Simon R.P., Greenberg D.A. Epileptic tolerance: prior seizures protect against seizure-induced neuronal injury. Neurosci. Lett 1995; 185:95–98PubMedCrossRefGoogle Scholar
  188. Sater R.A., Nadler J.V. On the relation between seizures and brain lesions after intracerebroventricular kainic acid. Neurosci Lett 1988; Jan 11;84(1):73–8PubMedCrossRefGoogle Scholar
  189. Sato K., Kashihara K., Morimoto K., Hayabara T. Regional increases in brain-derived neurotrophic factor and nerve growth factor mRNAs during amygdaloid kindling, but not in acidic and basic fibroblast growth factor mRNAs. Epilepsia 1996; Jan;37(1):6–14PubMedCrossRefGoogle Scholar
  190. Schallert T., Hernandez T.D., Barth T.M. Recovery of function after brain damage: severe and chronic disruption by diazepam. Brain Res 1986; Jul 30;379(1):104–11PubMedCrossRefGoogle Scholar
  191. Schauwecker P.E. Complications associated with genetic background effects in models of experimental epilepsy. Prog Brain Res 2002; 135:139–48PubMedCrossRefGoogle Scholar
  192. Schauwecker P.E. Genetic background as a determinant of seizure-induced ceIl death 2002 http://www.aesnet.org/edu_pub/PresidentialSymposium.cfm
  193. Schmid R., Tandon P., Stafstrom C.E., Holmes G.L. Effects of neonatal seizures on subsequent seizure-induced brain injury. Neurology 1999; 53(8):1754–1761PubMedCrossRefGoogle Scholar
  194. Schulz R., Ebner A. Prolonged febrile convulsions and mesial temporal lobe epilepsy in an identical twin. Neurology 2001; Jul 24;57(2):318–20PubMedCrossRefGoogle Scholar
  195. 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; 5:991–1014PubMedCrossRefGoogle Scholar
  196. Scott R.C., Gadian D.G., King M.D., Chong W.K., Cox T.C., Neville B.G., Connelly A. Magnetic resonance imaging findings within 5 days of status epilepticus in childhood. Brain 2002; Sep;125(Pt 9):1951–9. Erratum in: Brain 2002; Dec; 125(Pt 12):2792PubMedCrossRefGoogle Scholar
  197. Sheline Y.I., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999; 19(12): 5034–5043PubMedGoogle Scholar
  198. Shimosaka S., So Y.T., Simon R.P. Distribution of HSP72 induction and neuronal death following limbic seizures. Neurosci Lett 1992; Apr 27; 138(2):202–6PubMedCrossRefGoogle Scholar
  199. Shinnar S., Berg A.T., Moshe S.L., O’Dell C., Alemany M., Newstein D., Kang H., Goldensohn E.S., Hauser W.A. The risk of seizure recurrence after a first unprovoked afebrile seizure in childhood: an extended follow-up. Pediatrics 1996; Aug;98(2 Pt 1):216–25PubMedGoogle Scholar
  200. Shinnar S., Glauser T.A. Febrile seizures. J Child Neurol 2002; Jan; 17 Suppl 1:S44–52PubMedCrossRefGoogle Scholar
  201. Shinnar S., Pellock J.M., Berg A.T., O’Dell C., Driscoll S.M., Maytal J., Moshe S.L., DeLorenzo R.J. Short-term outcomes of children with febrile status epilepticus. Epilepsia 2001; Jan;42(1):47–53PubMedCrossRefGoogle Scholar
  202. Shorvon S. Status Epilepticus. J Neurol Neurosurg Psychiatry 2001; Jun;70 Suppl 2:1122–7Google Scholar
  203. Sloviter R.S. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 1992; 137:91–96PubMedCrossRefGoogle Scholar
  204. Sloviter R.S., Dean E., Neubort S. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: apoptosis in the adult central nervous system. J Comp Neurol 1993; Apr 15;330(3):337–51PubMedCrossRefGoogle Scholar
  205. Sloviter R.S., Dean E., Sollas A.L., Goodman J.H. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol 1996; Mar 11;366(3):516–33PubMedCrossRefGoogle Scholar
  206. Sloviter R.S., Lowenstein D.H. Heat shock protein expression in vulnerable cells of the rat hippocampus as an indicator of excitation-induced neuronal stress. J Neurosci 1992; Aug;12(8):3004–9PubMedGoogle Scholar
  207. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.L., Paul L.A., Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 1989; Jan 27;243(4890):535–8PubMedCrossRefGoogle Scholar
  208. Sloviter R.S., Damiano B.P. Sustained electrical stimulation of the perforant path duplicates kainate-induced electrophysiological effects and hippocampal damage in rats. Neurosci. Lett 1981; 24:279–284PubMedCrossRefGoogle Scholar
  209. Sogawa Y., Monokoshi M., Silveira D.C., Cha B.H., Cilio M.R., McCabe B.K., Liu X., Hu Y, Holmes G.L. Timing of cognitive deficits following neonatal seizures: relationship to histological changes in the hippocampus. Brain Res Dev Brain Res 2001; 26:73–83CrossRefGoogle Scholar
  210. Sommer C., Roth S.U., Kiessling M. Kainate-induced epilepsy alters protein expression of AMPA receptor subunits GluR1, GluR2 and AMPA receptor binding protein in the rat hippocampus. Acta Neuropathol (Berl) 2001; May; 101(5):460–8Google Scholar
  211. Sperber E.F., Haas K.Z., Stanton P.K., Moshe S.L. Resistance of the immature hippocampus to seizure-induced synaptic reorganization. Brain Res Dev Brain Res 1991; 60:88–93PubMedCrossRefGoogle Scholar
  212. Sperber E.F., Haas K.Z., Romero M.T., Stanton P.K. Flurothyl status epilepticus in developing rats: behavioral, electrographic histological and electrophysiological studies. Brain Res Dev Brain Res 1999; Aug 5;116(1):59–68PubMedCrossRefGoogle Scholar
  213. Sperk G., Lassmannv H., Baran H., Kish S.J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 1983; 10:1301–1315PubMedCrossRefGoogle Scholar
  214. Stafstrom C.E., Thompson J.L., Holmes G.L. Kainic acid seizures in the developing brain: status epilepticus and spontaneous recurrent seizures. Brain Res Dev Brain Res 1992; Feb 21;65(2):227–36PubMedCrossRefGoogle Scholar
  215. Stern M.B. Electroconvulsive therapy in untreated Parkinson’s disease. Mov Disord 1991; 6(3):265PubMedCrossRefGoogle Scholar
  216. Sullivan P.G., Dube C., Dorenbos K., Steward O., Baram T.Z. Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death. Ann Neurol 2003; 53(6):711–7PubMedCrossRefGoogle Scholar
  217. Sutula T.P., Pitkanen A. More evidence for seizure-induced neuron loss: is hippocampal sclerosis both cause and effect of epilepsy? Neurology 2001; Jul 24;57(2):169–70PubMedCrossRefGoogle Scholar
  218. Swann J., Smith K., Lee C. Neuronal activity and the establishment of normal and epileptic circuits during brain development. Int’l Rev Neurobio 2001; 45:89–118CrossRefGoogle Scholar
  219. Tanaka K., Simon R.P. The pattern of neuronal injury following seizures induced by intranigral kainic acid. Neurosci Lett 1994; Aug 1;176(2):205–8PubMedCrossRefGoogle Scholar
  220. Tandon P., Yang Y., Das K., Holmes G.L., Stafstrom C.E. Neuroprotective effects of brain derived neurotrophic factor in seizures during development. Neuroscience 1999; 91:293–303PubMedCrossRefGoogle Scholar
  221. Tang F.R., Lee W.L., Yang J., Sim M.K., Ling E.A. Expression of metabotropic glutamate receptor 1alpha in the hippocampus of rat pilocarpine model of status epilepticus. Epilepsy Res 2001; Aug;46(2): 179–89PubMedCrossRefGoogle Scholar
  222. Tang F.R., Lee W.L., Yang J., Sim M.K., Ling E.A. Metabotropic glutamate receptor 8 in the rat hippocampus after pilocarpine induced status epilepticus. Neurosci Lett 2001; Mar 16;300(3):137–40PubMedCrossRefGoogle Scholar
  223. Tarkka R., Paakko E., Pyhtinen J., Uhari M., Rantala H. Febrile seizures and mesial temporal sclerosis: No association in a long-term follow-up study. Neurology 2003; Jan 28;60(2):215–8PubMedCrossRefGoogle Scholar
  224. Tasch E., Cendes F., Li L.M., Dubeau F., Andermann F., Arnold D.L. Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol 1999;45: 568–76PubMedCrossRefGoogle Scholar
  225. Theodore W.H., Bhatia S., Hatta J., Fazilat S., DeCarli C., Bookheimer S.Y., et al. Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures. Neurology 1999; 52:132–6PubMedCrossRefGoogle Scholar
  226. Theodore W.H., DeCarli C., Gaillard W.D. Total cerebral volume is reduced in patients with localization-related epilepsy and a history of complex febrile seizures. Arch Neurol 2003; Feb;60(2):250–2PubMedCrossRefGoogle Scholar
  227. Toth Z., Yan X., Haftoglou S., Ribak C., Baram T. Seizure-induced neuronal injury: Vulnerability to febrile seizures in an immature rat model. J. Neuroscience 1998; 18(11):4285–4294Google Scholar
  228. Towfighi J., Housman C., Mauger D., Vannucci R.C. Effect of seizures on cerebral hypoxic-ischemic lesions in immature rats. Brain Res Dev Brain Res 1999; Mar 12;113(1–2): 83–95CrossRefGoogle Scholar
  229. Treiman D.M., Walton N.Y., Gunawan S. Brain amino acid concentrations during specific electroencephalographic stages of status epilepticus in the rat. Epilepsy Res 1992 Suppl. 8:283–94Google Scholar
  230. Turski L., Ikonomidou C., Turski W.A., Bortolotto Z.A., Cavalheiro E.A. Cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel model of intractable epilepsy. Synapse 1989; 3:154–171PubMedCrossRefGoogle Scholar
  231. Tuunanen J., Pitkanen A. Do seizures cause neuronal damage in rat amygdala kindling? Epilepsy Res 2000; Apr;39(2):171–6PubMedCrossRefGoogle Scholar
  232. Ulas J., Satou T., Ivins K.J., Kesslak J.P., Cotman C.W., Balazs R. Expression of metabotropic glutamate receptor 5 is increased in astrocytes after kainate-induced epileptic seizures. Glia 2000; Jun;30(4):352–61PubMedCrossRefGoogle Scholar
  233. Vezzani A., Moneta D., Richichi C., Aliprandi M., Burrows S.J., Ravizza T., Perego C., De Simoni M.G. Functional role of inflammatory cytokines and antiinflammatory molecules in seizures and epileptogenesis. Epilepsia 2002; 43 Suppl 5:30–5PubMedCrossRefGoogle Scholar
  234. Wasterlain C.G., Shirasaka Y., Mazarati A.M., Spigelman I. Chronic epilepsy with damage restricted to the hippocampus: possible mechanisms. Epilepsy Res 1996; Dec;26(1):255–65PubMedCrossRefGoogle Scholar
  235. Yager J.Y., Armstrong E.A., Miyashita H., Wirrell E.C. Prolonged neonatal seizures exacerbate hypoxic-ischemic brain damage: correlation with cerebral energy metabolism and excitatory amino acid release. Dev Neurosci 2002; 24(5):367–81PubMedCrossRefGoogle Scholar
  236. Yang Y., Tandon P., Liu Z., Sarkisian M.R., Stafstrom C.E., Holmes G.L. Synaptic reorganization following kainic acid-induced seizures during development. Brain Res Dev Brain Res 1998; 107:169–177PubMedCrossRefGoogle Scholar
  237. Yang D.D., Kuan C.Y., Whitmarsh A.J., Rincon M., Zheng T.S., Davis R.J., Rakic P., Flavell R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997; 389:865–870PubMedCrossRefGoogle Scholar
  238. Zhang J., Lee H., Agarwala A., Wen Lou D., Xu M. DNA fragmentation factor 45 mutant mice exhibit resistance to kainic acid-induced neuronal cell death. Biochem Biophys Res Commun 2001; Aug 3;285(5):1143–9PubMedCrossRefGoogle Scholar
  239. Zhang L.X., Smith M.A., Kim S.Y., Rosen J.B., Weiss S.R., Post R.M. Changes in cholecystokinin mRNA expression after amygdala kindled seizures: an in situ hybridization study. Brain Res Mol Brain Res 1996; Jan;35(1–2);278–84PubMedCrossRefGoogle Scholar
  240. Zhang X., Cui S.S., Wallace A.E., Hannesson D.K., Schmued L.C., Saucier D.M., Honer W.G., Corcoran M.E. Relations between brain pathology and temporal lobe epilepsy. J Neurosci 2002; Jul 15;22(14):6052–61PubMedGoogle Scholar
  241. Zhang X., Gelowitz D.L., Lai C.T., Boulton A.A., Yu P.H. Gradation of kainic acid-induced rat limbic seizures and expression of hippocampal heat shock protein-70. Eur J Neurosci 1997; 9:760–769PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2004

Authors and Affiliations

  • Karen Gale
    • 1
  1. 1.Department of PharmacologyGeorgetown UniversityWashingtonUSA

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