Table of Contents Author Guidelines Submit a Manuscript
Epilepsy Research and Treatment
Volume 2012 (2012), Article ID 342928, 9 pages
http://dx.doi.org/10.1155/2012/342928
Review Article

Atypical Febrile Seizures, Mesial Temporal Lobe Epilepsy, and Dual Pathology

1Département de Pédiatrie, Centre de Recherche du Centre Hospitalier Universitaire (CHU) Sainte-Justine, Université de Montréal, Montréal, QC, Canada H3T 1C5
2Département de Physiologie, Faculté de Médecine, Université de Montréal, Montréal, QC, Canada H3C 3J7

Received 25 December 2011; Revised 2 February 2012; Accepted 7 February 2012

Academic Editor: Seyed M. Mirsattari

Copyright © 2012 Nathalie T. Sanon et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Engel, “Mesial temporal lobe epilepsy: what have we learned?” Neuroscientist, vol. 7, no. 4, pp. 340–352, 2001. View at Google Scholar · View at Scopus
  2. S. Gibbs, B. Chattopadhyaya, S. Desgent et al., “Long-term consequences of a prolonged febrile seizure in a dual pathology model,” Neurobiology of Disease, vol. 43, no. 2, pp. 312–321, 2011. View at Publisher · View at Google Scholar
  3. M. H. Scantlebury and J. G. Heida, “Febrile seizures and temporal lobe epileptogenesis,” Epilepsy Research, vol. 89, no. 1, pp. 27–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. K. E. VanLandingham, E. R. Heinz, J. E. Cavazos, and D. V. Lewis, “Magnetic resonance imaging evidence of hippocampal injury after prolonged focal febrile convulsions,” Annals of Neurology, vol. 43, no. 4, pp. 413–426, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Ahmad and E. D. Marsh, “Febrile status epilepticus: current state of clinical and basic research,” Seminars in Pediatric Neurology, vol. 17, no. 3, pp. 150–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. A. T. Berg, S. Shinnar, S. R. Levy, and F. M. Testa, “Childhood-onset epilepsy with and without preceding febrile seizures,” Neurology, vol. 53, no. 8, pp. 1742–1748, 1999. View at Google Scholar · View at Scopus
  7. L. Carmant, “Developing a new animal model of temporal lobe epilepsy,” Medecine/Sciences, vol. 23, no. 11, pp. 929–933, 2007. View at Google Scholar · View at Scopus
  8. S. McClelland, C. M. Dubé, J. Yang, and T. Z. Baram, “Epileptogenesis after prolonged febrile seizures: mechanisms, biomarkers and therapeutic opportunities,” Neuroscience Letters, vol. 497, no. 3, pp. 155–162, 2011. View at Publisher · View at Google Scholar
  9. M. H. Scantlebury, S. A. Gibbs, B. Foadjo, P. Lema, C. Psarropoulou, and L. Carmant, “Febrile seizures in the predisposed brain: a new model of temporal lobe epilepsy,” Annals of Neurology, vol. 58, no. 1, pp. 41–49, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Shinnar and T. A. Glauser, “Febrile seizures,” Journal of Child Neurology, vol. 17, no. 1, pp. S44–S52, 2002. View at Google Scholar · View at Scopus
  11. C. Dubé, C. Richichi, R. A. Bender, G. Chung, B. Litt, and T. Z. Baram, “Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis,” Brain, vol. 129, no. 4, pp. 911–922, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. S. A. Gibbs, M. H. Scantlebury, P. Awad et al., “Hippocampal atrophy and abnormal brain development following a prolonged hyperthermic seizure in the immature rat with a focal neocortical lesion,” Neurobiology of Disease, vol. 32, no. 1, pp. 176–182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. W. H. Theodore, S. Bhatia, J. Hatta et al., “Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures,” Neurology, vol. 52, no. 1, pp. 132–136, 1999. View at Google Scholar · View at Scopus
  14. K. B. Nelson and J. H. Ellenberg, “Predictors of epilepsy in children who have experienced febrile seizures,” New England Journal of Medicine, vol. 295, no. 19, pp. 1029–1033, 1976. View at Google Scholar · View at Scopus
  15. T. Z. Baram, A. Gerth, and L. Schultz, “Febrile seizures: an appropriate-aged model suitable for long-term studies,” Developmental Brain Research, vol. 98, no. 2, pp. 265–270, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Morimoto, H. Nagao, N. Sano, M. Takahashi, and H. Matsuda, “Electroencephalographic study of rat hyperthermic seizures,” Epilepsia, vol. 32, no. 3, pp. 289–293, 1991. View at Google Scholar · View at Scopus
  17. M. H. Scantlebury, P. L. Ouellet, C. Psarropoulou, and L. Carmant, “Freeze lesion-induced focal cortical dysplasia predisposes to atypical hyperthermic seizures in the immature rat,” Epilepsia, vol. 45, no. 6, pp. 592–600, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Holtzman, K. Obana, and J. Olson, “Hyperthermia-induced seizures in the rat pup: a model for febrile convulsions in children,” Science, vol. 213, no. 4511, pp. 1034–1036, 1981. View at Google Scholar · View at Scopus
  19. T. Morimoto, M. Fukuda, Y. Aibara, H. Nagao, and K. Kida, “The influence of blood gas changes on hyperthermia-induced seizures in developing rats,” Developmental Brain Research, vol. 92, no. 1, pp. 77–80, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. D. L. Hjeresen, A. W. Guy, F. M. Petracca, and J. Diaz, “A microwave-hyperthermia model of febrile convulsions,” Bioelectromagnetics, vol. 4, no. 4, pp. 341–355, 1983. View at Google Scholar · View at Scopus
  21. T. Morimoto, H. Nagao, N. Sano, M. Takahashi, and H. Matsuda, “Hyperthermia-induced seizures with a servo system: neurophysiological roles of age, temperature elevation rate and regional GABA content in the rat,” Brain and Development, vol. 12, no. 3, pp. 279–283, 1990. View at Google Scholar · View at Scopus
  22. M. R. Sarkisian, G. L. Holmes, L. Carmant, Z. Liu, Y. Yang, and C. E. Stafstrom, “Effects of hyperthermia and continuous hippocampal stimulation on the immature and adult brain,” Brain and Development, vol. 21, no. 5, pp. 318–325, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Jiang, T. M. Duong, and N. C. De Lanerolle, “The neuropathology of hyperthermic seizures in the rat,” Epilepsia, vol. 40, no. 1, pp. 5–19, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Dube, K. Chen, M. Eghbal-Ahmadi, K. Brunson, I. Soltesz, and T. Z. Baram, “Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term,” Annals of Neurology, vol. 47, no. 3, pp. 336–344, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. R. A. Bender, C. Dubé, R. Gonzalez-Vega, E. W. Mina, and T. Z. Baram, “Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures,” Hippocampus, vol. 13, no. 3, pp. 399–412, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. H. X. Chen and S. N. Roper, “Reduction of spontaneous inhibitory synaptic activity in experimental heterotopic gray matter,” Journal of Neurophysiology, vol. 89, no. 1, pp. 150–158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. C. M. Dubé, A. L. Brewster, and T. Z. Baram, “Febrile seizures: mechanisms and relationship to epilepsy,” Brain and Development, vol. 31, no. 5, pp. 366–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. J. G. Heida, L. Boissé, and Q. J. Pittman, “Lipopolysaccharide-induced Febrile Convulsions in the rat: short-term sequelae,” Epilepsia, vol. 45, no. 11, pp. 1317–1329, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. M. T. Liebregts, R. S. McLachlan, and L. S. Leung, “Hyperthermia induces age-dependent changes in rat hippocampal excitability,” Annals of Neurology, vol. 52, no. 3, pp. 318–326, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. J. G. Heida and Q. J. Pittman, “Causal links between brain cytokines and experimental febrile convulsions in the rat,” Epilepsia, vol. 46, no. 12, pp. 1906–1913, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Toshihiro, D. E. Tracey, W. M. Mitchell, and E. B. De Souza, “Interleukin-1 receptors in mouse brain: characterization and neuronal localization,” Endocrinology, vol. 127, no. 6, pp. 3070–3078, 1990. View at Google Scholar · View at Scopus
  32. G. Li, S. Bauer, M. Nowak et al., “Cytokines and epilepsy,” Seizure, vol. 20, no. 3, pp. 249–256, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. A. Dinarello, “Infection,fever, and exogenous and endogenous pyrogens: some concepts have changed,” Journal of Endotoxin Research, vol. 10, no. 4, pp. 201–222, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. C. B. Saper and C. D. Breder, “Seminars in medicine of the Beth Israel Hospital, Boston: the neurologic basis of fever,” New England Journal of Medicine, vol. 330, no. 26, pp. 1880–1886, 1994. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Helminen and T. Vesikari, “Increased interleukin-1 (IL-1) production from LPS-stimulated peripheral blood monocytes in children with febrile convulsions,” Acta Paediatrica Scandinavica, vol. 79, no. 8-9, pp. 810–816, 1990. View at Google Scholar · View at Scopus
  36. K. Kanemoto, J. Kawasaki, S. Yuasa et al., “Increased frequency of interleukin-1β-511T allele in patients with temporal lobe epilepsy, hippocampal sclerosis, and prolonged febrile convulsion,” Epilepsia, vol. 44, no. 6, pp. 796–799, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Kira, H. Torisu, M. Takemoto et al., “Genetic susceptibility to simple febrile seizures: interleukin-1β promoter polymorphisms are associated with sporadic cases,” Neuroscience Letters, vol. 384, no. 3, pp. 239–244, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Matsuo, K. Sasaki, T. Ichimaru, S. Nakazato, and Y. Hamasaki, “Increased IL-1β Production From dsRNA-stimulated Leukocytes in Febrile Seizures,” Pediatric Neurology, vol. 35, no. 2, pp. 102–106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Wang, Q. Cheng, S. Malik, and J. Yang, “Interleukin-1β inhibits γ-aminobutyric acid type A (GABA(A)) receptor current in cultured hippocampal neurons,” Journal of Pharmacology and Experimental Therapeutics, vol. 292, no. 2, pp. 497–504, 2000. View at Google Scholar · View at Scopus
  40. B. Viviani, S. Bartesaghi, F. Gardoni et al., “Interleukin-1β enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases,” Journal of Neuroscience, vol. 23, no. 25, pp. 8692–8700, 2003. View at Google Scholar · View at Scopus
  41. J. Fotheringham, D. Donati, N. Akhyani et al., “Association of human herpesvirus-6B with mesial temporal lobe epilepsy,” PLoS Medicine, vol. 4, no. 5, pp. 0848–0857, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Karatas, G. Gurer, A. Pinar et al., “Investigation of HSV-1, HSV-2, CMV, HHV-6 and HHV-8 DNA by real-time PCR in surgical resection materials of epilepsy patients with mesial temporal lobe sclerosis,” Journal of the Neurological Sciences, vol. 264, no. 1-2, pp. 151–156, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. W. H. Theodore, L. Epstein, W. D. Gaillard, S. Shinnar, M. S. Wainwright, and S. Jacobson, “Human herpes virus 6B: a possible role in epilepsy?” Epilepsia, vol. 49, no. 11, pp. 1828–1837, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. D. M. Zerr, A. S. Meier, S. S. Selke et al., “A population-based study of primary human herpesvirus 6 infection,” New England Journal of Medicine, vol. 352, no. 8, pp. 768–776, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. M. V. Solbrig, R. Adrian, D. Y. Chang, and G. C. Perng, “Viral risk factor for seizures: pathobiology of dynorphin in herpes simplex viral (HSV-1) seizures in an animal model,” Neurobiology of Disease, vol. 23, no. 3, pp. 612–620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. H. M. Wu, C. C. Huang, S. H. Chen et al., “Herpes simplex virus type 1 inoculation enhances hippocampal excitability and seizure susceptibility in mice,” European Journal of Neuroscience, vol. 18, no. 12, pp. 3294–3304, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Battaglia and S. Bassanini, “MAM and other “lesion“ models of developmental epilepsy,” in Models of Seizure and Epilepsy, A. Pitkanen, P. A. Schwartzkroin, and S. Moshé, Eds., pp. 265–270, Elsevier Academic Press, San Diego, Calif, USA, 2006. View at Google Scholar
  48. M. R. De Feo, O. Mecarelli, and G. F. Ricci, “Seizure susceptibility in immature rats with micrencephaly induced by prenatal exposure to methylazoxymethanol acetate,” Pharmacological Research, vol. 31, no. 2, pp. 109–114, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. S. C. Baraban, H. J. Wenzel, D. W. Hochman, and P. A. Schwartzkroin, “Characterization of heterotopic cell clusters in the hippocampus of rats exposed to methylazoxymethanol in utero,” Epilepsy Research, vol. 39, no. 2, pp. 87–102, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Colacitti, G. Sancini, S. DeBiasi et al., “Prenatal methylazoxymethanol treatment in rats produces brain abnormalities with morphological similarities to human developmental brain dysgeneses,” Journal of Neuropathology and Experimental Neurology, vol. 58, no. 1, pp. 92–106, 1999. View at Google Scholar · View at Scopus
  51. I. M. Germano and E. F. Sperber, “Increased seizure susceptibility in adult rats with neuronal migration disorders,” Brain Research, vol. 777, no. 1-2, pp. 219–222, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. I. M. Germano, E. F. Sperber, S. Ahuja, and S. L. Moshe, “Evidence of enhanced kindling and hippocampal neuronal injury in immature rats with neuronal migration disorders,” Epilepsia, vol. 39, no. 12, pp. 1253–1260, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Sancini, S. Franceschetti, G. Battaglia et al., “Dysplastic neocortex and subcortical heterotopias in methylazoxymethanol-treated rats: an intracellular study of identified pyramidal neurones,” Neuroscience Letters, vol. 246, no. 3, pp. 181–185, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. E. P. Harrington, G. Möddel, I. M. Najm, and S. C. Baraban, “Altered glutamate receptor—transporter expression and spontaneous seizures in rats exposed to methylazoxymethanol in utero,” Epilepsia, vol. 48, no. 1, pp. 158–168, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. P. A. Castro, E. C. Cooper, D. H. Lowenstein, and S. C. Baraban, “Hippocampal heterotopia lack functional Kv4.2 potassium channels in the methylazoxymethanol model of cortical malformations and epilepsy,” Journal of Neuroscience, vol. 21, no. 17, pp. 6626–6634, 2001. View at Google Scholar · View at Scopus
  56. F. Gardoni, S. Pagliardini, V. Setola et al., “The NMDA receptor complex is altered in an animal model of human cerebral heterotopia,” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 6, pp. 662–675, 2003. View at Google Scholar · View at Scopus
  57. A. Karlsson, C. Lindquist, K. Malmgren, and F. Asztely, “Altered spontaneous synaptic inhibition in an animal model of cerebral heterotopias,” Brain Research, vol. 1383, pp. 54–61, 2011. View at Publisher · View at Google Scholar
  58. F. Cattabeni and M. Di Luca, “Developmental models of brain dysfunctions induced by targeted cellular ablations with methylazoxymethanol,” Physiological Reviews, vol. 77, no. 1, pp. 199–215, 1997. View at Google Scholar · View at Scopus
  59. C. Bocti, Y. Robitaille, P. Diadori et al., “The pathological basis of temporal lobe epilepsy in childhood,” Neurology, vol. 60, no. 2, pp. 191–195, 2003. View at Google Scholar · View at Scopus
  60. K. I. Park, K. Chu, K. H. Jung et al., “Role of cortical dysplasia in epileptogenesis following prolonged febrile seizure,” Epilepsia, vol. 51, no. 9, pp. 1809–1819, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Kondo, I. Najm, T. Kunieda, S. Perryman, K. Yacubova, and H. O. Lüders, “Electroencephalographic characterization of an adult rat model of radiation-induced cortical dysplasia,” Epilepsia, vol. 42, no. 10, pp. 1221–1227, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. S. N. Roper, L. A. Abraham, and W. J. Streit, “Exposure to in utero irradiation produces disruption of radial glia in rats,” Developmental Neuroscience, vol. 19, no. 6, pp. 521–528, 1997. View at Google Scholar · View at Scopus
  63. M. Marín-Padilla, R. J. Tsai, M. A. King, and S. N. Roper, “Altered corticogenesis and neuronal morphology in irradiation-induced cortical dysplasia: a Golgi-Cox study,” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 11, pp. 1129–1143, 2003. View at Google Scholar
  64. D. D. Lin and S. N. Roper, “In utero irradiation as a model of cortical dysplasia,” in Models of Seizure and Epilepsy, A. Pitkanen, P. A. Schwartzkroin, and S. Moshé, Eds., pp. 271–290, Elsevier Academic Press, San Diego, Calif, USA, 2006. View at Google Scholar
  65. J. Altman, W. J. Anderson, and K. A. Wright, “Differential radiosensitivity of stationary and migratory primitive cells in the brains of infant rats,” Experimental Neurology, vol. 22, no. 1, pp. 52–74, 1968. View at Google Scholar · View at Scopus
  66. C. Kellinghaus, T. Kunieda, Z. Ying, A. Pan, H. O. Lüders, and I. M. Najm, “Severity of histopathologic abnormalities and in vivo epileptogenicity in the in utero radiation model of rats is dose dependent,” Epilepsia, vol. 45, no. 6, pp. 583–591, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. F.-W. Zhou and S. N. Roper, “Altered firing rates and patterns in interneurons in experimental cortical Dysplasia,” Cerebral Cortex, vol. 21, no. 7, pp. 1645–1658, 2011. View at Publisher · View at Google Scholar
  68. K. Dvorak and J. Feit, “Migration of neuroblasts through partial necrosis of the cerebral cortex in newborn rats: contribution to the problems of morphological development and developmental period of cerebral microgyria. Histological and autoradiographical study,” Acta Neuropathologica, vol. 38, no. 3, pp. 203–212, 1977. View at Google Scholar · View at Scopus
  69. H. J. Luhmann, “The cortical freeze lesion model,” in Models of Seizure and Epilepsy, A. Pitkanen, P. A. Schwartzkroin, and S. Moshé, Eds., pp. 243–265, Elsevier Academic Press, San Diego, Calif, USA, 2006. View at Google Scholar
  70. A. Bordey, S. A. Lyons, J. J. Hablitz, and H. Sontheimer, “Electrophysiological characteristics of reactive astrocytes in experimental cortical dysplasia,” Journal of Neurophysiology, vol. 85, no. 4, pp. 1719–1731, 2001. View at Google Scholar · View at Scopus
  71. S. Bandyopadhyay and J. J. Hablitz, “NR2B antagonists restrict spatiotemporal spread of activity in a rat model of cortical dysplasia,” Epilepsy Research, vol. 72, no. 2-3, pp. 127–139, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Kellinghaus, G. Möddel, H. Shigeto et al., “Dissociation between in vitro and in vivo epileptogenicity in a rat model of cortical dysplasia,” Epileptic Disorders, vol. 9, no. 1, pp. 11–19, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. K. M. Jacobs, “Experimental microgyri disrupt the barrel field pattern in rat somatosensory cortex,” Cerebral Cortex, vol. 9, no. 7, pp. 733–744, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Brill and J. R. Huguenard, “Enhanced infragranular and supragranular synaptic input onto layer 5 pyramidal neurons in a rat model of cortical dysplasia,” Cerebral Cortex, vol. 20, no. 12, pp. 2926–2938, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. H. J. Luhmann, N. Karpuk, M. Qü, and K. Zilles, “Characterization of neuronal migration disorders in neocortical structures. II. Intracellular in vitro recordings,” Journal of Neurophysiology, vol. 80, no. 1, pp. 92–102, 1998. View at Google Scholar · View at Scopus
  76. K. Zilles, “Characterization of neuronal migration disorders in neocortical structures: quantitative receptor autoradiography of ionotropic glutamate, GABAA and GABAB receptors,” European Journal of Neuroscience, vol. 10, no. 10, pp. 3095–3106, 1998. View at Google Scholar · View at Scopus
  77. G. Hagemann, M. M. Kluska, C. Redecker, H. J. Luhmann, and O. W. Witte, “Distribution of glutamate receptor subunits in experimentally induced cortical malformations,” Neuroscience, vol. 117, no. 4, pp. 991–1002, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. R. A. Defazio and J. J. Hablitz, “Alterations in NMDA receptors in a rat model of cortical dysplasia,” Journal of Neurophysiology, vol. 83, no. 1, pp. 315–321, 2000. View at Google Scholar · View at Scopus
  79. H. J. Luhmann, “Characterization of neuronal migration disorders in neocortical structures: extracellular in vitro recordings,” European Journal of Neuroscience, vol. 10, no. 10, pp. 3085–3094, 1998. View at Publisher · View at Google Scholar · View at Scopus
  80. V. N. Kharazia, K. M. Jacobs, and D. A. Prince, “Light microscopic study of GluR1 and calbindin expression in interneurons of neocortical microgyral malformations,” Neuroscience, vol. 120, no. 1, pp. 207–218, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. P. Schwarz, C. C. Stichel, and H. J. Luhmann, “Characterization of neuronal migration disorders in neocortical structures: loss or preservation of inhibitory interneurons?” Epilepsia, vol. 41, no. 7, pp. 781–787, 2000. View at Google Scholar · View at Scopus
  82. C. Redecker, H. J. Luhmann, G. Hagemann, J. M. Fritschy, and O. W. Witte, “Differential downregulation of GABA(A) receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations,” Journal of Neuroscience, vol. 20, no. 13, pp. 5045–5053, 2000. View at Google Scholar · View at Scopus
  83. S. L. Patrick, B. W. Connors, and C. E. Landisman, “Developmental changes in somatostatin-positive interneurons in a freeze-lesion model of epilepsy,” Epilepsy Research, vol. 70, no. 2-3, pp. 161–171, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. F. Colciaghi, A. Finardi, A. Frasca et al., “Status epilepticus-induced pathologic plasticity in a rat model of focal cortical dysplasia,” Brain, vol. 134, no. 10, pp. 2828–2843, 2011. View at Publisher · View at Google Scholar
  85. K. I. Takase, H. Shigeto, S. O. Suzuki, H. Kikuchi, Y. Ohyagi, and J. I. Kira, “Prenatal freeze lesioning produces epileptogenic focal cortical dysplasia,” Epilepsia, vol. 49, no. 6, pp. 997–1010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. R. Schmid, P. Tandon, C. E. Stafstrom, and G. L. Holmes, “Effects of neonatal seizures on subsequent seizure-induced brain injury,” Neurology, vol. 53, no. 8, pp. 1754–1761, 1999. View at Google Scholar · View at Scopus
  87. M. Ouardouz, P. Lema, P. N. Awad, G. Di Cristo, and L. Carmant, “N-methyl-d-aspartate, hyperpolarization-activated cation current (I h) and -aminobutyric acid conductances govern the risk of epileptogenesis following febrile seizures in rat hippocampus,” European Journal of Neuroscience, vol. 31, no. 7, pp. 1252–1260, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Ouardouz and L. Carmant, “Changes in inhibitory CA1 network in dual pathology model,” Channels, vol. 6, no. 1, 2012. View at Google Scholar
  89. K. Chen, I. Aradi, N. Thon, M. Eghbal-Ahmadi, T. Z. Baram, and I. Soltesz, “Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability,” Nature Medicine, vol. 7, no. 3, pp. 331–337, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. D. C. Hesdorffer, E. K.T. Benn, E. Bagiella et al., “Distribution of febrile seizure duration and associations with development,” Annals of Neurology, vol. 70, no. 1, pp. 93–100, 2011. View at Publisher · View at Google Scholar
  91. D. C. Hesdorffer, S. Chan, H. Tian et al., “Are MRI-detected brain abnormalities associated with febrile seizure type?” Epilepsia, vol. 49, no. 5, pp. 765–771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. D. E. Crompton, I. E. Scheffer, I. Taylor et al., “Familial mesial temporal lobe epilepsy: a benign epilepsy syndrome showing complex inheritance,” Brain, vol. 133, no. 11, pp. 3221–3231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. R. P. Gamss, S. E. Slasky, J. A. Bello, T. S. Miller, and S. Shinnar, “Prevalence of hippocampal malrotation in a population without seizures,” American Journal of Neuroradiology, vol. 30, no. 8, pp. 1571–1573, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. I. Ali, M. R. Salzberg, C. French, and N. C. Jones, “Electrophysiological insights into the enduring effects of early life stress on the brain,” Psychopharmacology, vol. 214, no. 1, pp. 155–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. H. E. Edwards, D. Dortok, J. Tam, D. Won, and W. M. Burnham, “Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats,” Hormones and Behavior, vol. 42, no. 4, pp. 437–447, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Joëls, “Stress, the hippocampus, and epilepsy,” Epilepsia, vol. 50, no. 4, pp. 586–597, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. M. Salzberg, G. Kumar, L. Supit et al., “Early postnatal stress confers enduring vulnerability to limbic epileptogenesisy,” Epilepsia, vol. 48, no. 11, pp. 2079–2085, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. N. T. Sawyer and A. Escayg, “Stress and epilepsy: multiple models, multiple outcomes,” Journal of Clinical Neurophysiology, vol. 27, no. 6, pp. 445–452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Z. Baram and L. Schultz, “Corticotropin-releasing hormone is a rapid and potent convulsant in the infant rat,” Developmental Brain Research, vol. 61, no. 1, pp. 97–101, 1991. View at Publisher · View at Google Scholar · View at Scopus
  100. J. B. Rosen, S. K. Pishevar, S. R. B. Weiss et al., “Glucocorticoid treatment increases the ability of CRH to induce seizures,” Neuroscience Letters, vol. 174, no. 1, pp. 113–116, 1994. View at Publisher · View at Google Scholar · View at Scopus
  101. K. L. Brunson, S. Avishai-Eliner, C. G. Hatalski, and T. Z. Baram, “Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone,” Molecular Psychiatry, vol. 6, no. 6, pp. 647–656, 2001. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Joels, “Steroid hormones and excitability in the mammalian brain,” Frontiers in Neuroendocrinology, vol. 18, no. 1, pp. 2–48, 1997. View at Google Scholar
  103. M. Joels, H. Krugers, and H. Karst, “Stress-induced changes in hippocampal function,” Progress in Brain Research, vol. 167, pp. 3–15, 2008. View at Google Scholar
  104. A. S. Koe, N. C. Jones, and M. R. Salzberg, “Early life stress as an influence on limbic epilepsy: an hypothesis whose time has come?” Frontiers in Behavioral Neuroscience, vol. 3, p. 24, 2009. View at Google Scholar
  105. M. C. Lai, G. L. Holmes, K. H. Lee et al., “Effect of neonatal isolation on outcome following neonatal seizures in rats—the role of corticosterone,” Epilepsy Research, vol. 68, no. 2, pp. 123–136, 2006. View at Publisher · View at Google Scholar · View at Scopus
  106. M. C. Lai, S. N. Yang, and L. T. Huang, “Neonatal isolation enhances anxiety-like behavior following early-life Seizure in rats,” Pediatrics and Neonatology, vol. 49, no. 2, pp. 19–25, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. T. R. Taher, M. Salzberg, M. J. Morris, S. Rees, and T. J. O'Brien, “Chronic low-dose corticosterone supplementation enhances acquired epileptogenesis in the rat amygdala kindling model of TLE,” Neuropsychopharmacology, vol. 30, no. 9, pp. 1610–1616, 2005. View at Publisher · View at Google Scholar · View at Scopus