Spontaneous seizures in a rat model of multiple prenatal freeze lesioning

Epilepsy Research

Volumn 105, Issue 3, 2013, Pages 280-291

  Kamada, Takashi ^a   Sun, Wei ^a   Takase, Kei Ichiro ^a   Shigetou, Hiroshi ^a   Suzuki, Satoshi O ^a   Ohyagi, Yasumasa ^a   Kira, Jun Ichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Focal cortical dysplasia; Freeze lesion rat model; Temporal lobe epilepsy.

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH RECORDING; CONTROLLED STUDY; CORTICAL DYSPLASIA; DENSITOMETRY; ELECTROENCEPHALOGRAPHY; EMBRYO; EPILEPTOGENESIS; EVOKED RESPONSE; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MASTICATION; NERVE CONDUCTION; NONHUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEIZURE; SNIFFING;

FOCAL CORTICAL DYSPLASIA; FREEZE LESION RAT MODEL; TEMPORAL LOBE EPILEPSY.;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EXCITATORY AMINO ACID TRANSPORTER 2; FEMALE; FREEZING; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; MALE; PREGNANCY; PRENATAL INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SEIZURES;

EID: 84880039408     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2013.03.003     Document Type: Article

References (49)

1. Avoli M., Bernasconi A., Mattia D., Olivier A., Hwa G.G.C. Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology. Ann. Neurol. 1999, 46:816-826.
2. Bast T., Oezkan O., Rona S., Stippich C., Seitz A., Rupp A., Fauser S., Zentner J., Rating D., Scherg M. EEG and MEG source analysis of single and average interictal spikes reveals intrinsic epileptogenicity in focal cortical dysplasia. Epilepsia 2004, 45:621-631.
3. Bayer S.A., Altman J. Principles of neurogenesis, neuronal migration, and neural circuit formation. The Rat Nervous System 1995, 1079-1098. Academic Press, San Diego, CA. 2nd ed. P. George (Ed.).
4. Blümcke I., Thom M., Aronica E., Armstrong D.D., Vinters H.V., Palmini A., Jacques T.S., Avanzini G., Barkovich A.J., Battaglia G., Becker A., Cepeda C., Cendes F., Colombo N., Crino P., Cross J.H., Delalande O., Dubeau F., Duncan J., Guerrini R., Kahane P., Mathern G., Najm I., Özkara Ç., Raybaud C., Represa A., Roper S.N., Salamon N., Schulze-Bonhage A., Tassi L., Vezzani A., Spreafico R. The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011, 52:158-174.
5. Cepeda C., Hurst R.S., Flores-Hernández J., Hernández-Echeagaray E., Klapstein G.J., Boylan M.K., Calvert C.R., Jocoy E.L., Nguyen O.K., André V.M., Vinters H.V., Ariano M.A., Levine M.S., Mathern G.W. Morphological and electrophysiological characterization of abnormal cell types in pediatric cortical dysplasia. J. Neurosci. Res. 2003, 72:472-486.
6. Cepeda C., André V.M., Flores-Hernández J., Nguyen O.K., Wu N., Klapstein G.J., Nguyen S., Koh S., Vinters H.V., Levine M.S., Mathern G.W. Pediatric cortical dysplasia: correlations between neuroimaging, electrophysiology and location of cytomegalic neurons and balloon cells and glutamate/GABA synaptic circuits. Dev. Neurosci. 2005, 27:59-76.
7. Colcitti C., Sancini G., Franceschetti S., Cattabeni F., Avanzini G., Spreaficeo R., Luca M.D., Battaglia G. Altered connections between neocortical and heterotopic areas I methylazoxymethanol-treated rat. Epilepsy Res. 1998, 32:49-62.
8. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
9. DeFazio R.A., Hablitz J.J. Alterations in NMDA receptors in a rat model of cortical dysplasia. J. Neurophysiol. 2000, 83:315-321.
10. During M.J., Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993, 341:1607-1610.
11. Fauser S., Schulze-Bonhage A., Honegger J., Carmona H., Huppertz H.J., Pantazis G., Rona S., Bast T., Strobl K., Steinhoff B.J., Korinthenberg R., Rating D., Volk B., Zentner J. Focal cortical dysplasias: surgical outcome in 67 patients in relation to histological subtypes and dual pathology. Brain 2004, 127:2406-2418.
12. Fauser S., Huppertz H.J., Bast T., Strobl K., Pantazis G., Altenmueller D.M., Feil B., Rona S., Kurth C., Rating D., Korinthenberg R., Steinhoff B.J., Volk B., Schulze-Bonhage A. Clinical characteristics in focal cortical dysplasia: a retrospective evaluation in a series of 120 patients. Brain 2006, 129:1907-1916.
13. Ferrer I. A Golgi analysis of unlayered polymicrogyria. Acta Neuropathol. (Berl.) 1984, 65:69-76.
14. Francione S., Nobili L., Cardinale F., Citterio A., Galli C., Tassi L. Intra-lesional stereo-EEG activity in Taylor's focal cortical dysplasia. Epileptic. Disord. 2003, 5(Suppl. 2):S105-S114.
15. Germano I.M., Sperber E.F. Transplacentally induced neuronal migration disorders: an animal model for the study of the epilepsies. J. Neurosci. Res. 1998, 51:473-488.
16. Glass M., Dragunow M. Neurochemical and morphological changes associated with human epilepsy. Brain Res. Rev. 1995, 21:29-41.
17. Götz M., Barde Y.A. Radial glial cells defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 2005, 46:369-372.
18. Harrington E.P., Möddel G., Najm I.M., Baraban S.C. Altered glutamate receptor-transporter expression and spontaneous seizures in rats exposed to methylazoxymethanol in utero. Epilepsia 2008, 48:158-168.
19. Ho S.S., Kuzniecky R.I., Gilliam F., Faught E., Morawetz R. Temporal lobe development malformations and epilepsy: dual pathology and bilateral hippocampal abnormalities. Neurology 1998, 50:748-754.
20. Hofman P.A., Fitt G., Mitchell L.A., Jackson G.D. Hippocampal sclerosis and a second focal lesion - how often is it ipsilateral?. Epilepsia 2011, 52:718-721.
21. Ishii T., Moriyoshi K., Sugihara H., Sakurada K., Kadotani H., Yokoi M., Akazawa C., Shigemoto R., Mizuno N., Masu M., Nakanishi S. Molecular characterization of the family of the N-methyl-d-aspartate receptor subunits. J. Biol. Chem. 1993, 268:2836-2843.
22. Jacobs K.M., Gutnick M.J., Prince D.A. Hyperexcitability in a model of cortical maldevelopment. Cereb. Cortex 1996, 6:514-523.
23. Kakita A., Goldman J.E. Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron 1999, 23:461-472.
24. Kasper B.S., Stefan H., Buchfelder M., Paulus W. Temporal lobe microdysgenesis in epilepsy versus control brains. J. Neuropathol. Exp. Neurol. 1999, 58:22-28.
25. Kellinghaus C., Kunieda T., Ying Z., Pan A., Lüders H.O., Najm I.M. Severity of histopathologic abnormalities and in vivo epileptogenicity in the in utero radiation model of rats is dose dependent. Epilepsia 2004, 45:583-591.
26. Kellinghaus C., Möddel G., Shigeto H., Ying Z., Jacobsson B., Gonzalez-Martinez J., Burrier C., Janigro D., Najm I.M. Dissociation between in vitro and in vivo epileptogenicity in a rat model of cortical dysplasia. Epileptic. Disord. 2007, 9:11-19.
27. Kondo S., Najm I., Kunieda T., Perryman S., Yacubova K., Lüders H.O. Electroecephalographic characterization of an adult rat model of radiation-induced cortical dysplasia. Epilepsia 2001, 42:1221-1227.
28. Li L.M., Cendes F., Watson C., Andermann F., Fish D.R., Dubeau F., Free S., Olivier A., Harkness W., Thomas D.G.T., Duncan J.S., Sander J.W.A.S., Shorvon S.D., Cook M.J., Arnold D.L. Surgical treatment of patients with single and dual pathology: relevance of lesion and of hippocampal atrophy to seizure outcome. Neurology 1997, 48:437-444.
29. Luhmann H.J., Raabe K. Characterization of neuronal migration disorders in neocortical structures: I. Expression of epileptiform activity in an animal model. Epilepsy Res. 1996, 26:67-74.
30. Mathern G.W., Cepeda C., Hurst R.S., Flores-Hernandez J., Mendoza D., Levine M.S. Neurons recorded from pediatric epilepsy surgery patients with cortical dysplasia. Epilepsia 2000, 41(Suppl. 6):S162-S167.
31. Mattia D., Olivier A., Avoli M. Seizure-like discharges recorded in human dysplastic neocortex maintained in vitro. Neurology 1995, 45:1391-1395.
32. Meikle L., Talos D.M., Onda H., Pollizzi K., Rotenberg A., Sahin M., Jensen F.E., Kwiatkowski D.J. A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J. Neurosci. 2007, 27:5546-5558.
33. Mikuni N., Babb T.L., Ying Z., Najm I., Nishiyama K., Wylie C., Yacubova K., Okamoto T., Bingaman W. NMDA-receptors 1 and 2A/B coassembly increased in human epileptic focal cortical dysplasia. Epilepsia 1999, 40:1683-1687.
34. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., Seeburg P.H. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 1992, 256:1217-1221.
35. Morioka T., Nishio S., Ishibashi H., Muraishi M., Hisada K., Shigeto H., Yamamoto T., Fukui M. Intrinsic epileptogenicity of focal cortical dysplasia as revealed by magnetoencephalography and electrocorticography. Epilepsy Res. 1999, 33:177-187.
36. Nadarajah B., Parnavelas J.G. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 2002, 3:423-432.
37. Najm I.M., Ying Z., Babb T., Mohamed A., Hadam J., LaPresto E., Wyllie E., Kotagal P., Bingaman W., Foldvary N., Morris H., Lüders H.O. Epileptogenicity correlated with increased N-methyl-d-aspartate receptor subunit NR2A/B in human focal cortical dysplasia. Epilepsia 2000, 41:971-976.
38. Otsubo H., Iida K., Oishi M., Okuda C., Ochi A., Pang E., Weiss S.K., Rutka J.T., Chuang S.H., Snead O.C. Neurophysiologic findings of neuronal migration disorders: intrinsic epileptogenicity of focal cortical dysplasia on electroencephalography, electrocorticography, and magnetoencephalography. J. Child Neurol. 2005, 20:357-363.
39. Palmini A., Najm I., Avanzini G., Babb T., Guerrini R., Foldvary-Schaefer N., Jackson G., Lüders H.O., Prayson R., Spreafico R., Vinters H.V. Terminology and classification of the cortical dysplasias. Neurology 2004, 62:S2-S8.
40. Parnavelas J.G. The origin and migration of cortical neurones: new vistas. Trends Neurosci. 2000, 23:126-131.
41. Proper E.A., Hoogland G., Kappen S.M., Jansen G.H., Rensen G.A., Schrama L.H., van Veelen C.W., van Rijen P.C., van Nieuwenhuizen O., Gispen W.H., De Graan P.N. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 2002, 125:32-43.
42. Raymond A.A., Fish D.R., Stevens J.M., Cook M.J., Sisodiya S.M., Shorvon S.D. Association of hippocampal sclerosis with cortical dysgenesis in patients with epilepsy. Neurology 1994, 44:1841-1845.
43. Richman D.P., Stewart R.M., Caviness V.S. Cerebral microgyria in a 27-week fetus: an architectonic and topographic analysis. J. Neuropathol. Exp. Neurol. 1974, 33:374-384.
44. Scantlebury M.H., Gibbs S.A., Foadjo B., Lema P., Psarropoulou C., Carmant L. Febrile seizures in the predisposed brain: a new model of temporal lobe epilepsy. Ann. Neurol. 2005, 58:41-49.
45. Spreafico R., Tassi L., Colombo N., Bramerio M., Galli C., Garbelli R., Ferrario A., Lo Russo G., Munari C. Inhibitory circuits in human dysplastic tissue. Epilepsia 2000, 41:S168-S173.
46. Suzuki S.O., Goldman J.E. Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J. Neurosci. 2003, 23:4240-4250.
47. Takase K., Shigeto H., Suzuki S.O., Kikuchi H., Ohyagi Y., Kira J. Prenatal freeze lesioning produces epileptogenic focal cortical dysplasia. Epilepsia 2008, 49:997-1010.
48. Ying Z., Babb T.L., Comair Y.G., Bingaman W., Bushey M., Touhalisky K. Induced expression of NMDAR2 proteins and differential expression of NMDAR1 splice variants in dysplastic neurons of human epileptic neocortex. J. Neuropathol. Exp. Neurol. 1998, 57:47-62.
49. Zeng L.H., Xu L., Gutmann D.H., Wong M. Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Ann. Neurol. 2008, 63:444-453.