Cortical malformations and epilepsy
Corresponding Author
Philip A. Schwartzkroin
Department of Neurological Surgery, University of Washington, Health Sciences Center, Seattle, Washington
Department of Neurological Surgery, Health Sciences Center, Room RR-720, University of Washington, Box 356470, 1959 NE. Pacific St., Seattle, WA 98195-6470Search for more papers by this authorChristopher A. Walsh
Department of Neurology, Harvard University, Beth Israel Deaconess Medical Center, Boston, Massachusetts
Search for more papers by this authorCorresponding Author
Philip A. Schwartzkroin
Department of Neurological Surgery, University of Washington, Health Sciences Center, Seattle, Washington
Department of Neurological Surgery, Health Sciences Center, Room RR-720, University of Washington, Box 356470, 1959 NE. Pacific St., Seattle, WA 98195-6470Search for more papers by this authorChristopher A. Walsh
Department of Neurology, Harvard University, Beth Israel Deaconess Medical Center, Boston, Massachusetts
Search for more papers by this authorAbstract
Brain malformations, resulting from aberrant patterns of brain development, are highly correlated with childhood seizure syndromes, as well as with cognitive disabilities and other neurological disorders. The structural malformations, often referred to as cortical dysplasia, are extremely varied, reflecting diverse underlying processes and critical timing of the developmental aberration. Recent studies have revealed a genetic basis for many forms of dysplasia. Gene mutations responsible for such common forms of dysplasia as lissencephaly and tuberous sclerosis have been identified, and investigators are beginning to understand how these gene mutations interrupt and/or misdirect the normal developmental pattern. Laboratory investigations, using animal models of cortical dysplasia, are beginning to elucidate how these structural malformations give rise to epilepsy and other functional pathologies. MRDD Research Reviews 2000;6:268–280. © 2000 Wiley-Liss, Inc.
REFERENCES
- Amano S, Ihara N, Uemura S, Yokoyama M, Ikeda M, Serikawa T, Sasahara M, Kataoka H, Hayase Y, Hazama F. 1996. Development of a novel rat mutant with spontaneous limbic-like seizures. Am J Pathol 149: 329–336.
- Balduini W, Cimino M, Lombardelli G, Abbracchio MP, Peruzzi G, Cecchini T, Gazzanelli GC, Catebeni F. 1986. Microencephalic rats as a model of cognitive disorders. Clin Neuropharmacol 9(suppl 3): S8–S18.
- Baraban SC, Schwartzkroin PA. 1995. Electrophysiology of CA1 pyramidal neurons in an animal model of neuronal migration disorders: prenatal methylazoxymethanol treatment. Epilepsy Res 22: 145–156.
- Baraban SC, Schwartzkroin PA. 1996. Flurothyl seizure susceptibility in rats following prenatal methylazoxymethanol treatment. Epilepsy Res 23: 189–194.
- Baraban SC, Schwartzkroin PA. 1997. Effects of prenatal cocaine exposure on the developing hippocampus: intrinsic and synaptic physiology. J Neurophysiol 77: 126–136.
- Barkovich AJ, Kjos BO. 1992b. Gray matter heterotopias: MR characteristics and correlation with developmental and neurologic manifestations. Radiology 182: 493–499.
- Barkovich AJ, Kjos BO. 1992c. Schizencephaly: correlation of clinical findings with MR characteristics. AJNR Am J Neuroradiol 13: 85–94.
- Barkovich AJ, Peck WW. 1997. MR of Zellweger syndrome. AJNR Am J Neuroradiol. 18: 1163–1170.
- Barkovich AJ, Jackson DE Jr, Boyer RS. 1989. Band heterotopias: a newly recognized neuronal migration anomaly. Radiology 171: 455–458.
- Barkovich AJ, Gressens P, Evrard P. 1992a. Formation, maturation and disorders of brain neocortex. Am J Neuroradiol 13: 423–446.
- Barkovich AJ, Guerrini R, Battaglia G, Kalifa G, N'Guyen T, Parmeggiani A, Santucci M, Giovanardi-Rossi P, Granata T, D'Incerti L. 1994. Band heterotopia: correlation of outcome with magnetic resonance imaging parameters. Ann Neurol 36: 609–617.
- Barkovich AJ, Kuzniecky RI, Dobyns WB, Jackson GD, Becker LE, Evrard P. 1996. A classification scheme for malformations of cortical development. Neuropediatrics 27: 59–63.
- Barkovich AJ, Ferriero DM, Barr RM, Gressens P, Dobyns WB, Truwit CL, Evrard P. 1998. Microlissencephaly: a heterogeneous malformation of cortical development. Neuropediatrics 29: 113–119.
- Berry-Kravis E, Israel J. 1994. X-linked pachygyria and agenesis of the corpus callosum: evidence for an X chromosome lissencephaly locus. Ann Neurol 36: 229–333.
- Brunelli S, Faiella A, Capra V, Nigro V, Simeone A, Cama A, Boncinelli E. 1996. Germline mutations in the homeobox gene EMX2 in patients with severe schizencephaly. Nat Genet 12: 94–96.
- Caviness VS Jr. 1976. Patterns of cell and fiber distribution in the neocortex of reeler mutant mice. J Comp Neurol 170: 435–448.
- Caviness VS Jr, Sidman RL. 1973. Time of origin of corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol 148: 141–151.
- Cepeda C, Li Z, Cromwell HC, Altemus KL, Crawford CA, Nansen EA, Ariano MA, Sibley DR, Peacock WJ, Mathern GW, Levine MS. 1999. Electrophsyiological and morphological analyses of cortical neurons obtained from children with catastrophic epilepsy: dopamine receptor modulation of glutamatergic responses. Dev Neurosci 21: 223–235.
- Chae T, Kwon YT, Bronson R, Dikkes P, Li E, Tsai LH. 1997. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18: 29–42.
- Chevassus-au-Louis N, Ben-Ari Y, Vergnes M. 1998a. Decreased seizure threshold and more rapid rate of kindling in rats with cortical malformation induced by prenatal treatment with methylazoxymethanol. Brain Res 812: 252–255.
-
Chevassus-au-Louis N,
Rafiki A,
Jorquera I,
Ben-Ari Y,
Represa A.
1998b.
Neocortex in the hippocampus: an anatomical and functional study of CA1 heterotopias after prenatal treatment with methylazoxymethanol in rats.
J Comp Neurol
394:
520–536.
10.1002/(SICI)1096-9861(19980518)394:4<520::AID-CNE9>3.0.CO;2-3 CAS PubMed Web of Science® Google Scholar
- Chevassus-au-Louis N, Baraban SC, Gaiarsa J-L, Ben-Ari Y. 1999. Cortical malformations and epilepsy: new insights from animal models. Epilepsia 40: 811–821.
- Colacitti C, Sancini G, Franceschetti S, Cattabeni F, Avaznini G, Spreafico R, DiLuca M, Battaglia G. 1998. Altered connections between neocortical and heterotopic areas in methylazoxymethanol-treated rat. Epilepsy Res 32: 49–62.
- Colacitti C, Sancini G, DeBiasi S, Franceschetti S, Caputi A, Frassoni C, Cattabeni F, Avanzini G, Spreafico R, DiLuca M, Battaglia G. 1999. Prenatal methylazoxymethanol treatment in rats produces brain abnormalities with morphological similarities to human developmental brain dysgeneses. J Neuropathol Exp Neurol 58: 92–106.
- Cooperstone BG, Friedman A, Kaplan BS. 1993. Galloway-Mowat syndrome of abnormal gyral patterns and glomerulopathy. Am J Med Genet 47: 250–254.
- Copp JA, Harding BN. 1999. Neuronal migration disorders in humans and in mouse models: an overview. Epilepsy Res 36: 133–141.
- Defazio RA, Hablitz JJ. 1999. Reduction of zolpidem sensitivity in a freeze lesion model of neocortical dysgenesis. J Neurophysiol 81: 404–407.
- DeFeo MF, Cecarelli O, Ricci GF. 1995. Seizure susceptibility in immature rats with microencephaly induced by prenatal exposure to methylazoxymethanol acetate. Pharmacol Res 31: 109–114.
- des Portes V, Pinard J, Billuart P, Vinet M, Koulakoff A, Carrie A, Gelot A, Dupuis E, Motte J, Berwald-Netter Y, Catala M, Kahn A, Beldjord C, Chelly J. 1998. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92: 51–61.
- DiMario FJ Jr, Cobb RJ, Ramsby GR, Leicher C. 1993. Familial band heterotopias simulating tuberous sclerosis. Neurology 43: 1424–1426.
- Dobyns WB. 1987. Developmental aspects of lissencephaly and the lissencephaly syndromes. Birth Defects Orig Artic Ser 23: 225–241.
- Dobyns WB, Truwit CL. 1995. Lissencephaly and other malformations of cortical development: 1995 update. Neuropediatrics 26: 132–147.
- Dobyns WB, Reiner O, Carrozzo R, Ledbetter DH. 1993. Lissencephaly: a human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. JAMA 270: 2838–2842.
- Eksioglu YZ, Scheffer IE, Cardenas P, Knoll J, DiMario F, Ramsby G, Berg M, Kamuro K, Berkovic SF, Duyk GM, Parisi J, Huttenlocher PR, Walsh CA. 1996. Periventricular heterotopia: an X-linked dominant epilepsy locus causing aberrant cerebral cortical development. Neuron 16: 77–87.
- European-Chromosome 16 Tuberous Sclerosis Consortium. 1993. Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell 75: 1305–1315.
- Evrard P, Caviness VS, Prats-vinas J, Lyon G. 1978. The mechanism of arrest of neuronal migration in the zellweger malformation: an hypothesis based upon cytoarchitectonic analysis. Acta Neuropathol 41: 109–117.
- Evrard P, DeSaint-George P, Kadhim HJ, Gadisseux JF. 1989. Pathology of prenatal encephalopathies. In: J French, editor. Child neurology and developmental disabilities. Baltimore: Brookes. p 153–176.
- Farah S, Sabry MA, Khuraibet A, Khaffagi S, Rudwan M, Hassan M, Haseeb N, Abulhassan S, Abdel-Rasool MA, Elgamal S, Qasrawi B, Al-Busairi W, Farag TI. 1997. Lissencephaly associated with cerebellar hypoplasia and myoclonic epilepsy in a Bedouin kindred: a new syndrome? Clin Genet 51: 326–330.
- Ferrer I, Soriano E, Marti E, Laforet E, Reyners H, Gianfelici de Reyners E. 1991. Naturally occurring postnatal cell death in the cerebral cortex of the microencephalic rat induced by prenatal X-irradiation. Neurosci Res 12: 446–451.
- Ferrie CD, Jackson GD, Giannakodimos S, Panayiotopoulos CP. 1995. Posterior agyria-pachygyria with polymicrogyria: evidence for an inherited neuronal migration disorder. Neurology 45: 150–153.
- Fleck MW, Hirotsune S, Gambello MJ, Phillips-Tansey E, Suares G, Mervis RF, Wynshaw-Boris A, McBain CJ. 2000. Hippocampal abnormalities and enhanced excitability in a murine model of human lissencephaly. J Neurosci 20: 439–450.
- Fox JW, Lamperti ED, Eksioglu YZ, Hong SE, Feng Y, Graham DA, Scheffer IE, Dobyns WB, Hirsch BA, Radtke RA, Berkovic SF, Huttenlocher PR, Walsh CA. 1998. Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21: 1315–1325.
- Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J. 1999. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23: 247–256.
- Frotscher M. 1998. Cajal-Retzius cells, Reelin, and the formation of layers. Curr Opin Neurobiol 8: 570–575.
- Galaburda AM, Sherman GF, Rosen GD, Aboitiz F, Geschwind N. 1985. Developmental dyslexia: four consecutive cases with cortical anomalies. Ann Neurol 18: 222–233.
- Germano IM, Sperber EF. 1997. Increased seizure susceptibility in adult rats with neuronal migration disorders. Brain Res 777: 219–222.
- Germano IM, Zhang YF, Sperber EF, Moshe SL. 1996. Neuronal migration disorders increase susceptibility to hyperthermia-induced seizures in developing rats. Epilepsia 37: 902–910.
- Germano IM, Sperber EF, Ahuja S, Moshe SL. 1998. Evidence of enhanced kindling and hippocampal neuronal injury in immature rats with neuronal migration disorders. Epilepsia 39: 1253–1260.
- Gleeson J, Allen K, Fox J, Lamperti E, Berkovic S, Cooper E, Scheffer I, Dobyns W, Minnerath S, Ross M, Walsh C. 1998. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92: 63–72.
- Gleeson JG, Lin PT, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23: 257–271.
- Gonzalez J, Russo C, Goldowitz D, Sweet H, Davisson M, Walsh C. 1997. Birthdate and cell marker analysis of scrambler: a novel mutation affecting cortical development with a reeler-like phenotype. J Neurosci 17: 9204–9211.
- Graff-Radford NR, Bosch EP, Stears JC, Tranel D. 1986. Developmental Foix-Chavany-Marie syndrome in identical twins. Ann Neurol 20: 632–635.
- Green AJ, Smith M, Yates JR. 1994. Loss of heterozygosity on chromosome 16p13.3 in hamartomas from tuberous sclerosis patients. Nat Genet 6: 193–196.
- Gropman AL, Barkovich AJ, Vezina LG, Conry JA, Dubovsky EC, Packer RJ. 1997. Pediatric congenital bilateral perisylvian syndrome: clinical and MRI features in 12 patients. Neuropediatrics 28: 198–203.
- Guerrini R, Dubeau F, Dulac O, Barkovich AJ, Kuzniecky R, Fett C, Jones-Gotman M, Canapicchi R, Cross H, Fish D, Bonanni P, Jambaque I, Andermann F. 1997. Bilateral parasagittal parietooccipital polymicrogyria and epilepsy. Ann Neurol 41: 65–73.
- Hablitz JJ, DeFazio T. 1998. Excitability changes in freeze-induced cortical microgyria. Epilepsy Res 32: 78–82.
- Hattori M, Adachi H, Tsujimoto M, Arai H, Inoue K. 1994. Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected] [published erratum appears in Nature 1994; 370:391]. Nature 370: 216–218.
- Henry KW, Yuan X, Koszewski NJ, Onda H, Kwiatkowski DJ, Noonan DJ. 1998. Tuberous sclerosis gene 2 product modulates transcription mediated by steroid hormone receptor family members. J Biol Chem 273: 20535–20539.
- Henske EP, Neumann HP, Scheithauer BW, Herbst EW, Short MP, Kwiatkowski DJ. 1995. Loss of heterozygosity in the tuberous sclerosis (TSC2) region of chromosome band 16p13 occurs in sporadic as well as TSC-associated renal angiomyolipomas. Genes Chromosomes Cancer 13: 295–298.
- Henske EP, Scheithauer BW, Short MP, Wollmann R, Nahmias J, Hornigold N, van Slegtenhorst M, Welsh CT, Kwiatkowski DJ. 1996. Allelic loss is frequent in tuberous sclerosis kidney lesions but rare in brain lesions. Am J Hum Genet 59: 400–406.
- Hicks SP, D'Amato CJ, Lowe MJ. 1959. The development of the mammalian nervous system. J Comp Neurol 113: 435–469.
- Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A. 1998. Graded reduction of Pafah1b1 (LIS1) activity results in neuronal migration defects and early embryonic lethality [see comments]. Nat Genet 19: 333–339.
- Hourihane JO, Bennett CP, Chaudhuri R, Robb SA, Martin ND. 1993. A sibship with a neuronal migration defect, cerebellar hypoplasia and congenital lymphedema. Neuropediatrics 24: 43–46.
- Huttenlocher PR, Taravath S, Mojtahedi S. 1994. Periventricular heterotopia and epilepsy. Neurology 44: 51–55.
- Ito N, Rubin G. 1999. Gigas, a Drosophila homolog of tuberous sclerosis gene product-2, regulates the cell cycle. Cell 96: 529–539.
- Jacobs KM, Gutnick MJ, Prince DA. 1996. Hyperexcitability in a model of cortical maldevelopment. Cereb Cortex 6: 514:523.
- Jacobs KM, Hwang BJ, Prince DA. 1999a. Focal epileptogenesis in a rat model of polymicrogyria. J Neurophysiol 81: 159–173.
- Jacobs KM, Kharazia VN, Prince DA. 1999b. Mechanisms underlying epileptogenesis in cortical malformations. Epilepsy Res 36: 165–188.
- Kamuro K, Tenokuchi Y. 1993. Familial periventricular nodular heterotopia. Brain Dev 15: 237–241.
- Kerfoot C, Vinters, HV, Mathern GW. 1999. Cerebral cortical dysplasia: giant neurons show potential for increased excitation and axonal plasticity. Dev Neurosci 21: 260–270.
- Knudson AJ. 1986. Genetics of human cancer. Ann Rev Genet 20: 231–251.
- Kuzniecky R, Andermann F, Guerrini R. 1994. The epileptic spectrum in the congenital bilateral perisylvian syndrome: CBPS Multicenter Collaborative Study. Neurology 44: 379–385.
- Kwiatkowski DJ, Short MP. 1994. Tuberous sclerosis. Arch Dermatol 130: 348–354.
-
Kwon YT,
Tsai LH.
1998.
A novel disruption of cortical development in p35 (-/-) mice distinct from reeler.
J Comp Neurol
395:
510–522.
10.1002/(SICI)1096-9861(19980615)395:4<510::AID-CNE7>3.0.CO;2-4 CAS PubMed Web of Science® Google Scholar
- Lee KS, Schottler F, Collins JL, Lanzino G, Couture D, Rao A, Hiramatsu K, Goto Y, Hong SC, Caner H, Yamamoto H, Chen ZF, Bertram E, Berr S, Omary R, Scrable H, Jackson T, Goble J, Eisenman L. 1997. A genetic animal model of human neocortical heterotopia associated with seizures. J Neurosci 17: 6236–6242.
- Lo Nigro C, Chong CS, Smith AC, Dobyns WB, Carrozzo R, Ledbetter DH. 1997. Point mutations and an intragenic deletion in LIS1, the lissencephaly causative gene in isolated lissencephaly sequence and Miller-Dieker syndrome. Hum Mol Genet 6: 157–164.
- Luhmann HJ, Raabe K. 1996. Characterization of neuronal migration disorders in neocortical structures, I: expression of epileptiform activity in an animal model. Epilepsy Res 26: 67–74.
- Luhmann HJ, Karpuk N, Qu M, Zilles K. 1998a. Characterization of neuronal migration disorders in neocortical structures, II: intracellular in vitro recordings. J Neurophysiol 80: 92–102.
- Luhmann HJ, Raabe K, Qu M, Zilles K. 1998b. Characterization of neuronal migration disorders in neocortical structures: extracellular in vitro recordings. Eur J Neurosci 10: 3085–3094.
- Marin-Padilla M. 1999. Developmental neuropathology and impact of perinatal brain damage, III: gray matter lesions of the neocortex. J Neuropathol Exp Neurol 58: 407–429.
- Marret S., Mukendi R, Gadisseux J-F, Gressens P, Evrard P. 1995. Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions. J Neuropathol Exp Neurol 54: 358–370.
- Matsudaira P. 1994. Actin crosslinking proteins at the leading edge. Semin Cell Biol 5: 165–174.
- McBain CJ, Suares G, Fleck JW, Phillips-Tansey E. 1999. Dendritic atrophy and a reduced electrographic seizure threshold following abnormal neuronal migration in a mouse model of lissencephaly. Epilepsia 40(suppl 7): 8.
- Mohammed AK, Jonsson G, Sundstrom E, Minor BG, Soderberg U, Archer T. 1986. Selective attention and place navigation in rats treated prenatally with methylazoxymethanol. Brain Res 395: 145–155.
- Norman MG, Roberts M, Sirois J, Tremblay LJ. 1976. Lissencephaly. Can J Neurol Sci 3: 39–46.
- Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Micoshiba K. 1995. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14: 899–912.
- Ohshima T, Ward J, Huh C, Longenecker G, Veeranna Pant H, Brady R, Martin L, Kulkarni A. 1996. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad Sci U S A 93: 11173–1118.
- Pavone L, Curatolo P, Rizzo R, Micali G, Incorpora G, Garg BP, Dunn DW, Dobyns WB. 1991. Epidermal nevus syndrome: a neurologic variant with hemimegalencephaly, gyral malformation, mental retardation, seizures, and facial hemihypertrophy. Neurology 41: 266–271.
- Pellegrini M, Mansouri A, Simeone A, Boncinelli E, Gruss P. 1996. Dentate gyrus formation requires Emx2. Development 122: 3893–3898.
- Pilz DT, Matsumoto N, Minnerath S, Mills P, Gleeson JG, Allen KM, Walsh CA, Barkovich AJ, Dobyns WB, Ledbetter DH, Ross ME. 1998. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum Mol Genet 7: 2029–2037.
- Raymond AA, Fish DR, Sisodiya SM. 1995. Abnormalities of gyration, heterotopias, tuberous sclerosis, focal cortical dysplasia, microdysgenesis, dysembryoblastic neuroepithelial tumour and dysgenesis of the archicortex in epilepsy: clinical, EEG and neuroimaging features in 100 adult patients. Brain 188: 629–660.
- Redecker C, Hagemann G, Witte OW, Marret S, Evrard P, Gressens P. 1998a. Long-term evolution of excitotoxic cortical dysgenesis induced in the developing rat brain. Dev Brain Res 109: 109–113.
- Redecker C, Lutzenburg M, Gressens P, Evrard P, Witte OW, Hagemann G. 1998b. Excitability changes and glucose metabolism in experimentally induced focal cortical dysplasias. Cereb Cortex 8: 623–634.
- Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH. 1993. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364: 717–721.
- Robbins CA, Wenzel HJ, Tsai LH, Schwartzkroin PA. 1999. Structural organization and function in dentate gyrus of the p35 mutant model associated with spontaneous seizures. Epilepsia 40(suppl 7): 34.
- Roper SN. 1998. In utero irradiation of rats as a model of human cerebrocortical dysgenesis: a review. Epilepsy Res 32: 63–74.
- Roper SN, Abraham LA, Streit WJ. 1997a. Exposure to in utero irradiation produces disruption of radial glia in rats. Dev Neurosci 19: 521–528.
- Roper SN, King MA, Abraham LA, Boillot MA. 1997b. Disinhibited in vitro neocortical slices containing experimentally induced cortical dysplasia demonstrate hyperexcitability. Epilepsy Res 26: 443–449.
- Roper SN, Eisenschenk S, King MA. 1999. Reduced density of parvalbumin- and calbindin D28-immunoreactive neurons in experimental cortical dysplasia. Epilepsy Res 37: 63–71.
- Rosen GD, Sherman GF, Richman JM, Stone LV, Galaburda AM. 1992. Induction of molecular layer ectopias by puncture wounds in newborn rats and mice. Dev Brain Res 67: 285–291.
- Sapir T, Elbaum M, Reiner O. 1997. Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. Embo J 16: 6977–6984.
- Sarnat HB. 1992. Cerebral dysgenesis: embryology and clinical expression. New York: Oxford University Press.
-
Schottler F,
Couture D,
Rao A,
Kahn H,
Lee KS.
1998.
Subcortical connections of normotopic and heterotopic neurons in sensory and motor cortices of the tish mutant rat.
J Comp Neurol
395:
29–42.
10.1002/(SICI)1096-9861(19980525)395:1<29::AID-CNE3>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- Shimizu J, Tamaru M, Katsukura T, Matsutani T, Nagata Y. 1991. Effects of fetal treatment with methlazoxymethanol acetate on radial maze performance in rats. Epilepsy Res 11: 209–214.
- Shmuili O, Cahana A, Reiner O. 1999. Platelet-activating factor (PAF) acetylhydrolase activity, LIS1 expression, and seizures. J Neurosci Res 57: 176–184.
- Spreafico R, Battaglia G, Arcelli P, Andermann F, Dubeau F, Palmini A, Olivier A, Villemure JG, Tampieri D, Avanzini G, Avoli M. 1998. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 50: 27–36.
- Spreafico R, Avanzini G, Andermann F 1999. Abnormal cortical development and epilepsy. London: John Libbey.
- Straussberg R, Gross S, Amir J, Gadoth N. 1996. A new autosomal recessive syndrome of pachygyria. Clin Genet 50: 498–501.
- Tagawa T, Futagi Y, Arai H, Mushiake S, Nakayama M. 1997. Hypomelanosis of Ito associated with hemimegalencephaly: a clinicopathological study. Pediatr Neurol 17: 180–184.
- van Slegtenhorst M, de Hoogt R, Hermans C, Nellist M, Janssen B, Verhoef S, Lindhout D, van den Ouweland A, Halley D, Young J, Burley M, Jeremiah S, Woodward K, Nahmias J, Fox M, Ekong R, Osborne J, Wolfe J, Povey S, Snell RG, Cheadle JP, Jones AC, Tachataki M, Ravine D, Kwiatkowski DJ, et al. 1997. Identification of the tuberous sclerosis gene TSC1 on chromosome 9q34. Science 277: 805–808.
- Vinters HV, Fisher RS, Cornford ME, Mah V, Secor DL, DeRosa JM, Comair YG, Peacock WJ, Shields WD. 1992. Morphological stustrates of infantile spasms: studies based on surgically resected cerebral tissue. Childs Nerv Syst 8: 8–17.
- Vinters HV, Park SH, Johnson MW, Mischel PS, Catania M, Kerfoot C. 1999. Cortical dysplasia, genetic abnormalities and neurocutaneous syndromes. Dev Neurosci 21: 248–259.
- Walsh CA. 1995. Neuronal identity, neuronal migration, and epileptic disorders of the cerebral cortex. In: PA Schwartzkroin, JL Noebels, SL Moshe, JW Swann, editors. Brain development and epilepsy. New York: Oxford University Press. p 122–143.
- Whiting S, Duchowny M. 1999. Clinical spectrum of cortical dysplasia in childhood: diagnosis and treatment issues. J Child Neurol 14: 759–771.
- Wienecke R, Konig A, DeClue JE. 1995. Identification of tuberin, the tuberous sclerosis-2 product: tuberin possesses specific Rap1GAP activity. J Biol Chem 270: 16409–16414.
- Wolf HK, Normann S, Green AJ, von Bakel I, Blumcke I, Pietsch T, Wiestler OD, von Deimling A. 1997. Tuberous sclerosis-like lesions in epileptogenic human neocortex lack allelic loss at the TSC1 and TSC2 regions. Acta Neuropathol (Berl) 93: 93–96.
- Xiang X, Osmani AH, Osmani SA, Xin M, Morris NR. 1995. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol Biol Cell 6: 297–310.
- Xiao GH, Shoarinejad F, Jin F, Golemis EA, Yeung RS. 1997. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J Biol Chem 272: 6097–6100.
- Yeung RS, Katsetos CD, Klein-Szanto A. 1997. Subependymal astrocytic hamartomas in the Eker rat model of tuberous sclerosis. Am J Pathol 151: 1477–1486.
- Yeung RS, Katsetos CD, Klein-Szanto A. 1999. Subependymal astrocytic hamartomas in the Eker rat model of tuberous sclerosis. Am J Pathol 151: 1477–1486.
- Zhang LL, Collier PA, Ashwell KWS. 1995. Mechanisms in the induction of neuronal heterotopia following prenatal cytotoxic brain damage. Neurotoxicol Teratol 17: 297–311.
- Zilles K, Qu M, Schleicher A, Luhmann HJ. 1998. Characterization of neuronal migration disorders in neocortical structures: quantitative receptor autoradiography of ionotropic glutamate, GABA(A) and GABA(B) receptors. Eur J Neurosci 10: 3095–3106.
- Zollino M, Mastroiacovo P, Zampino G, Mariotti P, Neri G. 1992. New XLMR syndrome with characteristic face, hypogenitalism, congenital hypotonia and pachygyria. Am J Med Genet 43: 452–457.