Epileptogenesis in pediatric cortical dysplasia: The dysmature cerebral developmental hypothesis

Epilepsy and Behavior

Volumn 9, Issue 2, 2006, Pages 219-235

  Cepeda, Carlos ^a,b   André, Véronique M ^a,b   Levine, Michael S ^a,b   Salamon, Noriko ^a,b   Miyata, Hajime ^a,b   Vinters, Harry V ^a,b   Mathern, Gary W ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Tottori University   (Japan)

Author keywords

Balloon cell; Corticoneurogenesis; Cytomegalic neurons; Epilepsy; GABA; Glutamate; Infantile spasms; Interneurons; MRI; NMDA; Preplate; Review; Seizures; Subplate

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGE; BENIGN CHILDHOOD EPILEPSY; BRAIN DEVELOPMENT; BRAIN SIZE; CELL COUNT; CELL CYCLE; CELL DEGENERATION; CELL DENSITY; CELL INTERACTION; CELL MATURATION; CELL STRUCTURE; CELL SUBPOPULATION; CORTICAL DYSPLASIA; DISEASE SEVERITY; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EPILEPTOGENESIS; GLIA CELL; HISTOPATHOLOGY; HUMAN; HYPOTHESIS; IN VITRO STUDY; INCIDENCE; MEMBRANE DEPOLARIZATION; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROSURGERY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PERINATAL PERIOD; PRENATAL PERIOD; REVIEW; SYNAPTIC TRANSMISSION; TIME;

CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EPILEPSY; HUMANS; INFANT; NERVOUS SYSTEM MALFORMATIONS; NEURONS;

EID: 33748181142     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2006.05.012     Document Type: Review

References (98)

1. Taylor D.C., Falconer M.A., Bruton C.J., et al. Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry 34 4 (1971) 369-387
2. Mathern G.W., Giza C.C., Yudovin S., et al. Postoperative seizure control and antiepileptic drug use in pediatric epilepsy surgery patients: the UCLA experience, 1986-1997. Epilepsia 40 12 (1999) 1740-1749
3. Avoli M., Bernasconi A., Mattia D., et al. Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology. Ann Neurol 46 6 (1999) 816-826
4. Cepeda C., Peacock W., Levine M.S., et al. Iontophoretic application of NMDA produces different types of excitatory responses in developing human cortical and caudate neurons. Neurosci Lett 126 2 (1991) 167-171
5. Cepeda C., Walsh J.P., Peacock W., et al. Dye-coupling in human neocortical tissue resected from children with intractable epilepsy. Cereb Cortex 3 2 (1993) 95-107
6. Cepeda C., Li Z., Cromwell H.C., et al. Electrophysiological and morphological analyses of cortical neurons obtained from children with catastrophic epilepsy: dopamine receptor modulation of glutamatergic responses. Dev Neurosci 21 3-5 (1999) 223-235
7. Dudek F.E., Wuarin J.P., Tasker J.G., et al. Neurophysiology of neocortical slices resected from children undergoing surgical treatment for epilepsy. J Neurosci Methods 59 1 (1995) 49-58
8. Tasker J.G., Peacock W.J., and Dudek F.E. Local synaptic circuits and epileptiform activity in slices of neocortex from children with intractable epilepsy. J Neurophysiol 67 3 (1992) 496-507
9. Tasker J.G., Hoffman N.W., Kim Y.I., et al. Electrical properties of neocortical neurons in slices from children with intractable epilepsy. J Neurophysiol 75 2 (1996) 931-939
10. Wuarin J.P., Kim Y.I., Cepeda C., et al. Synaptic transmission in human neocortex removed for treatment of intractable epilepsy in children. Ann Neurol 28 4 (1990) 503-511
11. Wyllie E., Comair Y.G., Kotagal P., et al. Seizure outcome after epilepsy surgery in children and adolescents. Ann Neurol 44 5 (1998) 740-748
12. Cook S.W., Nguyen S.T., Hu B., et al. Cerebral hemispherectomy in pediatric patients with epilepsy: comparison of three techniques by pathological substrate in 115 patients. J Neurosurg 100 Suppl. 2 (2004) 125-141
13. Semah F., Picot M.C., Adam C., et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence?. Neurology 51 5 (1998) 1256-1262
14. Tassi L., Colombo N., Garbelli R., et al. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 125 Pt 8 (2002) 1719-1732
15. Jonas R., Nguyen S., Hu B., et al. Cerebral hemispherectomy: hospital course, seizure, developmental, language, and motor outcomes. Neurology 62 10 (2004) 1712-1721
16. Salamon N., Andres M., Chute D.J., et al. Contralateral hemimicroencephaly and clinical-pathological correlations in children with hemimegalencephaly. Brain 129 Pt 2 (2006) 352-365
17. Cepeda C., Andre V.M., Flores-Hernandez J., et al. Pediatric cortical dysplasia: correlations between neuroimaging, electrophysiology and location of cytomegalic neurons and balloon cells and glutamate/GABA synaptic circuits. Dev Neurosci 27 1 (2005) 59-76
18. Koh S., Mathern G.W., Glasser G., et al. Status epilepticus and frequent seizures: incidence and clinical characteristics in pediatric epilepsy surgery patients. Epilepsia 46 12 (2005) 1950-1954
19. Leiphart J.W., Peacock W.J., and Mathern G.W. Lobar and multilobar resections for medically intractable pediatric epilepsy. Pediatr Neurosurg. 34 6 (2001) 311-318
20. Palmini A., Gambardella A., Andermann F., et al. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol 37 4 (1995) 476-487
21. Palmini A. Disorders of cortical development. Curr Opin Neurol 13 2 (2000) 183-192
22. Lawson J.A., Birchansky S., Pacheco E., et al. Distinct clinicopathologic subtypes of cortical dysplasia of Taylor. Neurology 64 1 (2005) 55-61
23. Palmini A., Najm I., Avanzini G., et al. Terminology and classification of the cortical dysplasias. Neurology 62 6 Suppl. 3 (2004) S2-S8
24. Barkovich A.J., Kuzniecky R.I., Jackson G.D., et al. A developmental and genetic classification for malformations of cortical development. Neurology 65 12 (2005) 1873-1887
25. Mischel P.S., Nguyen L.P., and Vinters H.V. Cerebral cortical dysplasia associated with pediatric epilepsy. Review of neuropathologic features and proposal for a grading system. J Neuropathol Exp Neurol 54 2 (1995) 137-153
26. Avoli M., Louvel J., Pumain R., et al. Cellular and molecular mechanisms of epilepsy in the human brain. Prog Neurobiol 77 3 (2005) 166-200
27. Widdess-Walsh P., Kellinghaus C., Jeha L., et al. Electro-clinical and imaging characteristics of focal cortical dysplasia: correlation with pathological subtypes. Epilepsy Res 67 1-2 (2005) 25-33
28. Vinters H.V., Fisher R.S., Cornford M.E., et al. Morphological substrates of infantile spasms: studies based on surgically resected cerebral tissue. Childs Nerv Syst 8 1 (1992) 8-17
29. Urbach H., Scheffler B., Heinrichsmeier T., et al. Focal cortical dysplasia of Taylor's balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome. Epilepsia 43 1 (2002) 33-40
30. Schwartzkroin P.A., and Walsh C.A. Cortical malformations and epilepsy. Ment Retard Dev Disabil Res Rev 6 4 (2000) 268-280
31. Raymond A.A., Fish D.R., Sisodiya S.M., et al. Abnormalities of gyration, heterotopias, tuberous sclerosis, focal cortical dysplasia, microdysgenesis, dysembryoplastic neuroepithelial tumour and dysgenesis of the archicortex in epilepsy. Clinical, EEG and neuroimaging features in 100 adult patients. Brain 118 Pt 3 (1995) 629-660
32. Cotter D.R., Honavar M., and Everall I. Focal cortical dysplasia: a neuropathological and developmental perspective. Epilepsy Res 36 2-3 (1999) 155-164
33. Rakic P. Defects of neuronal migration and the pathogenesis of cortical malformations. Prog Brain Res 73 (1988) 15-37
34. Rakic S., and Zecevic N. Emerging complexity of layer I in human cerebral cortex. Cereb Cortex 13 10 (2003) 1072-1083
35. Zecevic N., Milosevic A., Rakic S., et al. Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J Comp Neurol 412 2 (1999) 241-254
36. Zecevic N., and Rakic P. Development of layer I neurons in the primate cerebral cortex. J Neurosci 21 15 (2001) 5607-5619
37. Dammerman R.S., Flint A.C., Noctor S., et al. An excitatory GABAergic plexus in developing neocortical layer 1. J Neurophysiol 84 1 (2000) 428-434
38. Kostovic I., and Rakic P. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 9 2 (1980) 219-242
39. Kostovic I., and Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297 3 (1990) 441-470
40. Letinic K., Zoncu R., and Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 417 6889 (2002) 645-649
41. Marin-Padilla M., and Marin-Padilla T.M. Origin, prenatal development and structural organization of layer I of the human cerebral (motor) cortex. A Golgi study. Anat Embryol (Berl) 164 2 (1982) 161-206
42. Marin-Padilla M. Developmental neuropathology and impact of perinatal brain damage. III: Gray matter lesions of the neocortex. J Neuropathol Exp Neurol 58 5 (1999) 407-429
43. Maas L.C., Mukherjee P., Carballido-Gamio J., et al. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22 3 (2004) 1134-1140
44. Mrzljak L., Uylings H.B., Kostovic I., et al. Prenatal development of neurons in the human prefrontal cortex. I. A qualitative Golgi study. J Comp Neurol 271 3 (1988) 355-386
45. Mrzljak L., Uylings H.B., Kostovic I., et al. Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study. J Comp Neurol 316 4 (1992) 485-496
46. Cepeda C., Hurst R.S., Flores-Hernandez J., et al. Morphological and electrophysiological characterization of abnormal cell types in pediatric cortical dysplasia. J Neurosci Res 72 4 (2003) 472-486
47. Friauf E., McConnell S.K., and Shatz C.J. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10 8 (1990) 2601-2613
48. Chun J.J., and Shatz C.J. Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J Comp Neurol 282 4 (1989) 555-569
49. Chi J.G., Dooling E.C., and Gilles F.H. Gyral development of the human brain. Ann Neurol 1 1 (1977) 86-93
50. Kriegstein A.R., and Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27 7 (2004) 392-399
51. Noctor S.C., Martinez-Cerdeno V., Ivic L., et al. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7 2 (2004) 136-144
52. Nadarajah B. Radial glia and somal translocation of radial neurons in the developing cerebral cortex. Glia 43 1 (2003) 33-36
53. Englund C., Folkerth R.D., Born D., et al. Aberrant neuronal-glial differentiation in Taylor-type focal cortical dysplasia (type IIA/B). Acta Neuropathol (Berl) 109 5 (2005) 519-533
54. Thom M., Martinian L., Sisodiya S.M., et al. Mcm2 labelling of balloon cells in focal cortical dysplasia. Neuropathol Appl Neurobiol 31 6 (2005) 580-588
55. Ying Z., Gonzalez-Martinez J., Tilelli C., et al. Expression of neural stem cell surface marker CD133 in balloon cells of human focal cortical dysplasia. Epilepsia 46 11 (2005) 1716-1723
56. Cepeda C., Andre V.M., Vinters H.V., et al. Are cytomegalic neurons and balloon cells generators of epileptic activity in pediatric cortical dysplasia?. Epilepsia 46 Suppl. 5 (2005) 82-88
57. Andres M., Andre V.M., Nguyen S., et al. Human cortical dysplasia and epilepsy: an ontogenetic hypothesis based on volumetric MRI and NeuN neuronal density and size measurements. Cereb Cortex 15 2 (2005) 194-210
58. Caviness Jr. V.S., Goto T., Tarui T., et al. Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb Cortex 13 6 (2003) 592-598
59. Caviness Jr. V.S., Takahashi T., and Nowakowski R.S. Neocortical malformation as consequence of nonadaptive regulation of neuronogenetic sequence. Ment Retard Dev Disabil Res Rev 6 1 (2000) 22-33
60. Benardete E.A., and Kriegstein A.R. Increased excitability and decreased sensitivity to GABA in an animal model of dysplastic cortex. Epilepsia 43 9 (2002) 970-982
61. Crino P.B., Trojanowski J.Q., and Eberwine J. Internexin, MAP1B, and nestin in cortical dysplasia as markers of developmental maturity. Acta Neuropathol (Berl) 93 6 (1997) 619-627
62. Prince D.A. Epileptogenic neurons and circuits. Adv Neurol 79 (1999) 665-684
63. Kerfoot C., Vinters H.V., and Mathern G.W. Cerebral cortical dysplasia: giant neurons show potential for increased excitation and axonal plasticity. Dev Neurosci 21 3-5 (1999) 260-270
64. Najm I., Ying Z., Babb T., et al. Mechanisms of epileptogenicity in cortical dysplasias. Neurology 62 6 Suppl. 3 (2004) S9-S13
65. Deukmedjian A.J., King M.A., Cuda C., et al. The GABAergic system of the developing neocortex has a reduced capacity to recover from in utero injury in experimental cortical dysplasia. J Neuropathol Exp Neurol 63 12 (2004) 1265-1273
66. Defazio R.A., and Hablitz J.J. Reduction of zolpidem sensitivity in a freeze lesion model of neocortical dysgenesis. J Neurophysiol 81 1 (1999) 404-407
67. Spreafico R., Battaglia G., Arcelli P., et al. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 50 1 (1998) 27-36
68. Spreafico R., Tassi L., Colombo N., et al. Inhibitory circuits in human dysplastic tissue. Epilepsia 41 Suppl. 6 (2000) S168-S173
69. Jacobs K.M., and Prince D.A. Excitatory and inhibitory postsynaptic currents in a rat model of epileptogenic microgyria. J Neurophysiol 93 2 (2005) 687-696
70. D'Antuono M., Louvel J., Kohling R., et al. GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 127 Pt 7 (2004) 1626-1640
71. Mathern G.W., Cepeda C., Hurst R.S., et al. Neurons recorded from pediatric epilepsy surgery patients with cortical dysplasia. Epilepsia 41 Suppl. 6 (2000) S162-S167
72. Alonso-Nanclares L., Garbelli R., Sola R.G., et al. Microanatomy of the dysplastic neocortex from epileptic patients. Brain 128 Pt 1 (2005) 158-173
73. Cepeda C., Andre V.M., Wu N., et al. Evidence for cytomegalic interneurons in pediatric cortical dysplasia. Soc Neurosci Abstr (2005) Program No. 217.2
74. Cepeda C, Andre VM, Wu N, et al. Immature neurons and networks may contribute to epileptogenesis in pediatric cortical dysplasia. Epilepsia 2006, in press.
75. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3 9 (2002) 728-739
76. De Felipe J., Marco P., Fairen A., et al. Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb Cortex 7 7 (1997) 619-634
77. Owens D.F., and Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nat Rev Neurosci 3 9 (2002) 715-727
78. Andre V.M., Flores-Hernandez J., Cepeda C., et al. Altered GABAergic functions in pediatric cortical dysplasia. Soc Neurosci Abstr (2005) Program No. 217.3
79. DeFazio R.A., and Hablitz J.J. Chloride accumulation and depletion during GABA(A) receptor activation in neocortex. Neuroreport 12 11 (2001) 2537-2541
80. Hubner C.A., Stein V., Hermans-Borgmeyer I., et al. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30 2 (2001) 515-524
81. Hutcheon B., Fritschy J.M., and Poulter M.O. Organization of GABA receptor alpha-subunit clustering in the developing rat neocortex and hippocampus. Eur J Neurosci 19 9 (2004) 2475-2487
82. Khazipov R., Khalilov I., Tyzio R., et al. Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 19 3 (2004) 590-600
83. Prescott C., Dzhala V., Sdrulla D., et al. NKCC1 transporter facilitates seizures in developing brain. Soc Neurosci Abstr (2004) Program No. 679.15
84. Stein V., Hermans-Borgmeyer I., Jentsch T.J., et al. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468 1 (2004) 57-64
85. Crino P.B., Duhaime A.C., Baltuch G., et al. Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia. Neurology 56 7 (2001) 906-913
86. Battaglia G., Pagliardini S., Ferrario A., et al. AlphaCaMKII and NMDA-receptor subunit expression in epileptogenic cortex from human periventricular nodular heterotopia. Epilepsia 43 Suppl. 5 (2002) 209-216
87. Andre V.M., Flores-Hernandez J., Cepeda C., et al. NMDA receptor alterations in neurons from pediatric cortical dysplasia tissue. Cereb Cortex 14 (2004) 634-646
88. Ben-Ari Y., Cherubini E., and Krnjevic K. Changes in voltage dependence of NMDA currents during development. Neurosci Lett 94 1-2 (1988) 88-92
89. Calcagnotto M.E., and Baraban S.C. Prolonged NMDA-mediated responses, altered ifenprodil sensitivity, and epileptiform-like events in the malformed hippocampus of methylazoxymethanol exposed rats. J Neurophysiol 94 1 (2005) 153-162
90. Ben-Ari Y., and Holmes G.L. The multiple facets of gamma-aminobutyric acid dysfunction in epilepsy. Curr Opin Neurol 18 2 (2005) 141-145
91. Tian G.F., Azmi H., Takano T., et al. An astrocytic basis of epilepsy. Nat Med 11 9 (2005) 973-981
92. Calcagnotto M.E., Paredes M.F., Tihan T., et al. Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia. J Neurosci 25 42 (2005) 9649-9657
93. Najm I.M., Ying Z., Babb T., et al. Epileptogenicity correlated with increased N-methyl-D-aspartate receptor subunit NR2A/B in human focal cortical dysplasia. Epilepsia 41 8 (2000) 971-976
94. Thom M., Martinian L., Sen A., et al. Cortical neuronal densities and lamination in focal cortical dysplasia. Acta Neuropathol (Berl) 110 4 (2005) 383-392
95. Moddel G., Jacobson B., Ying Z., et al. The NMDA receptor NR2B subunit contributes to epileptogenesis in human cortical dysplasia. Brain Res 1046 1-2 (2005) 10-23
96. Jonas R., Asarnow R.F., LoPresti C., et al. Surgery for symptomatic infant-onset epileptic encephalopathy with and without infantile spasms. Neurology 64 4 (2005) 746-750
97. Quilichini P.P., Diabira D., Chiron C., et al. Effects of antiepileptic drugs on refractory seizures in the intact immature corticohippocampal formation in vitro. Epilepsia 44 11 (2003) 1365-1374
98. Dzhala V.I., Talos D.M., Sdrulla D.A., et al. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11 11 (2005) 1205-1213