Cellular and molecular mechanisms of epilepsy in the human brain

Progress in Neurobiology

Volumn 77, Issue 3, 2005, Pages 166-200

  Avoli, Massimo ^a,b,c   Louvel, Jacques ^d   Pumain, René ^e   Köhling, Rüdiger ^e  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d CENTRE PAUL BROCA   (France)

^e UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Electrophysiology; Epilepsy; Focal dysplasia; GABA; Histology; Pathophysiology; Temporal lobe

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOPYRIDINE;

4 AMINOBUTYRIC ACID BRAIN LEVEL; BRAIN ELECTROPHYSIOLOGY; ELECTRIC SHOCK; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; EXCITATORY JUNCTION POTENTIAL; EXCITATORY POSTSYNAPTIC POTENTIAL; FOCAL EPILEPSY; GAP JUNCTION; HIPPOCAMPUS; HISTOCHEMISTRY; HISTOPATHOLOGY; HUMAN; HYPERPOLARIZATION; INTERNEURON; LIMBIC CORTEX; NEOCORTEX; NEUROTRANSMISSION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SPREADING CORTICAL DEPRESSION; SYNAPTIC MEMBRANE; TEMPORAL LOBE EPILEPSY; WHITE MATTER;

ANIMALS; BRAIN; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; HUMANS; NERVE NET; RECEPTORS, GABA;

EID: 27944503013     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2005.09.006     Document Type: Review

References (273)

1. L. Alonso-Nanclares, R. Garbelli, R.G. Sola, J. Pastor, L. Tassi, R. Sreafico, and J. DeFelipe Microanatomy of the dysplastic neocortex from epileptic patients Brain 128 2005 58 173
2. V.M. Andre, J. Flores-Hernandez, C. Cepeda, A.J. Starling, S. Nguyen, M.K. Lobo, H.V. Vinters, M.S. Levine, and G.W. Mathern NMDA receptor alterations in neurons from pediatric cortical dysplasia tissue Cereb. Cortex 14 2004 634 646
3. F. Angelatou, O. Pagonopoulou, T. Maraziotis, A. Olivier, J.G. Villemeure, M. Avoli, and G. Kostopoulos Upregulation of A1 adenosine receptors in human temporal lobe epilepsy: a quantitative autoradiographic study Neurosci. Lett. 163 1993 11 14
4. J.I. Arellano, A. Munoz, I. Ballesteros-Yanez, R.G. Sola, and J. DeFelipe Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus Brain 127 2004 45 64
5. E. Aronica, J.A. Gorter, G.H. Jansen, S. Leenstra, B. Yankaya, and D. Troost Expression of connexin 43 and connexin 32 gap-junction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex Acta. Neuropathol. (Berl.) 101 2001 449 459
6. E. Aronica, J.A. Gorter, G.H. Jansen, C.W. van Veelen, P.C. van Rijen, M. Ramkema, and D. Troost Expression and cell distribution of group I and group II metabotropic glutamate receptor subtypes in taylor-type focal cortical dysplasia Epilepsia 44 2003 785 795
7. E. Aronica, J.A. Gorter, G.H. Jansen, C.W. van Veelen, P.C. Van Rijen, S. Leenstra, M. Ramkema, G.L. Scheffer, R.J. Scheper, and D. Troost Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumors Neuroscience 118 2003 417 429
8. 2+]o in the human epileptogenic neocortex maintained in vitro. Brain Res. 417 1987 199 203
9. M. Avoli, P. Perreault, A. Olivier, and J.G. Villemure 4-Aminopyridine induces a long-lasting depolarizing GABA-ergic potential in human neocortical and hippocampal neurons maintained in vitro Neurosci. Lett. 94 1988 327 332
10. M. Avoli, and A. Olivier Electrophysiological properties and synaptic responses in the deep layers of the human epileptogenic neocortex maintained in vitro J. Neurophysiol. 61 1989 589 606
11. M. Avoli Excitatory amino acid receptors in the human epileptogenic neocortex Epilepsy Res. 10 1991 33 40
12. M. Avoli, C. Drapeau, J. Louvel, R. Pumain, A. Olivier, and J.G. Villemure Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro Ann. Neurol. 30 1991 589 596
13. M. Avoli Electrophysiology and pharmacology of human neocortex and hippocampus in vitro P.A. Schwartzkroin Epilepsy: Models, Mechanisms and Concepts 1993 Cambridge University Press Cambridge, UK 244 280
14. M. Avoli, C. Psarropoulou, V. Tancredi, and Y. Fueta On the synchronous activity induced by 4-aminopyridine in the CA3 subfield of juvenile rat hippocampus J. Neurophysiol. 70 1993 1018 1029
15. M. Avoli, and P.A. Schwartzkroin Electrophysiology and pharmacology of human neocortex and hippocampus in vitro P.A. Schwartzkroin Epilepsy: Models, Mechanisms and Concepts 1993 Cambridge University Press Cambridge, UK 506 510
16. M. Avoli, D. Mattia, A. Siniscalchi, P. Perreault, and F. Tomaiuolo Pharmacology and electrophysiology of a synchronous GABA-mediated potential in the human neocortex Neuroscience 62 1994 655 666
17. M. Avoli, G.G.C. Hwa, D. Mattia, A. Olivier, and J.G. Villemure Microphysiology of human neocortex in vitro R. Guerrini Dysplasias of Cerebral Cortex and Epilepsy 1995 Lippincott-Raven Publishers Philadelphia 35 42
18. A-mediated inhibition and in vitro epileptogenesis in the human neocortex J. Neurophysiol. 73 1995 468 484
19. M. Avoli, M. Barbarosie, A. Lücke, T. Nagao, V. Lopantsev, and R. Köhling Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro J. Neurosci. 16 1996 3912 3924
20. M. Avoli, J. Louvel, I. Kurcewicz, R. Pumain, and M. Barbarosie Extracellular free potassium and calcium during synchronous activity induced by 4-aminopyridine in the juvenile rat hippocampus J. Physiol. (Lond.). 493 1996 707 717
21. M. Avoli, and A. Williamson Functional and pharmacological properties of human neocortical neurons maintained in vitro Prog. Neurobiol. 48 1996 519 554
22. M. Avoli, G.G.C. Hwa, J. Louvel, I. Kurcewicz, R. Pumain, and J.C. Lacaille Functional and pharmacological properties of GABA-mediated inhibition in the human neocortex Can. J. Physiol. Pharm. 75 1997 526 534
23. M. Avoli, A. Bernasconi, D. Mattia, A. Olivier, and G.G.C. Hwa Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology Ann. Neurol. 46 1999 816 826
24. M. Avoli Epilepsy D.L. Martin R.W. Olsen GABA in the Nervous System: The View at Fifty Years 2000 Lippincott, Williams & Wilkins Philadelphia 293 316
25. M. Avoli, D. Mattia, and A. Olivier A window on the physiopathogenesis of seizures in patients with cortical dysplasia Adv. Exp. Med. Biol. 497 2002 123 132
26. M. Avoli, J. Louvel, D. Mattia, A. Olivier, V. Esposito, R. Pumain, and M. D'Antuono Epileptiform synchronization in the human dysplastic cortex Epileptic Disord. 5 2003 S45 S50
27. B receptor activation leads to plastic changes in limbic network ictogenesis Neuropharmacology 46 2004 43 51
28. T.L. Babb, J.K. Pretorius, W.R. Kupfer, and P.H. Crandall Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus J. Neurosci. 9 1989 2562 2574
29. S.C. Baraban, and M.K. Tallent Interneuron diversity series: interneuronal neuropeptides-endogenous regulators of neuronal excitability TINS 27 2004 135 142
30. M. Barbarosie, J. Louvel, M. D'Antuono, I. Kurcewicz, and M. Avoli Masking synchronous GABA-mediated potentials controls limbic seizures Epilepsia 43 2002 1469 1479
31. J.L. Barker, and N.L. McBurney Henobarbitone modulation of postsynaptic GABA receptor function on cultured mammalian neurons Proc. R. Soc. Lond. B Biol. Sci. 206 1979 319 327
32. A.L. Barth, and R.C. Malenka NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses Nat. Neurosci. 4 2001 235 236
33. F. Bartolomei, F. Wendling, J. Bellanger, J. Regis, and P. Chauvel Neural networks involved in temporal lobe seizures: a nonlinear regression analysis of SEEG signals interdependencies Clin. Neurophysiol. 112 2001 1746 1760
34. H. Beck, I. Blumcke, T. Kral, H. Clusmann, J. Schramm, O.D. Wiestler, U. Heinemann, and C.E. Elger Properties of a delayed rectifier potassium current in dentate granule cells isolated from the hippocampus of patients with chronic temporal lobe epilepsy Epilepsia 37 1996 892 901
35. 2+ currents in acutely isolated human hippocampal granule cells J. Neurophysiol. 77 1997 1526 1537
36. H. Beck, H. Clusmann, T. Kral, J. Schramm, U. Heinemann, and C.E. Elger Potassium currents in acutely isolated human hippocampal dentate granule cells J. Physiol. 498 1997 73 85
37. H. Beck, I.V. Goussakov, A. Lie, C. Helmstaedter, and C.E. Elger Synaptic plasticity in the human dentate gyrus J. Neurosci. 20 2000 7080 7086
38. A.J. Becker, H. Urbach, B. Scheffler, T. Baden, S. Normann, R. Lahl, H.W. Pannek, I. Tuxhorn, C.E. Elger, J. Schramm, O.D. Wiestler, and I. Blümcke Focal cortical dysplasia of Taylor's balloon cell type: mutational analysis of the TSC1 gene indicates a pathogenic relationship to tuberous sclerosis Ann. Neurol. 52 2002 29 37
39. A.J. Becker, J. Chen, A. Zien, D. Sochivko, S. Normann, J. Schramm, C.E. Elger, O.D. Wiestler, and I. Blumcke Correlated stage- and subfield-associated hippocampal gene expression patterns in experimental and human temporal lobe epilepsy Eur. J. Neurosci. 18 2003 2792 2802
40. J.W. Bekenstein, and E.W. Lothman Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy Science 259 1993 97 100
41. E.A. Benardete, and A.R. Kriegstein Increased excitability and decreased sensitivity to GABA in an animal model of dysplastic cortex Epilepsia 43 2002 970 982
42. L.S. Benardo Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex J. Neurophysiol. 77 1997 3134 3144
43. R.A. Bender, S.V. Soleymani, A.L. Brewster, S.T. Nguyen, H. Beck, G.W. Mathern, and T.Z. Baram Enhanced expression of a specific hyperpolarization- activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus J. Neurosci. 23 2003 6826 6836
44. M.V. Bennett, and R.S. Zukin Electrical coupling and neuronal synchronization in the mammalian brain Neuron 41 2004 495 511
45. C. Bernard, M. Esclapez, J.C. Hirsch, and Y. Ben-Ari Interneurones are not so dormant in temporal lobe epilepsy: a critical reappraisal of the dormant basket cell hypothesis Epilepsy Res. 32 1998 93 103
46. A. Bernasconi, S.B. Antel, D.L. Collins, N. Bernasconi, A. Olivier, F. Dubeau, and G.B. Pike Texture analysis and morphological processing of MRI assist detection of focal cortical dysplasis in extra-temporal partial epilepsy Ann. Neurol. 49 2001 770 775
47. I. Blümcke, H. Beck, R. Nitsch, C. Eickhoff, B. Scheffler, M.R. Celio, J. Schramm, C.E. Elger, H.K. Wolf, and O.D. Wiestler Preservation of calretinin-immunoreactive neurons in the hippocampus of epilepsy patients with Ammon's horn sclerosis J. Neuropathol. Exp. Neurol. 55 1996 329 341
48. I. Blümcke, H. Beck, A.A. Lie, and O.D. Wiestler Molecular neuropathology of human mesial temporal lobe epilepsy Epilepsy Res. 36 1999 205 223
49. I. Blümcke, J.C. Schewe, S. Normann, O. Brüstle, J. Schramm, C.E. Elger, and O.D. Wiestler Increase of nestin-immunoreactive neural precursor cells in the dentate gyrus of pediatric patients with early-onset temporal lobe epilepsy Hippocampus 11 2001 311 321
50. I. Blümcke, M. Thom, and O.D. Wiestler Ammon's horn sclerosis: a maldevelopmental disorder associated with temporal lobe epilepsy Brain Pathol. 12 2002 199 211
51. H. Blumenfeld, M. Rivera, K.A. McNally, K. Davis, D.D. Spencer, and S.S. Spencer Ictal neocortical slowing in temporal lobe epilepsy Neurology 63 2004 1015 1021
52. R.A. Bronen, K.P. Vives, J.H. Kim, R.K. Fulbright, S.S. Spencer, and D.D. Spencer Focal cortical dysplasia of Taylor, balloon cell subtype: MR differentiation from low-grade tumors A.J.N.R. Am. J. Neuroradiol. 18 1997 1141 1151
53. R. Bruzzone, and C. Ressot Connexins, gap junctions and cell-cell signalling in the nervous system Eur. J. Neurosci. 9 1997 1 6
54. P.J. Buckle, and H.L. Haas Enhancement of synaptic transmission by 4-aminopyridine in hippocampal slices of the rat J. Physiol. 326 1982 109 122
55. E.H. Buhl, T.S. Otis, and I. Mody Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model Science 271 1996 369 373
56. W.H. Calvin, and G.W. Sypert Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat J. Neurophysiol. 39 1976 420 434
57. M. Capogna, B.H. Gahwiler, and S.M. Thompson Mechanism of μ-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro J. Physiol. (Lond.) 470 1993 539 558
58. P.L. Carlen, F. Skinner, L. Zhang, C. Naus, M. Kushnir, and J.L. Perez Velazquez The role of gap junctions in seizures Brain Res. Brain Res. Rev. 32 2000 235 241
59. E.A. Cavalheiro, D.F. Silva, W.A. Turski, L.S. Calderazzo-Filho, Z.A. Bortolotto, and L. Turski The susceptibility of rat to pilocarpine-induced seizures is age dependent Dev. Brain Res. 37 1987 43 58
60. E.A. Cavalheiro, J.P. Leite, Z.A. Bortolotto, W.A. Turski, C. Ikonomidou, and L. Turski Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures Epilepsia 32 1991 778 782
61. J.E. Cavazos, G. Golarai, and T.P. Sutula Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence J. Neurosci. 11 1991 2795 2803
62. C. Cepeda, R.S. Hurst, J. Flores-Hernandez, E. Hernandez-Echeagaray, G.J. Klapstein, M.K. Boylan, C.R. Calvert, E.L. Jocoy, O.K. Nguyen, V.M. Andre, H.V. Vinters, M.A. Ariano, M.S. Levine, and G.W. Mathern Morphological and electrophysiological characterization of abnormal cell types in pediatric cortical dysplasia J. Neurosci. Res. 72 2003 472 486
63. Y. Chagnac-Amitai, H.J. Luhmann, and D.A. Prince Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features J. Comp. Neurol. 296 1990 598 613
64. 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 Nat. Med. 7 2001 331 337
65. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles On the origin of interictal activity in human temporal lobe epilepsy in vitro Science 298 2002 1418 1421
66. A.S. Cohen, D.D. Lin, G.L. Quirk, and D.A. Coulter Dentate granule cell GABA(A) receptors in epileptic hippocampus: enhanced synaptic efficacy and altered pharmacology Eur. J. Neurosci. 17 2003 1607 1616
67. B.W. Colder, R.C. Frysinger, C.L. Wilson, R.M. Harper, and J. Engel Jr. Decreased neuronal burst discharge near site of seizure onset in epileptic human temporal lobes Epilepsia 37 1996 113 121
68. B receptor-mediated responses in neocortex of rat and cat J. Physiol. 406 1988 443 468
69. B.W. Connors, and M.A. Long Electrical synapses in the mammalian brain Annu. Rev. Neurosci. 27 2004 393 418
70. D. Contreras Electrophysiological classes of neocortical neurons Neural Netw. 17 2004 633 646
71. R. Cossart, C. Dinocourt, J.C. Hirsch, A. Merchan-Perez, J. De Felipe, Y. Ben-Ari, M. Esclapez, and C. Bernard Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy Nat. Neurosci. 4 2001 52 62
72. P.B. Crino, A.C. Duhaime, G. Baltuch, and R. White Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia Neurology 56 2001 906 913
73. J. Cronin, S. Obenaus, C.R. Houser, and F.E. Dudek Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of the mossy fibers. Brain Res. 573 1992 305 310
74. T.R. Cummins, Y. Xia, and G.G. Haddad Functional properties of rat and human neocortical voltage-sensitive sodium currents J. Neurophysiol. 71 1994 1052 1064
75. A receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex Brain 127 2004 1626 1640
76. R.A. DeFazio, and J.J. Hablitz Alterations in NMDA receptors in a rat model of cortical dysplasia J. Neurophysiol. 83 2000 315 321
77. J. DeFelipe Chandelier cells and epilepsy Brain 122 1999 1807 1822
78. R. Deisz GABA(B) receptor-mediated effects in human and rat neocortical neurones in vitro Neuropharmacology 38 1999 1755 1766
79. R. Dermietzel, and D.C. Spray Gap junctions in the brain: where, what type, how many and why? Trends Neurosci. 16 1993 186 192
80. D. Dietrich, T. Kral, H. Clusmann, M. Friedl, and J. Schramm Reduced function of L-AP4-sensitive metabotropic glutamate receptors in human epileptic sclerotic hippocampus Eur. J. Neurosci. 11 1999 1109 1113
81. J. Doherty, and R. Dingledine Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus J. Neurosci. 21 2001 2048 2057
82. S.M. Dombrowski, S.Y. Desai, M. Marroni, L. Cucullo, K. Goodrich, W. Bingaman, M.R. Mayberg, L. Bengez, and D. Janigro Overexpression of multiple drug resistance genes in endothelial cells from patients with refractory epilepsy Epilepsia 42 2001 1501 1506
83. F. Du, W.O. Whetsell, B. Abou-Khalil, B. Blumenkopf, E.W. Lothman, and R. Schwarcz Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy Epilepsy Res. 16 1993 223 233
84. F. Du, T. Eid, E.W. Lothman, C. Kohler, and R. Schwarcz Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy J. Neurosci. 15 1995 6301 6313
85. F. Dubeau, A. Palmini, D. Fish, M. Avoli, A. Gambardella, A. Spreafico, and F. Andermann The significance of electrocorticographic findings in focal cortical dysplasia: a review of their clinical, electrophysiological and neurochemical characterstics L.F. Quesney C.D. Binnie G.E. Chatrian Electro Corticography: Current Trends and Future Perspectives (EEG Suppl. 48) 1998 Elsevier Amsterdam and New York 77 96
86. M.J. During, K.M. Ryder, and D.D. Spencer Hippocampal GABA transporter function in temporal lobe epilepsy Nature 376 1995 174 177
87. 2+ epileptiform activity in human temporal slices Exp. Brain Res. 107 1995 321 325
88. R.C. Foehring, N.M. Lorenzon, P. Herron, and C.J. Wilson Correlation of physiologically and morphologically identified neuronal types in the human association cortex in vitro J. Neurophysiol. 66 1991 1825 1837
89. R.C. Foehring, and R.S. Waters Contributions of low-threshold calcium current and anomalous rectifier (Ih) to slow depolarizations underlying burst firing in human neocortical neurons in vitro Neurosci. Lett. 124 1991 17 21
90. C.G. Fonseca, C.R. Green, and L.F. Nicholson Upregulation in astrocytic connexin 43 gap junction levels may exacerbate generalized seizures in mesial temporal lobe epilepsy Brain Res. 929 2002 105 116
91. L.K. Friedman, D.E. Pellegrini-Giampietro, E.F. Sperber, M.V. Bennett, S.L. Moshe, and R.S. Zukin Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study J. Neurosci. 14 1994 2697 2707
92. J.M. Fritschy, T. Kiener, V. Bouilleret, and F. Loup GABAergic neurons and GABA(A)-receptors in temporal lobe epilepsy Neurochem. Int. 34 1999 435 445
93. S. Furtinger, S. Pirker, T. Czech, C. Baumgartner, G. Ransmayr, and G. Sperk Plasticity of Y1 and Y2 receptors and neuropeptide Y fibers in patients with temporal lobe epilepsy J. Neurosci. 21 2001 5804 5812
94. L.A. Gabel, and J.J. Lo Turco Layer I ectopias and increased excitability in murine neocortex J. Neurophysiol. 87 2002 2471 2479
95. S. Gabriel, M. Njunting, J.K. Pomper, M. Merschhemke, E.R. Sanabria, A. Eilers, A. Kivi, M. Zeller, H.J. Meencke, E.A. Cavalheiro, U. Heinemann, and T.N. Lehmann Stimulus and potassium-induced epileptiform activity in the human dentate gyrus from patients with and without hippocampal sclerosis J. Neurosci. 24 46 2004 10416 10430
96. A. Gambardella, A. Palmini, F. Andermann, F. Dubeau, J.C. Da Costa, L.F. Quesney, E. Andermann, and A. Olivier Usefulness of focal rhythmic discharges on scalp EEG of patients with focal cortical dysplasia and intractable epilepsy Electroencephalogr. Clin. Neurophysiol. 98 1996 243 249
97. R. Garbelli, C. Munari, S. De Biasi, L. Vitellaro-Zuccarello, C. Galli, M. Bramerio, R. Mai, G. Battaglia, and R. Spreafico Taylor's cortical dysplasia: a confocal and ultrastructural immuno-histochemical study Brain Pathol. 9 1999 445 461
98. P. Gloor The Temporal Lobe and Limbic System 1997 Oxford University Press Oxford
99. R. Guerrini, E. Andermann, M. Avoli, and W.B. Dobyns Cortical dysplasias, genetics and epileptogenesis A.V. Delgado-Escueta W. Wilson R.W. Olsen R.J. Porter Jasper's Basic Mechanisms of the Epilepsies, Advances in Neurology 79 1999 Lippincott-Raven Publishers New York 95 121
100. M.J. Gutnick, B.W. Connors, and D.A. Prince Mechanisms of neocortical epileptogenesis in vitro J. Neurophysiol. 48 1982 1321 1335
101. C.A. Haas, O. Dudeck, M. Kirsch, C. Huszka, G. Kann, S. Pollak, J. Zentner, and M. Frotscher Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy J. Neurosci. 22 2002 5797 5802
102. 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 117 2003 991 1002
103. J.V. Halliwell M-current in human neocortical neurones Neurosci. Lett. 67 1986 1 6
104. P.J. Harrison The neuropathology of schizophrenia. A critical review of the data and their interpretation Brain 122 1999 593 624
105. A. Harvey The role of febrile convulsions in mesial temporal sclerosis The Epilepsies: Etiologies and Prevention 1999 Academic Press New York pp. 125-131
106. T.R. Henry, K.A. Frey, J.C. Sackellares, S. Gilman, R.A. Koeppe, J.A. Brunberg, D.A. Ross, S. Berent, A.B. Young, and D.E. Kuhl In vivo cerebral metabolism and central benzodiazepine-receptor binding in temporal lobe epilepsy Neurology 43 1993 1998 2006
107. A. Hermann, and A.L. Gorman Effects of 4-aminopyridine on potassium currents in a molluscan neuron J. Gen. Physiol. 78 1981 63 86
108. M. Higashima, H. Kinoshita, N. Yamaguchi, and Y. Koshino Activation of GABAergic function necessary for afterdischarge generation in rat hippocampal slices Neurosci. Lett. 207 1996 101 104
109. S.G. Hormuzdi, M.A. Filippov, G. Mitropoulou, H. Monyer, and R. Bruzzone Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks Biochem. Biophys. Acta 1662 2004 113 137
110. C.R. Houser Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy Brain Res. 535 1990 195 204
111. C.R. Houser, J.E. Miyashiro, B.E. Swartz, G.O. Walsh, J.R. Rich, and A.V. Delgado-Escueta Altered patterns of dynorphin immunoreactivity suggest mossy fiber oreorganization in human hippocampal epilepsy J. Neurosci. 10 1990 267 282
112. C.R. Houser, and M. Esclapez Downregulation of the alpha 5 subunit of the GABA(A) receptor in the pilocarpine model of temporal lobe epilepsy Hippocampus 13 2003 633 645
113. G.G. Hwa, and M. Avoli The involvement of excitatory amino acids in neocortical epileptogenesis: NMDA and non-NMDA receptors Exp. Brain Res. 86 1991 248 256
114. G.G. Hwa, M. Avoli, A. Oliver, and J.G. Villemure Bicuculline-induced epileptogenesis in the human neocortex maintained in vitro Exp. Brain Res. 83 1991 329 339
115. G.G. Hwa, and M. Avoli Excitatory synaptic transmission mediated by NMDA and non-NMDA receptors in the superficial/middle layers of the epileptogenic human neocortex maintained in vitro Neurosci. Lett. 143 1992 83 86
116. M. Isokawa, G. Avanzini, D.M. Finch, T.L. Babb, and M.F. Levesque Physiologic properties of human dentate granule cells in slices prepared from epileptic patients Epilepsy Res. 9 1991 242 250
117. M. Isokawa, and M.F. Levesque Increased NMDA responses and dendritic degeneration in human epileptic hippocampal neurons in slices Neurosci. Lett. 132 1991 212 216
118. M. Isokawa, M.F. Levesque, T.L. Babb, and J. Engel Jr. Single mossy fiber axonal systems of human dentate granule cells studied in hippocampal slices from patients with temporal lobe epilepsy J. Neurosci. 13 1993 1511 1522
119. M. Isokawa Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus J. Neurophysiol. 75 1996 1901 1908
120. M. Isokawa, M. Levesque, I. Fried, and J. Engel Jr. Glutamate currents in morphologically identified human dentate granule cells in temporal lobe epilepsy J. Neurophysiol. 77 1997 3355 3369
121. M. Isokawa Remodeling dendritic spines of dentate granule cells in temporal lobe epilepsy patients and the rat pilocarpine model Epilepsia 41 2000 S14 S17
122. G.D. Jackson, A.M. McIntosh, R.S. Briellmann, and S.F. Berkovic Hippocampal sclerosis studied in identical twins Neurology 51 1998 78 84
123. K.M. Jacobs, M.J. Gutnick, and D.A. Prince Hyperexcitability in a model of cortical maldevelopment Cereb. Cortex 6 1996 514 523
124. J. Janszky, R. Schulz, M. Hoppe, and A. Ebner Spikes on the postoperative EEG are related to preoperative spike frequency and postoperative seizures Epilepsy Res. 57 2003 153 158
125. E.W. Johnson, N.C. deLanerolle, and J.H. Kim Central and peripheral benzodiazepine receptors: opposite changes in human epileptogenic tissue Neurology 42 1992 811 815
126. D.J. Jones, and W.B. Stavinoha Levels of cyclic nucleotides in mouse regional brain following 300 ms microwave inactivation J. Neurochem. 28 1977 759 763
127. K. Kaila Ionic basis of GABAA receptor channel function in the nervous system Prog. Neurobiol. 42 1994 489 537
128. + transient J. Neurosci. 17 1997 7662 7672
129. H. Kato, Z. Ito, S. Matsuoko, and Y. Sakurai Electrical activities of neurons in the sliced human cortex in vitro Electroenceph. Clin. Neurophysiol. 35 1973 457 462
130. C. Kerfoot, H.V. Vinters, and G.W. Mathern Cerebral cortical dysplasia: giant neurons show potential for increased excitation and axonal plasticity Dev. Neurosci. 21 1999 260 270
131. I. Khalilov, G.L. Holmes, and Y. Ben-Ari In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures Nat. Neurosci. 6 2003 1079 1085
132. S.J. Kish, L.M. Dixon, and A.L. Sherwin Aspartic acid aminotransferase activity is increased in actively spiking compared with non-spiking human epileptic cortex J. Neurol. Neurosurg. Psychiatry 51 1988 552 556
133. G.J. Klapstein, and W.F. Colmers Neuropeptide Y suppresses epileptiform activity in rat hippocampus in vitro J. Neurophysiol. 78 1997 1651 1961
134. R. Köhling, A. Lücke, H. Straub, E.J. Speckmann, I. Tuxhorn, P. Wolf, H. Pannek, and F. Oppel Spontaneous sharp waves in human neocortical slices excised from epileptic patients Brain 121 1998 1073 1087
135. R. Köhling, M. Que, K. Zilles, and E.J. Speckmann Current-source density profiles associated with sharp waves in human epileptic neocortical tissue Neuroscience 94 1999 1039 1050
136. R. Köhling, J.M. Höhling, H. Straub, D. Kuhlmann, U. Kuhnt, I. Tuxhorn, A. Ebner, P. Wolf, H.W. Pannek, A. Gorji, and E.J. Speckmann Optical monitoring of neuronal activity during spontaneous sharp waves in chronically epileptic human neocortical tissue J. Neurophysiol. 84 2000 2161 2165
137. A receptor-mediated oscillations J. Neurosci. 20 2001 6820 6829
138. R. Köhling, U.R. Koch, G. Hagemann, C. Redecker, H. Straub, and E.J. Speckmann Differential sensitivity to induction of spreading depression by partial disinhibition in chronically epileptic human and rat as compared to native rat neocortical tissue Brain Res. 975 2003 129 134
139. G. Kostopoulos, C. Drapeau, M. Avoli, A. Olivierm, and J.G. Villemeure Endogenous adenosine can reduce epileptiform activity in the human epileptogenic cortex maintained in vitro Neurosci. Lett. 106 1989 119 124
140. K. Krnjevic Principles of synaptic transmission Adv. Neurol. 27 1980 127 154
141. K. Krnjevic GABA mechanisms in epilepsy G. Tunnicliff B.U. Raess Significance of GABA in Brain Function 1991 Wiley-Liss New York 47 87
142. P. Kwan, G.J. Sills, E. Butler, T.W. Gant, B.S. Meldrum, and M.J. Brodie Regional expression of multidrug resistance genes in genetically epilepsy-prone rat brain after a single audiogenic seizure Epilepsia 43 2002 1318 1323
143. N.A. Lambert, and W.A. Wilson Heterogeneity in presynaptic regulation of GABA release from hippocampal inhibitory neurons Neuron 11 1993 1057 1067
144. K. Lamsa, and K. Kaila Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine J. Neurophysiol. 78 1997 2582 2591
145. J. Laschet, S. Trottier, V. Leviel, B. Guibert, J.Y. Bansard, P. Chauvel, and M. Bureau Heterogeneous distribution of polyamines in temporal lobe epilepsy Epilepsy Res. 35 1999 161 172
146. A. Lazarowski, G. Sevlever, A. Taratuto, M. Massaro, and A. Rabinowicz Tuberous sclerosis associated with MDR1 gene expression and drug-resistant epilepsy Pediatr. Neurol. 21 1999 731 734
147. D.V. Lewis Febrile convulsions and mesial temporal sclerosis Curr. Opin. Neurol. 12 1999 197 201
148. A-mediated inhibition in ictal-like discharges in the rat entorhinal cortex J. Neurophysiol. 79 1998 352 360
149. N.M. Lorenzon, and R.C. Foehring Relationship between repetitive firing and afterhyperpolarizations in human neocortical neurons J. Neurophysiol. 67 1992 350 363
150. W. Löscher, and H. Potschka Role of multidrug transporters in pharmacoresistance to antiepileptic drugs J. Pharmacol. Exp. Ther. 301 2002 7 14
151. F. Loup, H.G. Wieser, Y. Yonekawa, A. Aguzzi, and J.M. Fritschy Selective alterations in GABAA receptor subtypes in human temporal lobe epilepsy J. Neurosci. 20 2000 5401 5419
152. J. Louvel, R. Pumain, M. Avoli, I. Kurcewicz, B. Devaux, and J.P. Chodkiewicz GABAA inhibition controls the calcium flows during NMDA-dependent epileptiform activity in human epileptogenic neocortex Epilepsy Res. Suppl. 12 1996 293 300
153. J. Louvel, C. Papatheodoropoulos, A. Siniscalchi, I. Kurciewicz, R. Pumain, B. Devaux, B. Turak, J.P. Chodkiewicz, V. Esposito, J.G. Villemeure, and M. Avoli GABA-Mediated synchronization in the human cortex: elevations in extracellular potassium and presynaptic mechanisms Neuroscience 105 2001 803 813
154. H.J. Luhmann, and K. Raabe Characterization of neuronal migration disorders in neocortical structures. I. Expression of epileptiform activity in an animal model Epilepsy Res. 26 1996 67 74
155. H.J. Luhmann, N. Karpuk, M. Qu, and K. Zilles Characterization of neuronal migration disorders in neocortical structures. II. Intracellular in vitro recordings J. Neurophysiol. 80 1998 92 102
156. D.V. Madison, and R.A. Nicoll Enkephalin hyperpolarizes interneurons in the rat hippocampus J. Physiol. (Lond.) 398 1988 123 130
157. L. Maillard, J.P. Vignal, M. Gavaret, M. Guye, A. Biraben, A. McGonigal, P. Chauvel, and F. Bartolomei Semiologic and electrophysiologic correlations in temporal lobe seizure subtypes Epilepsia 45 2004 1590 1599
158. P. Marco, R.G. Sola, P. Pulido, M.T. Alijarde, A. Sanchez, S. Ramon y Cajal, and DeFelipe S J. Inhibitory neurons in the human epileptogenic temporal neocortex. An immunocytochemical study Brain 119 1996 1327 1347
159. G.W. Mathern, J.K. Pretorius, H.I. Kornblum, D. Mendoza, A. Lozada, J.P. Leite, L.M. Chimelli, I. Fried, A.C. Sakamoto, J.A. Assirati, M.F. Levesque, P.D. Adelson, and W.J. Peacock Human hippocampal AMPA and NMDA mRNA levels in temporal lobe epilepsy patients Brain 120 1997 1937 1959
160. G.W. Mathern, J.K. Pretorius, J.P. Leite, H.I. Kornblum, D. Mendoza, A. Lozada, and E.H. Bertram III Hippocampal AMPA and NMDA mRNA levels and subunit immunoreactivity in human temporal lobe epilepsy patients and a rodent model of chronic mesial limbic epilepsy Epilepsy Res. 32 1998 154 171
161. G.W. Mathern, J.K. Pretorius, D. Mendoza, J.P. Leite, L. Chimelli, D.E. Born, I. Fried, J.A. Assirati, G.A. Ojemann, P.D. Adelson, L.D. Cahan, and H.I. Kornblum Hippocampal N-methyl-d-aspartate receptor subunit mRNA levels in temporal lobe epilepsy patients Ann. Neurol. 46 1999 343 358
162. D. Mattia, A. Olivier, and M. Avoli Seizure-like discharges recorded in the human dysplastic neocortex maintained in vitro Neurology 45 1995 1391 1395
163. D.A. McCormick, B.W. Connors, J.W. Lighthall, and D.A. Prince Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex J. Neurophysiol. 54 1985 782 806
164. D.A. McCormick GABA as an inhibitory neurotransmitter in human cerebral cortex J. Neurophysiol. 62 1989 1018 1027
165. D.A. McCormick, and A. Williamson Convergence and divergence of neurotransmitter action in human cerebral cortex Proc. Natl. Acad. Sci. U.S.A. 86 1989 8098 8102
166. J.W. McDonald, E. Garafalo, T. Hood, J.C. Sackellares, S. Gilman, P.E. McKeever, J.C. Troncoso, and M.V. Johnston Altered excitatory and inhibitory amino acid receptor binding in hippocampus of patients with temporal lobe epilepsy Ann. Neurol. 29 1991 529 541
167. B. Meldrum Excitotoxicity and epileptic brain damage Epilepsy Res. 10 1991 55 61
168. B.S. Meldrum, and A.G. Chapman Excitatory amino acid receptors and antiepileptic drug development Adv. Neurol. 79 1999 965 978
169. L. Menendez de la Prida, R. Benavides-Piccione, R. Sola, and M.A. Pozo Electrophysiological properties of interneurons from intraoperative spiking areas of epileptic human temporal neocortex Neuroreport 13 2002 1421 1425
170. A receptors in the hippocampus Science 253 1991 1420 1423
171. U. Misgeld, W. Müller, and H. Brunner Effects of (-)baclofen on inhibitory neurons in the guinea pig hippocambpal slice Pflügers Arch. 414 1989 139 144
172. + accumulations and synchronous GABA-mediated potentials evoked by 4-aminopyridine in the adult rat hippocampus Exp. Brain Res. 109 1996 71 82
173. S.L. Moshe Mechanisms of action of anticonvulsant agents Neurology 55 2000 S32 S40
174. U. Mußhoff, R. Kohling, A. Lucke, E. Speckmann, I. Tuxhorn, P. Wolf, H.W. Pauuek, and F. Oppel Vigabatrin reduces epileptiform activity in brain slices from pharmacoresistant epilepsy patients Eur. J. Pharmacol. 401 2000 167 172
175. T. Nakase, and C.C. Naus Gap junctions and neurological disorders of the central nervous system Biochim. Biophys. Acta. 1662 2004 149 158
176. C.C. Naus, J.F. Bechberger, and D.L. Paul Gap junction gene expression in human seizure disorder Exp. Neurol. 111 1991 198 203
177. N.R. Newberry, and R.A. Nicoll Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells Nature 308 1984 450 452
178. N.R. Newberry, and R.A. Nicoll Comparison of the action of baclofen with gamma-aminobutyric acid on rat hippocampal slices in vitro J. Physiol. 360 1985 161 185
179. R.A. Nicoll, J.C. Eccles, T. Oshima, and F. Rubia Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates Nature 258 1975 625 627
180. R.W. Olsen, M. Bureau, C.R. Houser, A.V. Delgado-Escueta, J.G. Richards, and H. Möhler GABA/benzodiazepine receptors in human focal epilepsy Epilepsy Res. (Suppl.) 8 1992 383 891
181. R.W. Olsen, and M. Avoli GABA and epileptogenesis Epilepsia 38 1997 399 407
182. R.W. Olsen, and R.L. Macdonald GABAA receptor complex: structure and function J. Egeberg A. Schousboe P. Krogsgaard-Larsen Glutamate and GABA receptors and transporters: structure, function and pharmacology 2002 Taylor & Francis London 202 219
183. R.W. Olsen, C.S. Chang, G. Li, H.J. Hanchar, and M. Wallner Fishing for allosteric sites on GABA(A) receptors Biochem. Pharmacol. 68 2004 1675 1684
184. E. Palma, D.A. Ragozzino, S. Di Angelantonio, G. Spinelli, F. Trettel, A. Martinez-Torres, G. Torchia, A. Arcella, G. Di Gennaro, P.P. Quarato, V. Esposito, G. Cantore, R. Miledi, and F. Eusebi Phosphatase inhibitors remove the run-down of gamma-aminobutyric acid type A receptors in the human epileptic brain Proc. Natl. Acad. Sci. U.S.A. 101 2004 10183 10188
185. E. Palma, G. Torchia, C. Limatola, F. Trettel, A. Arcella, G. Cantore, G. Di Gennaro, M. Manfredi, V. Esposito, P.P. Quarato, R. Miledi, and F. Eusebi BDNF modulates GABAA receptors microtransplanted from the human epileptic brain to Xenopus oocytes Proc. Natl. Acad. Sci. U.S.A. 102 2005 1667 1672
186. E. Palma, G. Spinelli, G. Torchia, A. Martinez-Torres, D. Ragozzino, R. Miledi, and F. Eusebi Abnormal GABAA receptors from the human epileptic hippocampal subiculum microtransplanted to Xenopus oocytes Proc. Natl. Acad. Sci. U.S.A. 102 2005 2514 2518
187. A. Palmini, F. Andermann, A. Olivier, D. Tampieri, Y. Robitaille, E. Andermann, and G. Wright Focal neuronal migration disorders and intractable partial epilepsy: a study of 30 patients Ann. Neurol. 30 1991 741 749
188. A. Palmini, A. Gambardella, F. Andermann, F. Dubeau, J.C. da Costa, A. Olivier, D. Tampieri, P. Gloor, F. Quesney, and E. Andermann Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results Ann. Neurol. 37 1995 476 487
189. Z. Peng, C.S. Huang, B.M. Stell, I. Mody, and C.R. Houser Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy J. Neurosci. 24 2004 8629 8639
190. J.L. Perez-Velazquez, and P.L. Carlen Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice Eur. J. Neurosci. 11 1999 4110 4118
191. P. Perreault, and M. Avoli Effects of low concentrations of 4-aminopyridine on CA1 pyramidal cells of the hippocampus J. Neurophysiol. 61 1989 953 970
192. P. Perreault, and M. Avoli Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices J. Neurophysiol. 65 1991 771 785
193. P. Perreault, and M. Avoli 4-Aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus J. Neurosci. 12 1992 104 115
194. H. Potschka, and W. Loscher In Vivo evidence for P-glycoprotein-mediated transport of phenytoin at the blood-brain barrier of rats Epilepsia 42 2001 1231 1240
195. H. Potschka, M. Fedrowitz, and W. Loscher P-Glycoprotein and multidrug resistance-associated protein are involved in the regulation of extracellular levels of the major antiepileptic drug carbamazepine in the brain Neuroreport 12 2001 3557 3560
196. H. Potschka, M. Fedrowitz, and W. Loscher Multidrug resistance protein MRP2 contributes to blood-brain barrier function and restricts antiepileptic drug activity J. Pharmacol. Exp. Ther. 306 2003 124 131
197. M.O. Poulter, L.A. Brown, S. Tynan, G. Willick, R. William, and D.C. McIntyre Differential expression of alpha1, alpha2, alpha3, and alpha5 GABAA receptor subunits in seizure-prone and seizure-resistant rat models of temporal lobe epilepsy J. Neurosci. 19 1999 4654 4661
198. D.A. Prince, and R.K. Wong Human epileptic neurons studied in vitro Brain. Res. 210 1981 323 333
199. D.P. Purpura Stability and seizure susceptibility of immature brain H.H. Jasper A.A. Ward A. Pope Basic Mechanisms of the Epilepsies 1969 Little Brown Boston 481 505
200. 2+ entry J. Neurosci. 17 1997 8169 8177
201. + currents in acutely isolated human hippocampal dentate granule cells J. Physiol. 509 1998 139 150
202. S. Remy, S. Gabriel, B.W. Urban, D. Dietrich, T.N. Lehmann, C.E. Elger, U. Heinemann, and H. Beck A novel mechanism underlying drug resistance in chronic epilepsy Ann. Neurol. 53 2003 469 479
203. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation Nature 397 1999 251 255
204. C. Rivera, J. Voipio, J. Thomas-Crusells, H. Li, Z. Emri, S. Sipila, J.A. Payne, L. Minichiello, M. Saarma, and K. Kaila Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2 J. Neurosci. 24 2004 4683 4691
205. M. Rizzi, S. Caccia, G. Guiso, C. Richichi, J.A. Gorter, E. Aronica, M. Aliprandi, R. Bagnati, R. Fanelli, M. D'Incalci, R. Samanin, and A. Vezzani Limbic seizures induce P-glycoprotein in rodent brain: functional implications for pharmacoresistance J. Neurosci. 22 2002 5833 5839
206. M.A. Rogawski The NMDA receptor, NMDA antagonists and epilepsy therapy: a status report Drugs 44 1992 279 292
207. S.N. Roper, M.A. King, L.A. Abraham, and M.A. Boillot Disinhibited in vitro neocortical slices containing experimentally induced cortical dysplasia demonstrate hyperexcitability Epilepsy Res. 26 1997 443 449
208. P.A. Rutecki, F.J. Lebeda, and D. Johnston 4-Aminopyridine produces epileptiform activity in hippocampus and enhances synaptic excitation and inhibition J. Neurophysiol. 57 1987 1911 1924
209. P.A. Rutecki, R.G. Grossman, D. Armstrong, and S.J. Irish-Loewen Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures J. Neurosurg. 70 1989 667 675
210. Y. Sata, K. Matsuda, T. Mihara, M. Aihara, K. Yagi, and Y. Yonekura Quantitative analysis of benzodiazepine receptor in temporal lobe epilepsy: [(125)I]iomazenil autoradiographic study of surgically resected specimens Epilepsia 43 2002 1039 1048
211. I. Savic, P. Roland, F. Sedvall, A. Persson, S. Pauli, and L. Widen In-vivo demonstration of reduced benzodiazepine receptor binding in human epileptic foci Lancet 2 1988 863 866
212. R.J. Sayer, A.M. Brown, P.C. Schwindt, and W.E. Crill Calcium currents in acutely isolated human neocortical neurons J. Neurophysiol. 69 1993 1596 1606
213. A.H. Schinkel, U. Mayer, E. Wagenaar, C.A.A.M. Mol, L. Van Deemter, J.J.M. Smit, M.A. van der Valk, A.C. Voordouw, H. Spits, O. van Tellingen, J.M. Zijlmans, W.E. Fibbe, and P. Borst Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins Proc. Natl. Acad. Sci. U.S.A. 94 1997 4028 4033
214. A. Schousboe, A. Frandsen, P. Wahl, and P. Krogsgaard-Larsen Neurotoxicity and excitatory amino acid antagonists Neurotoxicology 15 1994 477 481
215. T.B. Schumacher, H. Beck, C. Steinhauser, J. Schramm, and C.E. Elger Effects of phenytoin, carbamazepine, and gabapentin on calcium channels in hippocampal granule cells from patients with temporal lobe epilepsy Epilepsia 39 1998 355 363
216. P.A. Schwartzkroin, D.A. Turner, W.D. Knowles, and A.R. Wyler Studies of human and monkey "epileptic" neocortex in the in vitro slice preparation Ann. Neurol. 13 1983 249 257
217. P.A. Schwartzkroin, and W.D. Knowles Intracellular study of human epileptic cortex: in vitro maintenance of epileptiform activity? Science 223 1984 709 712
218. P.A. Schwartzkroin, and M.M. Haglund Spontaneous rhythmic synchronous activity in epileptic human and normal monkey temporal lobe Epilepsia 27 1986 523 533
219. A. Semyanov, M.C. Walker, D.M. Kullmann, and R.A. Silver Tonically active GABA A receptors: modulating gain and maintaining the tone Trends Neurosci. 27 2004 262 269
220. M.D. Shumate, D.D. Lin, J.W. Gibbs III, K.L. Holloway, and D.A. Coulter GABA(A) receptor function in epileptic human dentate granule cells: comparison to epileptic and control rat Epilepsy Res. 32 1998 114 128
221. S.M. Sisodiya, W.R. Lin, M.V. Squier, and M. Thom Multidrug-resistance protein 1 in focal cortical dysplasia Lancet 357 2001 42 43
222. S.M. Sisodiya, W.R. Lin, B.N. Harding, M.V. Squier, and M. Thom Drug resistance in epilepsy: expression of drug resistance proteins in common causes of refractory epilepsy Brain 125 2002 22 31
223. S.M. Sisodiya Mechanisms of antiepileptic drug resistance Curr. Opin. Neurol. 16 2003 197 201
224. R.S. Sloviter Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy Hippocampus 1 1991 41 66
225. S. Smirnov, P. Paalasmaa, M. Uusisaari, J. Voipio, and K. Kaila Pharmacological isolation of the synaptic and nonsynaptic components of the GABA-mediated biphasic response in rat CA1 hippocampal pyramidal cells J. Neurosci. 19 1999 9252 9260
226. M.D. Smyth, N.M. Barbaro, and S.C. Baraban Effects of antiepileptic drugs on induced epileptiform activity in a rat model of dysplasia Epilepsy Res. 50 2002 251 264
227. W. Sommer Erkrankungen des Ammonshorns als aetiologisches Moment der Epilepsie Arch. Psych. Nervenkr. 10 1880 631 675
228. S.S. Spencer, and D.D. Spencer Entorhinal-hippocampal interactions in temporal lobe epilepsy Epilepsia 35 1994 721 727
229. D. Spray Physiological properties of gap junction channels in the nervous system D.C. Spray Gap Junctions in the Nervous System 1996 Landes, RG Austin, Texas 27 36
230. R. Spreafico, G. Battaglia, P. Arcelli, F. Andermann, F. Dubeau, A. Palmini, A. Olivier, J.G. Villemure, D. Tampieri, G. Avanzini, and M. Avoli Cortical dysplasia: an immunocytochemical study of three patients Neurology 50 1998 27 36
231. C.E. Stafstrom, P.C. Schwindt, J.A. Flatman, and W.E. Crill Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro J. Neurophysiol. 52 1984 244 263
232. A receptors Science 269 1995 977 981
233. M. Steriade The Intact and Sliced Brain 2001 The MIT Press Cambridge, MA
234. H. Straub, R. Köhling, J. Höhling, C. Rundfeldt, I. Tuxhorn, A. Ebner, P. Wolf, H. Pannek, and E. Speckmann Effects of retigabine on rhythmic synchronous activity of human neocortical slices Epilepsy Res. 44 2001 155 165
235. B.W. Strowbridge, L.M. Masukawa, D.D. Spencer, and G.M. Shepherd Hyperexcitability associated with localizable lesions in epileptic patients Brain Res. 587 1992 158 163
236. T. Sutula, G. Cascino, J. Cavazos, I. Parada, and L. Ramirez Mossy fiber synaptic reorganization in the epileptic human temporal lobe Ann. Neurol. 26 1989 321 330
237. J.G. Tasker, W.J. Peacock, and F.E. Dudek Local synaptic circuits and epileptiform activity in slices of neocortex from children with intractable epilepsy J. Neurophysiol. 67 1992 496 507
238. L. Tassi, B. Pasquier, L. Minotti, R. Garbelli, P. Kahane, A.L. Benabid, G. Battaglia, C. Munari, and R. Spreafico Cortical dysplasia: electroclinical, imaging, and neuropathologic study of 13 patients. Epilepsia 42 2001 1112 1123
239. L. Tassi, N. Colombo, R. Garbelli, S. Francione, G. Lo Russo, R. Mai, F. Cardinale, M. Cossu, A. Ferrario, C. Galli, M. Bramerio, A. Citterio, and R. Spreafico Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome Brain 125 2002 1719 1732
240. L. Tassi, N. Colombo, M. Cossu, R. Mai, S. Francione, G. Lo Russo, C. Galli, M. Bramerio, G. Battaglia, R. Garbelli, A. Meroni, and R. Spreafico Electroclinical, MRI and neuropathological study of 10 patients with nodular heterotopia, with surgical outcomes Brain 12 2005 321 337
241. D.C. Taylor, M.A. Falconer, C.J. Bruton, and J.A.N. Corsellis Focal dysplasia of the cerebral cortex in epilepsy J. Neurol. Neurosurg. Psychiatry 34 1971 369 387
242. A.E. Telfeian, and B.W. Connors Epileptiform propagation patterns mediated by NMDA and non-NMDA receptors in rat neocortex Epilepsia 40 1999 1499 1506
243. A.E. Telfeian, D.D. Spencer, and A. Williamson Lack of correlation between neuronal hyperexcitability and electrocorticographic responsiveness in epileptogenic human neocortex J. Neurosurg. 90 1999 939 945
244. P.M. Thomas, J.P. Phillips, and W.T. O'Connor Microdialysis of the lateral and medial temporal lobe during temporal lobe epilepsy surgery Surg. Neurol. 63 2005 70 79
245. S.M. Thompson, and B.H. Gähwiler Comparison of the actions of baclofen at pre- and post-synaptic receptors in the rat hippocampus in vitro J. Physiol. (Lond.) 451 1992 329 345
246. A.M. Thomson, and J. Deuchars Temporal and spatial properties of local circuits in neocortex Trends Neurosci. 7 1994 119 126
247. D.M. Tishler, K.I. Weinberg, D.R. Hinton, N. Barbaro, G.M. Annett, and C. Raffel MDR1 gene expression in brain of patients with medically intractable epilepsy Epilepsia 36 1995 1 6
248. M.N. Titulaer, W. Kamphuis, C.W. Pool, J.J. van Heerikhuize, and F.H. Lopes da Silva Kindling induces time-dependent and regional specific changes in the [3H]muscimol binding in the rat hippocampus: a quantitative autoradiographic study Neuroscience 59 1994 817 826
249. K. Toyooka, S. Iritani, T. Makifuchi, O. Shirakawa, N. Kitamura, K. Maeda, R. Nakamura, K. Niizato, M. Watanabe, A. Kakita, H. Takahashi, T. Someya, and H. Nawa Selective reduction of a PDZ protein, SAP-97, in the prefrontal cortex of patients with chronic schizophrenia J. Neurochem. 83 2002 797 806
250. R.D. Traub, and R. Dingledine Model of synchronized epileptiform bursts induced by high potassium in CA3 region of rat hippocampal slice. Role of spontaneous EPSPs in initiation J. Neurophysiol. 64 1990 1009 1018
251. S.F. Traynelis, and R. Dingledine Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice J. Neurophysiol. 59 1988 259 276
252. S. Trottier, B. Evrard, A. Biraben, and P. Chauvel Altered patterns of catecholaminergic fibers in focal cortical dysplasia in two patients with partial seizures Epilepsy Res. 19 1994 161 179
253. S. Trottier, B. Evrard, J.P. Vignal, J.M. Scarabin, and P. Chauvel The serotonergic innervation of the cerebral cortex in man and its changes in focal cortical dysplasia Epilepsy Res. 25 1996 79 106
254. B. Tu, O. Timofeeva, Y. Jiao, and J.V. Nadler Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain J. Neurosci. 25 2005 1718 1729
255. C. Vale, and D.H. Sanes Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain J. Neurosci. 20 2000 1912 1921
256. M. Vreugdenhil, C.W. van Veelen, P.C. van Rijen, F.H. Lopes da Silva, and W.J. Wadman Effect of valproic acid on sodium currents in cortical neurons from patients with pharmaco-resistant temporal lobe epilepsy Epilepsy Res. 32 1998 309 320
257. M. Vreugdenhil, G. Hoogland, C.W. van Veelen, and W.J. Wadman Persistent sodium current in subicular neurons isolated from patients with temporal lobe epilepsy Eur. J. Neurosci. 19 2004 2769 2778
258. F. Wendling, F. Bartolomei, J.J. Bellanger, and P. Chauvel Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition Eur. J. Neurosci. 15 2002 1499 1508
259. H.J. Wenzel, C.A. Robbins, L.H. Tsai, and P.A. Schwartzkroin Abnormal morphological and functional organization of the hippocampus in a p35 mutant model of cortical dysplasia associated with spontaneous seizures J. Neurosci. 21 2001 983 998
260. S. Wiebe, W.T. Blume, J.P. Girvin, and M. Eliasziw A randomized, controlled trial of surgery for temporal-lobe epilepsy N. Engl. J. Med. 345 2001 311 318
261. S. Williams, and J.C. Lacaille GABAB receptor-mediated inhibitory post-synaptic potentials evoked by electrical stimulation and by glutamate stimulation of interneurons in stratum lacunosum-moleculare in hippocampal CA1 pyramidal cells in vitro Synapse 11 1992 249 258
262. S. Williams, P. Vachon, and J.C. Lacaille Monosynaptic GABA-mediated inhibitory postsynaptic potentials in CA1 pyramidal of hyperexcitable hippocampal slices from kainic acid-treated rats Neuroscience 52 1993 541 554
263. A. Williamson, S.S. Spencer, and D.D. Spencer Depth electrode studies and intracellular dentate granule cell recordings in temporal lobe epilepsy Ann. Neurol. 38 1995 778 787
264. A. Williamson, P.R. Patrylo, S. Lee, and D.D. Spencer Physiology of human cortical neurons adjacent to cavernous malformations and tumors Epilepsia 44 2003 1413 1419
265. C.L. Wilson, S.U. Khan, J. Engel Jr., M. Isokawa, T.L. Babb, and E.J. Behnke Paired pulse suppression and facilitation in human epileptogenic hippocampal formation Epilepsy Res. 31 1998 211 230
266. A receptor alpha 1 subunit in patients with chronic pharmacoresistant epilepsies Acta Neuropathol. 88 1994 313 319
267. C. Wozny, A. Kivi, T.N. Lehmann, C. Dehnicke, U. Heinemann, and J. Behr Comment on "On the origin of interictal activity in human temporal lobe epilepsy in vitro" Science 301 2003 463
268. J.P. Wuarin, W.J. Peacock, and F.E. Dudek Single-electrode voltage-clamp analysis of the N-methyl-d-aspartate component of synaptic responses in neocortical slices from children with intractable epilepsy J. Neurophysiol. 67 1992 84 93
269. A.R. Wyler, F.C. Dohan Jr., J.B. Schweitzer, and A.D. Berry A grading system for mesial temporal pathology (hippocampal sclerosis) from anterior temporal lobectomy J. Epilepsy 5 1992 220 225
270. D.M. Yilmazer-Hanke, H.K. Wolf, J. Schramm, C.E. Elger, O.D. Wiestler, and I. Blümcke Subregional pathology of the amygdala complex and entorhinal region in surgical specimens from patients with pharmacoresistant temporal lobe epilepsy J. Neuropathol. Exp. Neurol. 59 2000 907 920
271. Z. Ying, T.L. Babb, N. Mikuni, I. Najm, J. Drazba, and W. Bingaman Selective coexpression of NMDAR2A/B and NMDAR1 subunit proteins in dysplastic neurons of human epileptic cortex Exp. Neurol. 159 1999 409 418
272. W.J. Zhu, and S.N. Roper Reduced inhibition in an animal model of cortical dysplasia J. Neurosci. 20 2000 8925 8931
273. E.C. Zuckermann, and G.H. Glaser Hippocampal epileptic activity induced by localized ventricular perfusion with high-potassium cerebrospinal fluid Exp. Neurol. 20 1968 87 110