GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex

Brain

Volumn 127, Issue 7, 2004, Pages 1626-1640

  D'Antuono, M ^a,b   Louvel, J ^d   Kohling R ^e   Mattia, D ^c   Bernasconi, A ^f   Olivier, A ^f   Turak, B ^d   Devaux, A ^d   Pumain, R ^d   Avoli, M ^a,b,f,g  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS NEUROMED   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d CENTRE HOSPITALIER SAINTE ANNE   (France)

^e UNIVERSITY OF BONN   (Germany)

^f MCGILL UNIVERSITY   (Canada)

^g NONE   (Canada)

Author keywords

Baclofen; Epileptiform synchronization; Focal cortical dysplasia; GABA receptors

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; POTASSIUM ION; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; 4 AMINOPYRIDINE; BACLOFEN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM; POTASSIUM CHANNEL BLOCKING AGENT;

4 AMINOBUTYRIC ACID RELEASE; ADOLESCENT; ADULT; ARTICLE; BRAIN SLICE; CHILD; CONTROLLED STUDY; CORTICAL DYSPLASIA; CORTICAL SYNCHRONIZATION; EPILEPTIC STATE; EPILEPTOGENESIS; FACILITATION; FEMALE; GABAERGIC SYSTEM; HUMAN; HUMAN TISSUE; INTERNEURON; INTRACTABLE EPILEPSY; MALE; NEOCORTEX; NERVE CELL NETWORK; NERVE ENDING; PRIORITY JOURNAL; RECEPTOR UPREGULATION; TEMPORAL LOBE EPILEPSY; ANALYSIS OF VARIANCE; DRUG EFFECT; ELECTROPHYSIOLOGY; FOCAL EPILEPSY; HOMEOSTASIS; IN VITRO STUDY; METABOLISM;

4-AMINOPYRIDINE; ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; BACLOFEN; CHILD; ELECTROPHYSIOLOGY; EPILEPSIES, PARTIAL; EPILEPSY, TEMPORAL LOBE; FEMALE; GABA AGONISTS; HOMEOSTASIS; HUMANS; MALE; NEOCORTEX; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 3142547228     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awh181     Document Type: Article

References (73)

1. Aasly J, Silfvenius H, Aas TC, Sonnewald U, Olivecrona M, Juul R, et al. Proton magnetic resonance spectroscopy of brain biopsies from patients with intractable epilepsy. Epilepsy Res 1999; 35: 211-7.
2. Aronica E, Gorter JA, Jansen GH, van Veelen CW, van Rijen PC, Ramkema M, et al. Expression and cell distribution of group I and group II metabotropic glutamate receptor subtypes in Taylor-type focal cortical dysplasia. Epilepsia 2003; 44: 785-95.
3. Avoli M, Drapeau C, Louvel J, Pumain R, Olivier A, Villemure JG. Epileptiform activity induced by low extracellular magnesium in the human cortex maintained in vitro. Ann Neurol 1991; 30: 589-96.
4. Avoli M, Psarropoulou C, Tancredi V, Fueta Y, On the synchronous activity induced by 4-aminopyridine in the CA3 subfield of juvenile rat hippocampus. J Neurophysiol 1993; 70: 1018-29.
5. Avoli M, Mattia D, Siniscalchi A, Perreault P, Tomaiuolo F. Pharmacology and electrophysiology of a synchronous GABA-mediated potential in the human neocortex. Neuroscience 1994; 62: 655-66.
6. A-mediated inhibition and in vitro epileptogenesis in the human neocortex. J Neurophysiol 1995; 73: 468-84.
7. Avoli M, Barbarosie M, Lücke A, Nagao T, Lopantsev V, Köhling R. Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J Neurosci 1996a; 16: 3912-24.
8. Avoli M, Louvel J, Kurcewicz I, Pumain R, Barbarosie M. Extracellular free potassium and calcium during synchronous activity induced by 4-aminopyridine in the juvenile rat hippocampus. J Physiol 1996b; 493: 707-17.
9. Avoli M, Bernasconi A, Mattia D, Olivier A, Hwa GGC. Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology. Ann Neurol 1999; 46: 816-26.
10. Baraban SC, Schwartzkroin PA. Flurothyl seizure susceptibility in rats following prenatal methylazoxymethanol treatment. Epilepsy Res 1996; 23: 189-94.
11. Barbarosie M, Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J Neurosci 1997; 17: 9308-14.
12. Barbarosie M, Louvel J, D'Antuono M, Kurcewicz I, Avoli M. Masking synchronous GABA-mediated potentials controls limbic seizures. Epilepsia 2002; 43: 1469-79.
13. Barker JL, McBurney RN. Phenobarbitone modulation of postsynaptic GABA receptor function on cultured mammalian neurons. Proc R Soc Lond B Biol Sci 1979; 206: 319-27.
14. Benardete EA, Kriegstein AR. Increased excitability and decreased sensitivity to GABA in an animal model of dysplastic cortex. Epilepsia 2002; 43: 970-82.
15. Benardo LS. Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J Neurophysiol 1997; 77: 3134-44.
16. Bernasconi A, Antel SB, Collins DL, Bernasconi N, Olivier A, Dubeau F, et al. Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra-temporal partial epilepsy. Ann Neurol 2001; 49: 770-5.
17. Bronen RA, Vives KP, Kim JH, Fulbright RK, Spencer SS, Spencer DD. Focal cortical dysplasia of Taylor, balloon cell subtype: MR differentiation from low-grade tumors. AJNR Am J Neuroradiol 1997; 18: 1141-51.
18. Bruckner C, Stenkamp K, Meierkord H, Heinemann U. Epileptiform discharges induced by combined application of bicuculline and 4-aminopyridine are resistant to standard anticonvulsants in slices of rats. Neurosci Lett 1999; 268: 163-5.
19. 2+- and 4-aminopyridine-induced seizure-like events reveals characteristic features in adult rat limbic system. Epilepsia 2000; 41: 635-41.
20. Capogna M, Gahwiler BH, Thompson SM. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J Physiol 1993; 470: 539-58.
21. Castro PA, Cooper EC, Lowenstein DH, Baraban SC. Hippocampal heterotopia lack functional Kv4.2 potassium channels in the methylazoxymethanol model of cortical malformations and epilepsy. J Neurosci 2001; 21: 6626-34.
22. Cavalheiro EA, Silva DF, Turski WA, Calderazzo-Filho LS, Bortolotto ZA, Turski L. The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Brain Res 1987; 465: 43-58.
23. DeFazio RA, Hablitz JJ. Alterations in NMDA receptors in a rat model of cortical dysplasia. J Neurophysiol 2000; 83: 315-21.
24. Deisz R. GABA(B) receptor-mediated effects in human and rat neocortical neurones in vitro. Neuropharmacology 1999; 38: 1755-66.
25. Gabel LA, Lo Turco JJ. Layer I ectopias and increased excitability in murine neocortex. J Neurophysiol 2002; 87: 2471-9.
26. Gambardella A, Palmini A, Andermann F, Dubeau F, Da Costa JC, Quesney LF, et al. Usefulness of focal rhythmic discharges on scalp EEG of patients with focal cortical dysplasia and intractable epilepsy. Electroencephalogr Clin Neurophysiol 1996; 98: 243-9.
27. Garbelli R, Munari C, De Biasi S, Vitellaro-Zuccarello L, Galli C, Bramerio M, et al. Taylor's cortical dysplasia: a confocal and ultrastructural immuno-histochemical study. Brain Pathol 1999; 9: 445-61.
28. Guerrini R, Andermann E, Avoli M, Dobyns WB. Cortical dysplasias, genetics and epileptogenesis. In: Delgado-Escueta AV, Wilson W, Olsen RW, Porter RJ, editors. Jasper's basic mechanisms of the epilepsies. Advances in neurology, Vol. 79. New York: Lippincott-Raven; 1999. p. 95-121.
29. Hagemann G, Kluska MM, Redecker C, Luhmann HJ, Witte OW. Distribution of glutamate receptor subunits in experimentally induced cortical malformations. Neuroscience 2003; 117: 991-1002.
30. Higashima M, Kinoshita H, Yamaguchi N, Koshino Y. Activation of GABAergic function necessary for afterdischarge generation in rat hippocampal slices. Neurosci Lett 1996; 207: 101-4.
31. Jacobs KM, Gutnick MJ, Prince DA. Hyperexcitability in a model of cortical maldevelopment. Cereb Cortex 1996; 6: 514-23.
32. Kaila K. Ionic basis of GABAA receptor channel function in the nervous system. Prog Neurobiol 1994; 42: 489-537.
33. A receptor-mediated IPSPs in rat neocortical neurons. J Physiol 1993; 464: 273-89.
34. + transient. J Neurosci 1997; 17: 7662-72.
35. Köhling R, Que M, Zilles K, Speckmann EJ. Current-source density profiles associated with sharp waves in human epileptic neocortical tissue. Neuroscience 1999; 94: 1039-50,
36. A receptor-mediated oscillations. J Neurosci 2000; 20: 6820-9.
37. Lambert NA, Wilson WA. Heterogeneity in presynaptic regulation of GABA release from hippocampal inhibitory neurons. Neuron 1993; 11: 1057-67.
38. Lamsa K, Kaila K. Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. J Neurophysiol 1997; 78: 2582-91.
39. A-mediated inhibition in ictal-like discharges in the rat entorhinal cortex. J Neurophysiol 1998; 79: 352-60.
40. Louvel J, Papatheodoropoulos C, Siniscalchi A, Kurciewicz I, Pumain R, Devaux B, et al. GABA-mediated synchronization in the human cortex: elevations in extracellular potassium and presynaptic mechanisms. Neuroscience 2001; 105: 803-13.
41. Luhmann HJ, Raabe K. Characterization of neuronal migration disorders in neocortical structures: I. Expression of epilepfiform activity in an animal model. Epilepsy Res 1996; 26: 67-74.
42. Luhmann HJ, Karpuk N, Qu M, Zilles K. Characterization of neuronal migration disorders in neocortical structures. II. Intracellular in vitro recordings. J Neurophysiol 1998; 80: 92-102.
43. Madison DV, Nicoll RA. Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol 1988; 398: 123-30.
44. Mattia D, Olivier A, Avoli M. Seizure-like discharges recorded in the human dysplastic neocortex maintained in vitro. Neurology 1995; 45: 1391-5.
45. A receptors in the hippocampus. Science 1991; 253: 1420-3.
46. Misgeld U, Müller W, Brunner H. Effects of (-)baclofen on inhibitory neurons in the guinea pig hippocampal slice. Pflügers Arch 1989; 414: 139-44.
47. Moshe SL. Seizures in the developing brain. Neurology 1993; 43 (11 Suppl S): S3-7.
48. Newberry NR, Nicoll RA. Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature 1984; 308: 450-2.
49. Newberry NR, Nicoll RA. Comparison of the action of baclofen with gamma-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J Physiol 1985; 360: 161-85.
50. Nicoll RA, Eccles JC, Oshima T, Rubia F. Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature 1975; 258: 625-7.
51. Palmini A, Andermann F, Olivier A, Tampieri D, Robitaille Y, Andermann E, Wright G. Focal neuronal migration disorders and intractable partial epilepsy: a study of 30 patients. Ann Neurol 1991; 30: 741-9.
52. Palmini A, Gambardella A, Andermann F, Dubeau F, da Costa JC, Olivier A, et al. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol 1995; 37: 476-87.
53. Perreault P, Avoli M. 4-aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. J Neurosci 1992; 12: 104-15.
54. Pierau FK, Zimmermann P. Action of a GABA-derivative on postsynaptic potentials and membrane properties of cats' spinal motoneurones. Brain Res 1973; 54: 376-80.
55. Potashner SJ. Baclofen: effects on amino acid release. Can J Physiol Pharmacol 1978; 56: 150-4.
56. Purpura DP. Stability and seizure susceptibility of immature brain. In: Jasper HH, Ward AA, Pope A, editors. Basic mechanisms of the epilepsies. Boston: Little Brown; 1969. p. 481-505.
57. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999; 397: 251-5.
58. Roper SN, King MA, Abraham LA, Boillot MA. Disinhibited in vitro neocortical slices containing experimentally induced cortical dysplasia demonstrate hyperexcitability. Epilepsy Res 1997; 26: 443-9.
59. Smirnov S, Paalasmaa P, Uusisaari M, Voipio J, Kaila K. Pharmacological isolation of the synaptic and nonsynaptic components of the GABA-mediated biphasic response in rat CA1 hippocampal pyramidal cells. J Neurosci 1999; 19: 9252-60.
60. Smyth MD, Barbaro NM, Baraban SC. Effects of antiepileptic drugs on induced epileptiform activity in a rat model of dysplasia. Epilepsy Res 2002; 50: 251-64.
61. Spreafico R, Battaglia G, Arcelli P, Andermann F, Dubeau F, Palmini A, et al. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 1998; 50: 27-36.
62. A receptors. Science 1995; 269: 977-81.
63. A receptors. J Neurophysiol 1993; 70: 976-84.
64. Tassi L, Colombo N, Garbelli R, Francione S, Lo Russo G, Mai R, et al. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 2002; 125: 1719-32.
65. Tassi L, Pasquier B, Minotti L, Garbelli R, Kahane P, Benabid AL, et al. Cortical dysplasia: electroclinical, imaging, and neuropathologic study of 13 patients. Epilepsia 2001; 42: 1112-23.
66. Taylor DC, Falconer MA, Bruton CJ, Corsellis JAN. Focal dysplasia of the cerebral cortex in epilepsy. J Neurol Neurosurg Psychiatry 1971; 34: 369-87.
67. Thompson SM, Gähwiler BH. Comparison of the actions of baclofen at pre- and post-synaptic receptors in the rat hippocampus in vitro. J Physiol 1992; 451: 329-45.
68. Traub RD, Dingledine R. Model of synchronized epileptiform bursts induced by high potassium in CA3 region of rat hippocampal slice. Role of spontaneous EPSPs in initiation. J Neurophysiol 1990; 64: 1009-18.
69. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 1988; 59: 259-76.
70. Uusisaari M, Smirnov S, Voipio J, Kaila K. Spontaneous epileptiform activity mediated by GABA(A) receptors and gap juncfions in the rat hippocampal slice following long-term exposure to GABA(B) antagonists. Neuropharmacology 2002; 43: 563-72.
71. Velazquez JL, Carlen PL. Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice. Eur J Neurosci 1999; 11: 4110-8.
72. Williams S, Lacaille JC. 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 1992; 11: 249-58.
73. Zuckermann EC, Glaser GH. Hippocampal epileptic activity induced by localized ventricular perfusion with high-potassium cerebrospinal fluid. Exp Neurol 1968; 20: 87-110.