GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity

Progress in Neurobiology

Volumn 95, Issue 2, 2011, Pages 104-132

  Avoli, Massimo ^a,b   de Curtis, Marco ^c,d  

^a MCGILL UNIVERSITY   (Canada)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c DEPARTMENT OF NEUROSURGERY   (Italy)

^d ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Epileptiform synchronization; GABA; High frequency oscillations; Limbic structures

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR;

AMYGDALOID NUCLEUS; ENTORHINAL CORTEX; EPILEPTIC DISCHARGE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; INTERNEURON; LIMBIC SYSTEM; MEDICAL LITERATURE; NERVE CELL; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PERIRHINAL CORTEX; PRIORITY JOURNAL; REVIEW; SYNAPSE; TEMPORAL LOBE EPILEPSY;

ANIMALS; CORTICAL SYNCHRONIZATION; EPILEPSY; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; HUMANS; LIMBIC SYSTEM; NERVE TISSUE PROTEINS; RECEPTORS, GABA;

EID: 80052026214     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2011.07.003     Document Type: Review

References (327)

1. Aicardi J. Epilepsy in children. International Review of Child Neurology Series 1986, 413. Raven Press, New York. J. Aicardi (Ed.).
2. +-2Cl cotransport in immature rat neocortical neurons. J. Neurosci. 2007, 27:8616-8627.
3. Alakuijala A., Alakuijala J., Pasternack M. Evidence for a functional role of GABA-C receptors in the rat mature hippocampus. Eur. J. Neurosci. 2006, 23:514-520.
4. Alger B.E., Nicoll R.A. Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro. J. Physiol. 1982, 328:125-141.
5. Alonso-Nanclares L., Garbelli R., Sola R.G., Pastor J., Tassi L., Sreafico R., De Felipe J. Microanatomy of the dysplastic neocortex from epileptic patients. Brain 2005, 128:158-173.
6. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of the anatomical data. Neuroscience 1989, 31:571-591.
7. Andersen P., Andersson S.A., Lǿmo T. Patterns of spontaneous rhythmic activity within various thalamic nuclei. Nature 1966, 211:888-889.
8. Andersen P., Andersson S.A., Junge K., Loǿmo T., Sveen O.H. Physiological mechanism of the slow 10c/sec cortical rhythmic activity. Electroencephalogr. Clin. Neurophysiol. 1967, 23:394-395.
9. Andersen P., Dingledine R., Gjerstad L., Langmoen I.A., Laursen A.M. Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid. J. Physiol. 1980, 305:279-296.
10. Ang C.W., Carlson G.C., Coulter D.A. Massive and specific dysregulation of direct cortical input to the hippocampus in temporal lobe epilepsy. J. Neurosci. 2006, 26:11850-11856.
11. Aram J.A., Michaelson H.B., Wong R.K.S. Synchronized GABAergic IPSPs recorded in the neocortex after blockade of synaptic transmission mediated by excitatory amino acids. J. Neurophysiol. 1991, 65:1034-1041.
12. 2+ in adult hippocampal slices. J. Neurophysiol. 1999, 81:811-815.
13. Avoli M. Epileptiform discharges and a synchronous GABAergic potential induced by 4-aminopyridine in the rat immature hippocampus. Neurosci. Lett. 1990, 117:93-98.
14. Avoli M. GABA-mediated synchronous potentials and seizure generation. Epilepsia 1996, 37:1035-1042.
15. Avoli M., Perreault P. A GABAergic depolarizing potential in the hippocampus disclosed by the convulsant 4-aminopyridine. Brain Res. 1987, 400:191-195.
16. Avoli M., Olivier A. Electrophysiological properties and synaptic responses in the deep layers of the human epileptogenic neocortex in vitro. J. Neurophysiol. 1989, 61:589-606.
17. Avoli M., Drapeau C., Perreault P., Louvel J., Pumain R. Epileptiform activity induced by low chloride medium in the CA1 subfield of the hippocampal slice. J. Neurophysiol. 1990, 64:1747-1757.
18. 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, 62:655-666.
19. 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, 70:1018-1029.
20. A-mediated inhibition and in vitro epileptogenesis in the human neocortex. J. Neurophysiol. 1995, 73:468-484.
21. Avoli M., Barbarosie M., Lucke A., Nagao T., Lopantsev V., Kohling R. Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J. Neurosci. 1996, 16:3912-3924.
22. Avoli M., Louvel J., Kurcewicz I., Pumain R., Barbarosie M. Extracellular free potassium and calcium during synchronous activity induced by 4-aminopyridine in the immature rat hippocampus. J. Physiol. 1996, 493:707-717.
23. Avoli M., Nagao T., Köhling R., Lücke A., Mattia D. Synchronization of rat hippocampal neurons in the absence of excitatory amino acid-mediated transmission. Brain Res. 1996, 735:188-196.
24. Avoli M., Methot M., Kawasaki H. GABA-dependent generation of ectopic action potentials in the rat hippocampus. Eur. J. Neurosci. 1998, 10:2714-2722.
25. Avoli M., Bernasconi A., Mattia D., Olivier A., Hwa G.G. Epileptiform discharges in the human dysplastic neocortex: in vitro physiology and pharmacology. Ann. Neurol. 1999, 46:816-826.
26. Avoli M., D'Antuono M., Louvel J., Kohling R., Biagini G., Pumain R., D'Arcangelo G., Tancredi V. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system. Progr. Neurobiol. 2002, 68:167-207.
27. Ayala G.F., Dichter M., Gumnit R.J., Matsumoto H., Spencer W.A. Genesis of epileptic interictal spikes. New knowledge of cortical feedback systems suggests a neurophysiological explanation of brief paroxysms. Brain Res. 1973, 52:1-17.
28. Babb T.L., Pretorius J.K., Kupfer W.R., Crandall P.H. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci. 1989, 9:2562-2574.
29. A, slow. J. Neurosci. 1998, 18:1305-1317.
30. Barbarosie M., Avoli M. CA3-driven hippocampal-entorhinal loop controls rather than sustain in vitro limbic seizures. J. Neurosci. 1997, 17:9308-9314.
31. Barbarosie M., Louvel J., Kurcewicz I., Avoli M. CA3-Released entorhinal seizures disclose dentate gyrus epileptogenicity and unmask a temporoammonic pathway. J. Neurophysiol. 2000, 83:1115-1124.
32. Barbarosie M., Louvel J., D'Antuono M., Kurcewicz I., Avoli M. Masking synchronous GABA-mediated potentials controls limbic seizures. Epilepsia 2002, 43:1469-1479.
33. + evoked by GABA, THIP and baclofen in the guinea-pig hippocampal slice. Exp. Brain Res. 1991, 84:591-598.
34. Bartos M., Vida I., Frotscher M., Geiger J.R., Jonas P. Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J. Neurosci. 2001, 21:2687-2698.
35. Bartos M., Vida I., Frotscher M., Meyer A., Monyer H., Geiger J.R., Jonas P. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13222-13227.
36. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007, 8:45-56.
37. Basar E., Basar-Eroglu C., Karakas S., Schürmann M. Oscillatory brain theory: a new trend in neuroscience. IEEE Eng. Med. Biol. Mag. 1999, 18:56-66.
38. Basemore A., Elliott K.A., Florey E. Factor I and gamma-aminobutyric acid. Nature 1956, 178:1052-1053.
39. Bazelot M., Dinocourt C., Cohen I., Miles R. Unitary inhibitory field potentials in the CA3 region of rat hippocampus. J. Physiol. 2010, 588:2077-2090.
40. Bekenstein J.W., Lothman E.W. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 1993, 259:97-100.
41. Benardo L.S. Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J. Neurophysiol. 1997, 77:3134-3144.
42. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
43. Ben-Ari Y., Cherubini E., Corradetti R., Gaiarsa J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 1989, 416:303-325.
44. Ben-Ari Y., Gaiarsa J.L., Tyzio R., Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 2007, 87:1215-1284.
45. Benassi P., Bertolotti P. Experimental research on the anticonvulsant properties of 1-glutamine, 1-asparagine, gamma-aminobutyric acid and gamma-amino-beta-hydroxybutyric acid. Riv. Sper. Freniatr. Med. Leg. Alien. Ment. 1962, 86:342-354.
46. Benini R., D'Antuono M., Pralong E., Avoli M. Involvement of amygdala networks in epileptiform synchronization in vitro. Neuroscience 2003, 120:75-84.
47. Benini R., Avoli M. Rat subicular networks gate hippocampal output activity in an in vitro model of limbic seizures. J. Physiol. 2005, 566:885-900.
48. Benini R., Longo D., Biagini G., Avoli M. Perirhinal cortex hyperexcitability in pilocarpine-treated epileptic rats. Hippocampus 2011, 21:702-713.
49. Bernard C., Cossart R., Hirsch J.C., Esclapez M., Ben-Ari Y. What is GABAergic inhibition? How is it modified in epilepsy?. Epilepsia 2000, 41(Suppl. 6):S90-S95.
50. Biagini G., Panuccio G., Avoli M. Neurosteroids and epilepsy. Curr. Opin. Neurol. 2010, 23:170-176.
51. Biella G., Uva L., Hoffman U., de Curtis M. Associative potentials in the entorhinal cortex of the guinea pig. J. Neurophysiol. 2002, 88:1159-1165.
52. Biella G., Gnatkovsky V., de Curtis M. Olfactory projections to the parahippocampal region of the isolated guinea pig brain. Eur. J. Neurosci. 2003, 18:95-101.
53. Biella G., Toselli M., de Curtis M., Gnatkovsky V. Functional perirhinal-postrhinal-entorhinal connections revealed by voltage sensitive dye imaging in the isolated guinea pig brain. J. Neurophysiol. 2010, 103:725-732.
54. Blaesse P., Airaksinen M.S., Rivera C., Kaila K. Cation-chloride cotransporters and neuronal function. Neuron 2009, 61:820-838.
55. Bormann J. The 'ABC' of GABA receptors. Trends Pharmacol. Sci. 2000, 21:16-19.
56. Boue-Grabot E., Roudbaraki M., Bascles L., Tramu G., Bloch B., Garret M. Expression of GABA receptor rho subunits in rat brain. J. Neurochem. 1998, 70:899-907.
57. Bracci E., Vreugdenhil M., Hack S.P., Jefferys J.G. On the synchronizing mechanisms of tetanically induced hippocampal oscillations. J. Neurosci. 1999, 19:8104-8113.
58. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15:47-60.
59. Bragin A., Engel J., Wison C.L. Hippocampal and entorhinal cortex high-frequency oscillations in human epileptic brain and kainic acid treated rats. Epilepsia 1999, 40:127-137.
60. Bragin A., Mody I., Wilson C.L., Engel J. Local generation of fast ripples in epileptic brain. J. Neurosci. 2002, 22:2012-2021.
61. Bragin A., Benassi S.K., Kheiri F., Engel J.J.R. Further evidence that pathologic high-frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia 2011, 52:45-52.
62. A receptor subunit expression and function in temporal lobe epilepsy. Nat. Med. 1998, 4:1166-1172.
63. Buckle P.J., Haas H.L. Enhancement of synaptic transmission by 4-aminopyridine in hippocampal slices of the rat. J. Physiol. 1982, 326:109-122.
64. Buhl E.H., Otis T.S., Mody I. Zinc-induced collapse of augmented GABAergic inhibition by GABA in a temporal lobe epilepsy model. Science 1996, 271:369-373.
65. A receptor subtypes: from pharmacology to molecular biology. FASEB J. 1991, 5:2916-2923.
66. Buzsáki G., Horváth Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science 1992, 256:1025-1027.
67. Capogna M., Gahwiller B.H., Thompson S.M. Mechanism of μ-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J. Physiol. 1993, 470:539-558.
68. Carriero G., Uva L., Gnatkovsky V., Avoli M., de Curtis M. Independent epileptiform discharge patterns in the olfactory and limbic areas of the in vitro isolated guinea pig brain during 4-aminopyridine treatment. J. Neurophysiol. 2010, 103:2728-2736.
69. Cavalheiro E.A., Leite J.P., Bortolotto Z.A., Turski W.A., Ikonomidou C., Turski L. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 1991, 32:778-782.
70. Chatrian G.E., Bergamini L., Dondey M., Klass D.W., Lennox-Buchthal M., Petersen I. A glossary of terms most commonly used by clinical electroencephalographers. Electroenceph. Clin. Neurophysiol. 1974, 37:538-548.
71. Cherubini E., Gaiarsa J.L., Ben-Ari Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 1991, 14:515-519.
72. Chrobak J.J., Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 1998, 18:388-398.
73. Cohen I., Navarro V., Clemenceau S., Baulac M., Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 2002, 298:1418-1421.
74. Compte A., Reig R., Descalzo V.F., Harvey M.A., Puccini G.D., Sanchez-Vives M.V. Spontaneous high-frequency (10-80Hz) oscillations during up states in the cerebral cortex in vitro. J. Neurosci. 2008, 28:13828-13844.
75. A receptor-mediated tonic inhibition in thalamic neurons. J. Neurosci. 2005, 25:11553-11563.
76. Coursin D.B. Convulsive seizures in infants with pyridoxine-deficient diet. J. Am. Med. Assoc. 1954, 154:406-408.
77. Cossart R., Dinocourt C., Hirsch J.C., Merchan-Perez A., De Felipe J., Ben-Ari Y., Esclapez M., Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat. Neurosci. 2001, 4:52-62.
78. Cossart R., Bernard C., Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies. Trends Neurosci. 2005, 28:108-115.
79. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 1999, 19:274-287.
80. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
81. Curia G., Longo D., Biagini G., Jones R.S., Avoli M. The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 2008, 172:143-157.
82. D'Antuono M., Benini R., Biagini G., D'Arcangelo G., Barbarosie M., Tancredi V., Avoli M. Limbic network interactions leading to hyperexcitability in temporal lobe epilepsy. J. Neurophysiol. 2002, 87:634-639.
83. A receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 2004, 127:1626-1640.
84. D'Antuono M., de Guzman P., Kano T., Avoli M. Ripple activity in the dentate gyrus of disinhibited hippocampus-entorhinal cortex slices. J. Neurosci. Res. 2005, 80:92-103.
85. D'Arcangelo G., Panuccio G., Tancredi V., Avoli M. Repetitive low-frequency repetitive stimulation reduces epileptiform synchronization in limbic neuronal networks. Neurobiol. Dis. 2005, 19:119-128.
86. Davenport C.J., Brown W.J., Babb T.L. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 1990, 109:180-190.
87. de Curtis M., Biella G., Forti M., Panzica F. Multifocal spontaneous epileptic activity induced by restricted convulsing ejection in the piriform cortex of the isolated guinea pig brain. J. Neurophysiol. 1994, 71:2463-2476.
88. de Curtis M., Avanzini G. Interictal spikes in focal epileptogenesis. Progr. Neurobiol. 2001, 63:541-567.
89. de Curtis M., Gnatkovsky V. Reevaluating the mechanisms of focal ictogenesis: the role of low-voltage fast activity. Epilepsia 2009, 50:2514-2525.
90. de Curtis M., Paré D. The parahippocampal cortex: a wall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 2004, 74:101-110.
91. de Curtis M., Biella G., Buccellati C., Folco G. Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res. Protocol. 1998, 3:221-228.
92. de Curtis M., Gnatkovsky V. Re-considering the mechanisms of focal ictogenesis: the role of low-voltage fast activity. Epilepsia 2009, 50:2514-2525.
93. de Guzman P., D'Antuono M., Avoli M. Initiation of electrographic seizures by neuronal networks in entorhinal and perirhinal cortices in vitro. Neuroscience 2004, 123:875-886.
94. de Guzman P., Inaba Y., Baldelli E., de Curtis M., Biagini G., Avoli M. Network hyperexcitability within the deep layers of the pilocarpine-treated rat entorhinal cortex. J. Physiol. 2008, 586:1867-1883.
95. de Guzman P., Inaba Y., Biagini G., Baldelli E., Mollinari C., Merlo D., Avoli M. Subiculum network excitability is increased in a rodent model of temporal lobe epilepsy. Hippocampus 2006, 16:843-860.
96. Derchansky M., Jahromi S.S., Mamani M., Shin D.S., Sik A., Carlen P.L. Transition to seizures in the isolated immature mouse hippocampus: a switch from dominant phasic inhibition to dominant phasic excitation. J. Physiol. 2008, 586:477-494.
97. Dichter M., Spencer W.A. Penicillin-induced interictal discharges from the cat hippocampus. I. Characteristics and topographical features. J. Neurophysiol. 1969, 32:649-662.
98. Dickson C.T., Alonso A. Muscarinic induction of synchronous population activity in the entorhinal cortex. J. Neurosci. 1997, 17:6729-6744.
99. Dickson C.T., Biella G., de Curtis M. Evidence for spatial modules mediated by temporal synchronization of carbachol-induced gamma rhythm in medial entorhinal cortex. J. Neurosci. 2000, 20:7846-7854.
100. Dickson C.T., Biella G., de Curtis M. Slow periodic events and their transition to fast gamma oscillations in the entorhinal cortex of the isolated guinea-pig brain. J. Neurophysiol. 2003, 90:39-46.
101. Dodgson S.J., Shank R.P., Maryanoff B.E. Topiramate as an inhibitor of carbonic anhydrase isoenzymes. Epilepsia 2000, 41(Suppl. 1):S35-S39.
102. Doherty J., Dingledine R. Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus. J. Neurosci. 2001, 21:2048-2057.
103. Draguhn A., Axmacher N., Kolbaev S. Presynaptic ionotropic GABA receptors. Results Probl. Cell Differ. 2008, 44:69-85.
104. 2+ induced epileptiform activityin rat temporal cortex slices. Exp. Brain Res. 1991, 87:581-596.
105. Du F., Eid T., Lothman E.W., Kohler C., Schwarcz R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci. 1995, 15:6301-6313.
106. Du F., Whetsell W.O., Abou-Khalil B., Blumenkopf B., Lothman E.W., Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res. 1993, 16:223-233.
107. Dzhala V.I., Staley K.J. Mechanisms of fast ripples in the hippocampus. J. Neurosci. 2004, 24:8896-8906.
108. Dzhala V.I., Talos D.M., Sdrulla D.A., Brumback A.C., Mathews G.C., Benke T.A., Delpire E., Jensen F.E., Staley K.J. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 2005, 11:1205-1213.
109. Dzhala V.I., Kuchibhotla K.V., Glykys J.C., Kahle K.T., Swiercz W.B., Feng G., Kuner T., Augustine G.J., Bacskai B.J., Staley K.J. Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J. Neurosci. 2010, 30:11745-11761.
110. Engel J.J.R., Bragin A., Staba R., Mody I. High-frequency oscillations: what is normal and what is not?. Epilepsia 2009, 50:598-604.
111. Enz R., Brandstätter J.H., Hartveit E., Wässle H., Bormann J. Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur. J. Neurosci. 1995, 7:1495-1501.
112. Esclapez M., Hirsch J.C., Khazipov R., Ben-Ari Y., Bernard C. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:12151-12156.
113. Farrant M., Kaila K. The cellular, molecular and ionic basis of GABA(A) receptor signaling. Prog. Brain Res. 2007, 160:59-87.
114. A receptors. Nat. Rev. Neurosci. 2005, 6:215-229.
115. Fisahn A., Pike F.G., Buhl E.H., Paulsen O. Cholinergic induction of network oscillations at 40Hz in the hippocampus in vitro. Nature 1998, 394:186-189.
116. Florey E., McLennan H. Effects of an inhibitory factor (factor I) from brain on central synaptic transmission. J. Physiol. 1955, 130:446-455.
117. Foffani G., Uzcategui Y.G., Gal B., Menendez de la Prida L. Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 2007, 55:930-941.
118. Forti M., Biella G., Caccia S., de Curtis M. Persistent excitability changes in the piriform cortex of the isolated guinea-pig brain after transient exposure to bicuculline. Eur. J. Neurosci. 1997, 9:435-451.
119. A/benzodiazepine receptors in acutely isolated hippocampal astrocytes. J. Neurosci. 1995, 15:2720-2732.
120. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
121. Frick A., Johnston D. Plasticity of dendritic excitability. J. Neurobiol. 2005, 64:100-115.
122. Fritschy J.M., Kiener T., Bouilleret V., Loup F. GABAergic neurons and GABA(A)-receptors in temporal lobe epilepsy. Neurochem. Int. 1999, 34:435-445.
123. Fujiwara-Tsukamoto Y., Isomura Y., Kaneda K., Takada M. Synaptic interactions between pyramidal cells and interneurone subtypes during seizure-like activity in the rat hippocampus. J. Physiol. 2004, 557:961-979.
124. 2+ conditions. J. Neurophysiol. 2006, 95:2013-2019.
125. Fujiwara-Tsukamoto Y., Isomura Y., Imanishi M., Fukai T., Takada M. Distinct types of ionic modulation of GABA actions in pyramidal cells and interneurons during electrical induction of hippocampal seizurelike network activity. Eur. J. Neurosci. 2007, 25:2713-2725.
126. Galarreta M., Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 1999, 402:72-75.
127. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999, 402:75-79.
128. Gibson J.R., Beierlein M., Connors B.W. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J. Neurophysiol. 2004, 93:467-480.
129. Gigout S., Louvel J., Kawasaki H., D'Antuono M., Armand V., Kurcewicz I., Olivier A., Laschet J., Turak B., Devaux B., Pumain R., Avoli M. Role of gap junctions in human neocortical network synchronization. Neurobiol. Dis. 2006, 22:496-508.
130. Gilbert P., Kettenmann H., Schachner M. γ-Aminobutyric acid directly depolarizes cultured oligodendrocytes. J. Neurosci. 1984, 4:561-569.
131. Girardeau G., Benchenane K., Wiener S.I., Buzsáki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009, 12:1222-1223.
132. Gloor P. Mesial temporal sclerosis: historical background and an overview from a modern perspective. Epilepsy Surgery 1991, 689-703. Raven Press, New York. H. Lüders (Ed.).
133. Gloor P. The Temporal Lobe and Limbic System 1997, Oxford University Press, New York.
134. 2+ induced epileptiform activity in rat hippocampal and entorhinal cortex slices during adolescence. Dev. Brain Res. 1995, 87:145-152.
135. A receptor subunits are necessary for tonic inhibition in the hippocampus?. J. Neurosci. 2008, 28:1421-1426.
136. Gnatkovsky V., Wendling F., de Curtis M. Spontaneous periodic oscillatory events are generated by superficial neurons in medial entorhinal cortex of the isolated guinea pig brain. Eur. J. Neurosci. 2007, 26:302-311.
137. Gnatkowsky V., Librizzi L., Trombin F., de Curtis M. Fast activity at seizure onset is mediated by inhibitory networks in the entorhinal cortex in vitro. Ann. Neurol. 2008, 64:674-686.
138. Gorter J.A., van Vliet E.A., Aronica E., Lopes da Silva F.H. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur. J. Neurosci. 2001, 13:657-669.
139. Gray C.M., König P., Engel A.K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 1989, 338:334-337.
140. A receptor-mediated responses in pyramidal cells of rat hippocampus. J. Neurophysiol. 1993, 69:1541-1555.
141. Gulledge A.T., Stuart G.J. Excitatory actions of GABA in the cortex. Neuron 2003, 37:299-309.
142. Gulyás A.I., Hájos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 1996, 16:3397-3411.
143. Gutnick M.J., Connors B.W., Prince D.A. Mechanisms of neocortical epileptogenesis in vitro. J. Neurophysiol. 1982, 48:1321-1335.
144. Gutnick M.J., Prince D.A. Thalamocortical relay neurons: antidromic invasion of spikes from a cortical epileptogenic focus. Science 1972, 176:424-426.
145. Hawkins J.E., Sarett L.H. On the efficacy of asparagine, glutamine, gamma-aminobutyric acid and 1-pyrroiidinone in preventing chemically induced seizures in mice. Clin. Chim. Acta 1957, 2:481-484.
146. Hayashi T. Neurophysiology and Neurochemistry of Convulsion 1959, Dainihon-Tosho Co., Tokyo, p. 222.
147. Hájos N., Pálhalmi J., Mann E.O., Németh B., Paulsen O., Freund T.F. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J. Neurosci. 2004, 24:9127-9137.
148. Heinemann U., Lux H.D., Gutnick M.J. Extracellular free calcium and potassium during paroxsmal activity in the cerebral cortex of the cat. Exp. Brain Res. 1977, 27:237-243.
149. Herrero A.I., Del Olmo N., González-Escalada J.R., Solís J.M. Two new actions of topiramate: inhibition of depolarizing GABA(A)-mediated responses and activation of a potassium conductance. Neuropharmacology 2002, 42:210-220.
150. Higashima M., Kinoshita H., Yamaguchi N., Koshino Y. Activation of GABAergic function necessary for afterdischarge generation in rat hippocampal slices. Neurosci. Lett. 1996, 207:101-104.
151. Houser C.R. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv. Neurol. 1999, 79:743-761.
152. Houser C.R., Escaplez M. Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res. 1996, 26:207-218.
153. Huberfeld G., Wittner L., Clemenceau S., Baulac M., Kaila K., Miles R., Rivera C. Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J. Neurosci. 2007, 27:9866-9873.
154. Huberfeld G., Menendez de la Prida L., Pallud J., Cohen I., Le Van Quyen M., Adam C., Clemenceau S., Baulac M., Miles R. Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy. Nat. Neurosci. 2011, 14:627-634.
155. Ibarz J.M., Foffani G., Cid E., Inostroza M., Menendez de la Prida L. Emergent dynamics of fast ripples in the epileptic hippocampus. J. Neurosci. 2010, 30:16249-16261.
156. Iijima T., Witter M.P., Ichikawa M., Tominaga T., Kajiwara R., Matsumoto G. Entorhinal-hippocampal interactions revealed by real-time imaging. Science 1996, 272:1176-1179.
157. Isokawa-Akesson M., Wilson C.L., Babb T.L. Inhibition in synchronously firing human hippocampal neurons. Epilepsy Res. 1989, 3:236-247.
158. A receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. 2008, 9:331-343.
159. Jefferys J.G.R. Basic mechanism of focal epilepsies. Exp. Physiol. 1990, 75:127-162.
160. Jia F., Yue M., Chandra D., Keramidas A., Goldstein P.A., Homanics G.E., Harrison N.L. Taurine is a potent activator of extrasynaptic GABA(A) receptors in the thalamus. J. Neurosci. 2008, 28:106-115.
161. Jirsch J.D., Urrestarazu E., LeVan P., Olivier A., Dubeau F., Gotman J. High-frequency oscillations during human focal seizures. Brain 2006, 129:1593-1608.
162. Johnston D., Brown T.H. Giant synaptic potential hypothesis for epileptiform activity. Science 1981, 16:294-297.
163. Johnston D., Hoffman D.A., Colbert C.M., Magee J.C. Regulation of back-propagating action potentials in hippocampal neurons. Curr. Opin. Neurobiol. 1999, 9:288-292.
164. Jones R.S., Lambert J.D.C. Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors. Neuroscience 1990, 34:657-670.
165. Jones R.S., Lambert J.D.C. The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyrus in vitro. Exp. Brain Res. 1990, 80:310-322.
166. Kahle K.T., Barnett S.M., Sassower K.C., Staley K.J. Decreased seizure activity in a human neonate treated with bumetanide, an inhibitor of the Na(+)-K(+)-2Cl(-) cotransporter NKCC1. J. Child Neurol. 2009, 24:572-576.
167. A receptor-mediated IPSPs of rat neocortical neurons. J. Physiol. 1993, 464:273-289.
168. Kaila K. Ionic basis of GABAA receptor channel function in the nervous system. Prog. Neurobiol. 1994, 42:489-537.
169. + transient. J. Neurosci. 1997, 17:7662-7767.
170. Khalilov I., Khazipov R., Esclapez M., Ben-Ari Y. Bicuculline induces ictal seizures in the intact hippocampus recorded in vitro. Eur. J. Pharmacol. 1997, 319:R5-R6.
171. Kamphuis W., DeRijk T.C., lopes Da Silva F.H. GABA-A receptor β1-3 subunit gene expression in the hippocampus of kindled rats. Neurosci. Lett. 1994, 174:5-8.
172. A receptor subunit mRNAs in hippocampal pyramidal and granular neurons in the kindling model of epileptogenesis: an in situ hybridization study. Mol. Brain Res. 1995, 31:33-47.
173. Kilb W., Sinning A., Luhmann H.J. Model-specific effects of bumetanide on epileptiform activity in the in-vitro intact hippocampus of the newborn mouse. Neuropharmacology 2007, 53:524-533.
174. Klaassen A., Glykys J., Maguire J., Labarca C., Mody I., Boulter J. Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19152-19157.
175. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
176. Knopp A., Frahm C., Fidzinski P., Witte O.W., Behr J. Loss of GABAergic neurons in the subiculum and its functional implications in temporal lobe epilepsy. Brain 2008, 131:1516-1527.
177. Köhling R., Lucke A., Straub H., Speckmann E.J., Tuxhorn I., Wolf P., Pannek H., Oppel F. Spontaneous sharp waves in human neocortical slices excised from epileptic patients. Brain 1998, 121:1073-1087.
178. A receptor-mediated oscillations. J. Neurosci. 2000, 20:6820-6829.
179. Krnjevic K. GABA-mediated inhibitory mechanisms in relation to epileptic discharge. Basic Mechanisms of Neuronal Hyperexcitability 1983, 249-280. Liss, New York. H.H. Jasper, N.M. van Gelder (Eds.).
180. + activity accompanying hippocampal discharges. Can. J. Physiol. Pharmacol. 1980, 58:570-583.
181. Krnjevic K., Schwartz S. Some properties of unresponsive cells in the cerebral cortex. Exp. Brain Res. 1967, 3:306-319.
182. Kumar S.S., Buckmaster P.S. Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J. Neurosci. 2006, 26:4613-4623.
183. Labyt E., Uva L., de Curtis M., Wendling F. Realistic modeling of entorhinal cortex field potentials and interpretation of epileptic activity in the guinea-pig isolated brain preparation. J. Neurophysiol. 2006, 97:363-377.
184. Lacaille J.C. Postsynaptic potentials mediated by excitatory and inhibitory amino acids in interneurons of stratum pyramidale of the CA1 region of rat hippocampal slices in vitro. J. Neurophysiol. 1991, 66:1441-1454.
185. Lacaille J.C., Williams S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 1990, 36:349-359.
186. A receptors. Psychoneuroendocrinology 2009, 34(Suppl. 1):S48-S58.
187. Lamsa K., Kaila K. Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. J. Neurophysiol. 1997, 78:2582-2591.
188. Lasztocki B., Nyitrai G., Heja L., Kardos J. Synchronization of GABAergic inputs to CA3 principal cells precedes seizure-like even onset in juvenile rat hippocampal slices. J. Neurophysiol. 2009, 102:2538-2553.
189. Laschet J.J., Kurcewicz I., Minier F., Trottier S., Khallou-Laschet J., Louvel J., Gigout S., Turak B., Biraben A., Scarabin J.M., Devaux B., Chauvel P., Pumain R. Dysfunction of GABAA receptor glycolysis-dependent modulation in human partial epilepsy. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3472-3477.
190. Lee S., Yoon B.E., Berglund K., Oh S.J., Park H., Shin H.S., Augustine G.J., Lee C.J. Channel-mediated tonic GABA release from glia. Science 2010, 330:790-796.
191. Le Van Quyen M., Bragin A., Staba R., Crepon B., Wilson C.L., Engel J. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J. Neurosci. 2008, 28:6104-6110.
192. - co-transporter 2 (KCC2) in CA1 region of hippocampus following lithium-pilocarpine induced status epilepticus (PISE). Brain Res. 2008, 1221:141-146.
193. Librizzi L., de Curtis M. Epileptiform ictal discharges are prevented by periodic interictal spiking activity in the guinea-pig olfactory-limbic cortex. Ann. Neurol. 2003, 53:382-389.
194. Llinás R., Urbano F.J., Leznik E., Ramírez R.R., van Marle H.J. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 2005, 28:325-333.
195. A-mediated inhibition in ictal-like discharges in the rat entorhinal cortex. J. Neurophysiol. 1998, 79:352-360.
196. Lopantsev V., Avoli M. Laminar organization of epileptiform discharges in the rat entorhinal cortex in vitro. J. Physiol. 1998, 509:785-796.
197. Louvel J., Papatheodoropoulos C., Siniscalchi A., Kurciewicz I., Pumain R., Devaux B., Turak B., Chodkiewicz J.P., Esposito V., Villemeure J.G., Avoli M. GABA-Mediated synchronization in the human cortex: elevations in extracellular potassium and presynaptic mechanisms. Neuroscience 2001, 105:803-813.
198. Lu Y., Zheng J., Xiong L., Zimmermann M., Yang J. Spinal cord injury-induced attenuation of GABAergic inhibition in spinal dorsal horn circuits is associated with down-regulation of the chloride transporter KCC2 in rat. J. Physiol. 2008, 586:5701-5715.
199. Luhmann H.J., Dzhala V.I., Ben-Ari Y. Generation and propagation of 4-AP-induced epileptiform activity in neonatal intact limbic structures in vitro. Eur. J. Neurosci. 2000, 12:2757-2768.
200. Lux H.D., Heinemann U., Dietzel I. Ionic changes and alterations in the size of the extracellular space during epileptic activity. Adv. Neurol. 1986, 44:619-639.
201. Maccaferri G., Lacaille J.C. Interneuron diversity series: hippocampal interneuron classifications-making things as simple as possible, not simpler. Trends Neurosci. 2003, 26. 564-271.
202. A receptor channels. Annu. Rev. Neurosci. 1994, 17:569-602.
203. - channels in astrocytes of hippocampal slices. J. Neurosci. 1989, 9:3577-3583.
204. Madison D.V., Nicoll R.A. Enkephalin hyperpolarizes interneurons in the rat hippocampus. J. Physiol. 1988, 398:123-130.
205. Maglóczky Z., Freund T.F. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci. 2005, 28:334-340.
206. Mancilla J.G., Lewis T.J., Pinto D.J., Rinzel J., Connors B.W. Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J. Neurosci. 2007, 27:2058-2073.
207. Mann E.O., Paulsen O. Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 2007, 30:343-349.
208. Mann E.O., Mody I. The multifaceted role of inhibition in epilepsy: seizure-genesis through excessive GABAergic inhibition in autosomal dominant nocturnal frontal lobe epilepsy. Curr. Opin. Neurol. 2008, 21:155-160.
209. Martin D.L., Olsen R.W. GABA in the Nervous System: The View at Fifty Years 2000, Lippincott, Williams & Wilkins, Philadelphia.
210. Martina M., Royer S., Pare D. Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdale. J. Neurophysiol. 2001, 86:2887-2895.
211. Matsumoto H., Ajmone-Marsan C. Cortical cellular phenomena in experimental epilepsy: interictal manifestations. Exp. Neurol. 1964, 9:286-304.
212. A receptors in the hippocampus. Science 1991, 253:1420-1423.
213. Michelson H.B., Wong R.K.S. Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J. Physiol. 1994, 477:35-45.
214. Mihalek R.M., Banerjee P.K., Korpi E.R., Quinlan J.J., Firestone L.L., Mi Z.P., Lagenaur C., Tretter V., Sieghart W., Anagnostaras S.G., Sage J.R., Fanselow M.S., Guidotti A., Spigelman I., Li Z., DeLorey T.M., Olsen R.W., Homanics G.E. Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:12905-12910.
215. Miles R., Wong R.K. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 1983, 306:371-373.
216. Miles R., Wong R.K. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J. Physiol. 1987, 388:611-629.
217. Misgeld U., Deisz R.A., Dodt H.U., Lux H.D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 1986, 232:1413-1415.
218. Molony C.J., Parmelee A.H. Convulsions in young infats as the result of pyridoxine (vitamin B6) deficiency. J. Am. Med. Assoc. 1954, 154:405-406.
219. Montgomery S.M., Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl. Acad. Sci. (U.S.A.) 2007, 104:14495-14500.
220. + accumulations and synchronous GABA-mediated potentials evoked by 4-aminopyridine in the adult rat hippocampus. Exp. Brain Res. 1996, 109:71-82.
221. Munakata M., Watanabe M., Otsuki T., Nakama H., Arima K., Itoh M., Nabekura J., Iinuma K., Tsuchiya S. Altered distribution of KCC2 in cortical dysplasia in patients with intractable epilepsy. Epilepsia 2007, 48:837-844.
222. Munoz A., Mendez P., DeFelipe J., Alvarez-Leefmans F.J. Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 2007, 48:663-673.
223. Murthy V.N., Fetz E.E. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc. Natl. Acad. Sci., U.S.A. 1992, 89:5670-5674.
224. Nagao T., Alonso A., Avoli M. Epileptiform activity induced by pilocarpine in the rat hippocampal-entorhinal slice preparation. Neuroscience 1996, 72:399-408.
225. Nardou R., Ben-Ari Y., Khalilov I. Bumetanide, an NKCC1 antagonist, does not prevent formation of epileptogenic focus but blocks epileptic focus seizures in immature rat hippocampus. J. Neurophysiol. 2009, 101:2878-2888.
226. Nusser Z., Sieghart W., Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 1998, 18:1693-1703.
227. Obenaus A., Esclapez M., Houser C.R. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J. Neurosci. 1993, 13:4470-4485.
228. Oláh S., Füle M., Komlósi G., Varga C., Báldi R., Barzó P., Tamás G. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 2009, 461:1278-1281.
229. Olsen R.W., Macdonald R.L. GABAA receptor complex: structure and function. Glutamate and GABA Receptors and Transporters: Structure, Function and Pharmacology 2002, 202-219. Taylor & Francis, London. J. Egeberg, A. Schousboe, P. Krogsgaard-Larsen (Eds.).
230. a receptors: classification on the basis of subunit composition, pharmacology, and function update. Pharmacol. Rev. 2008, 60:243-260.
231. Olsen R.W., Chang C.S., Li G., Hanchar H.J., Wallner M. Fishing for allosteric sites on GABA(A) receptors. Biochem. Pharmacol. 2004, 68:1675-1684.
232. Otis T.S., De Koninck Y., Mody I. Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors activated during miniature inhibitory postsynaptic currents. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:7698-7702.
233. Panuccio G., Curia G., Colosimo A., Cruccu G., Avoli M. Epileptiform synchronization in the cingulate cortex. Epilepsia 2009, 50:521-536.
234. Panuccio G., D'Antuono M., de Guzman P., De Lannoy L., Biagini G., Avoli M. In vitro ictogenesis and parahippocampal networks in a rodent model of temporal lobe epilepsy. Neurobiol. Dis. 2010, 39:372-380.
235. A responses in rat hippocampus. Neuron 1993, 10:189-200.
236. Pelletier J.G., Apergis J., Parè D. Low-probability transmission of neocortical and entorhinal impulses through the perirhinal cortex. J. Neurophysiol. 2004, 91:2079-2089.
237. Perez Velazquez J.L., Carlen P.L. Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice. Eur. J. Neurosci. 1999, 11:1-10.
238. Perreault P., Avoli M. Effects of low concentrations of 4-aminopyridine on CA1 pyramidal cells of the hippocampus. J. Neurophysiol. 1989, 61:953-970.
239. Perreault P., Avoli M. Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J. Neurophysiol. 1991, 65:771-785.
240. Perreault P., Avoli M. 4-aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. J. Neurosci. 1992, 12:104-115.
241. Price T.J., Cervero F., de Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr. Top. Med. Chem. 2005, 5:547-555.
242. Prince D.A. The depolarization shift in " epileptic" neurons. Exp. Neurol. 1968, 21:467-485.
243. Prince D.A., Jacobs K. Inhibitory function in two models of chronic epileptogenesis. Epilepsy Res. 1998, 32:83-92.
244. Psarropoulou C., Avoli M. 4-Aminopyridine-induced spreading depression episodes in immature hippocampus: developmental and pharmacological characteristics. Neuroscience 1993, 55:57-68.
245. Ribak C.E., Vaughn J.E., Saito K. Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res. 1978, 140:315-332.
246. Ribak C.E., Bradburne R.M., Harris A.B. A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastructural analysis of monkey neocortex. J. Neurosci. 1982, 2:1725-1735.
247. Ribak C.E., Reiffenstein R.J. Selective inhibitory synapse loss in chronic cortical slabs: a morphological basis for epileptic susceptibility. Can. J. Physiol. Pharmacol. 1982, 60:864-870.
248. Rice A., Rafiq A., Shapiro S.M., Jakoi E.R., Coulter D.A., De Lorenzo R.J. Long-lasting reduction of inhibitory function and gamma-aminobutyric acid type A receptor subunit mRNA expression in a model of temporal lobe epilepsy. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:9665-9669.
249. Rivera C., Voipio J., Thomas-Crusells J., Li H., Emri Z., Sipila S., Payne J.A., Minichiello L., Saarma M., Kaila K. Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 2004, 24:4683-4691.
250. - cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. 2005, 562:27-36.
251. - extrusion. J. Cell Biol. 2002, 159:747-752.
252. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
253. Rutecki P.A., Lebeda F.J., Johnston D. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J. Neurophysiol. 1985, 54:1363-1374.
254. Rutecki P.A., Lebeda F.J., Johnston D. 4-Aminopyridine produces epileptiform activity in hippocampus and enhances synaptic excitation and inhibition. J. Neurophysiol. 1987, 57:1911-1924.
255. Rutecki P.A., Lebeda F.J., Johnston D. Epileptiform activity in the hippocampus produced by tetraethylammonium. J. Neurophysiol. 1990, 64:1077-1088.
256. Salah A., Perkins K.L. Effects of subtype-selective group I mGluR antagonists on synchronous activity induced by 4-aminopyridine/CGP 55845 in adult guinea pig hippocampal slices. Neuropharmacology 2008, 55:47-54.
257. Sanchez-Vives M.V., Nowak L.G., McCormick D.A. Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J. Neurosci. 2000, 20:4286-4299.
258. Schwartzkroin P.A., Mutani R., Prince D.A. Orthodromic and antidromic effects of a cortical epileptiform focus on ventrolateral nucleus of the cat. J. Neurophysiol. 1975, 38:795-811.
259. Schwartzkroin P.A., Prince D.A. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Res. 1978, 147:117-130.
260. Schwartzkroin P.A., Prince D.A. Changes in excitatory and inhibitory synaptic potentials leading to epileptogenic activity. Brain Res. 1980, 183:61-73.
261. A receptor currents in the hippocampus. J. Neurosci. 2005, 25:10016-10024.
262. Semyanov A., Walker M.C., Kullmann D.M. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat. Neurosci. 2003, 6:484-490.
263. A receptors: modulating gain and maintaining the tone. Trends Neurosci. 2004, 27:262-269.
264. Singer W., Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 1995, 18:555-586.
265. Sipilä S.T., Huttu K., Yamada J., Afzalov R., Voipio J., Blaesse P., Kaila K. Compensatory enhancement of intrinsic spiking upon NKCC1 disruption in neonatal hippocampus. J. Neurosci. 2009, 29:6982-6988.
266. Sloviter R.S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 1987, 235:73-76.
267. Sloviter R.S., Zappone C.A., Harvey B.D., Bumanglag A.V., Bender R.A., Frotscher M. 'Dormant basket cell' hypothesis revisited: relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat. J. Comp. Neurol. 2003, 459:44-76.
268. 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, 19:9252-9260.
269. Somogyi P., Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 2005, 562:9-26.
270. Spreafico R., Battaglia G., Arcelli P., Andermann F., Dubeau F., Palmini A., Olivier A., Villemure J.G., Tampieri D., Avanzini G., Avoli M. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 1998, 50:27-36.
271. Staba R.J., Wilson C.L., Bragin A., Fried I., Engel J. Quantitative analysis of high-frequency oscillations (80-500Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol. 2002, 88:1743-1752.
272. A receptors. Science 1995, 269:977-981.
273. Stasheff S.F., Hines M., Wilson W.A. Axon terminal hyperexcitability associated with epileptogenisis in vitro. I. Origin of ectopic spikes. J. Neurophysiol. 1993, 70:961-975.
274. A receptors. J. Neurophysiol. 1993, 70:976-984.
275. Sudbury J., Avoli M. Epileptiform synchronization in the rat insular and perirhinal cortices in vitro. Eur. J. Neurosci. 2007, 26:3571-3582.
276. Swann J.W., Brady R.J. Penicillin-induced epileptogenesis in immature rat CA3 hippocampal pyramidal cells. Dev. Brain Res. 1984, 12:243-254.
277. Swartzwelder S.H., Lewis D.V., Anderson W.W., Wilson W.A. Seizure-like events in brain slices: supression by interictal activity. Brain Res. 1987, 410:362-366.
278. Tamás G., Somogyi P., Buhl E.H. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J. Neurosci. 1998, 18:4255-4270.
279. Tamás G., Buhl E.H., Lörincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 2000, 3:366-371.
280. Tassi L., Colombo N., Garbelli R., Francione S., Lo Russo G., Mai R., Cardinale F., Cossu M., Ferrario A., Galli C., Bramerio M., Citterio A., Spreafico R. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 2002, 125:1719-1732.
281. Traub R.D., Wong R.K. Cellular mechanism of neuronal synchronization in epilepsy. Science 1982, 216:745-747.
282. Traub R.D., Jefferys J.G. Simulations of epileptiform activity in the hippocampal CA3 region in vitro. Hippocampus 1994, 4:281-285.
283. Traub R.D., Borck C., Collins S.B., Jefferys J.G. On the structure of ictal events in vitro. Epilepsia 1996, 37:879-891.
284. Traub R.D., Whittington M.A., Buhl E.H., Jefferys J.G., Faulkner H.J. On the mechanism of the gamma → beta frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation. J. Neurosci. 1999, 19:1088-1105.
285. Traub R.D. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur. J. Neurosci. 2000, 12:4093-4106.
286. Traub R.D., Pais I., Bibbig A., LeBeau F.E., Buhl E.H., Hormuzdi S.G., Monyer H., Whittington M.A. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc. Natl. Acad. Sci., U.S.A. 2003, 100:1370-1374.
287. Traub R.D., Michelson-Law H., Bibbig A.E., Buhl E.H., Whittington M.A. Gap junctions, fast oscillations and the initiation of seizures. Adv. Exp. Med. Biol. 2004, 548:110-122.
288. Trevelyan A.J. The direct relationship between inhibitory currents and local field potentials. J. Neurosci. 2009, 29:15299-15307.
289. Trombin F., Gnatkovsky V., de Curtis M. Changes in action potential features during focal seizure discharges in the entorhinal cortex of the in vitro isolated guinea pig brain. J. Neurophysiol 2011, [Epub ahead of print], PMID: 21676935.
290. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 2010, 11:100-113.
291. A receptor subunit expression bypharmacological agents. Pharmacol. Rev. 2010, 62:97-135.
292. Urrestarazu E., Chander R., Dubeau F., Gotman J. Interictal high-frequency oscillations (100-500Hz) in the intra-cerebral EEG of epileptic patients. Brain 2007, 130:2354-2366.
293. Uusisaari M., Smirnov S., Voipio J., Kaila K. Spontaneous epileptiform activity mediated by GABA(A) receptors and gap junctions in the rat hippocampal slice following long-term exposure to GABA(B) antagonists. Neuropharmacology 2002, 43:563-572.
294. Uva L., Librizzi L., Wendling F., de Curtis M. Propagation dynamics of epileptiform activity in the hippocampal-parahippocampal region of the isolated guinea pig brain. Epilepsia 2005, 46:1914-1925.
295. A receptor-dependent potentials in limbic areas of the in vitro isolated adult guinea pig brain. Eur. J. Neurosci. 2009, 29:911-920.
296. van der Linden S., Panzica F., de Curtis M. Carbachol induces fast oscillations in the medial but not in the lateral entorhinal cortex of the isolated guinea pig brain. J. Neurophysiol. 1999, 82:2441-2450.
297. van Groen T., Lopes da Silva F.H. Organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat: II. An electrophysiological study. J. Comp. Neurol. 1986, 251:111-120.
298. van Groen T., van Haren F.J., Witter M.P., Groenewegen H.J. The organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat: I. A neuroanatomical tracing study. J. Comp. Neurol. 1986, 250:485-497.
299. van Vliet E.A., Aronica E., Tolner E.A., Lopes da Silva F.H., Gorter J.A. Progression of temporal lobe epilepsy in the rat is associated with immunocytochemical changes in inhibitory interneurons in specific regions of the hippocampal formation. Exp. Neurol. 2004, 187:367-379.
300. Vanhatalo S., Hellstrom-Westas L., de Vries L.S. Bumetanide for neonatal seizures: based on evidence or enthusiasm?. Epilepsia 2009, 50:1292-1293.
301. Velazquez J.L., Carlen P.L. Synchronization of GABAergic interneuronal networks during seizure-like activity in the rat horizontal hippocampal slice. Eur. J. Neurosci. 1999, 11:4110-4118.
302. - cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J. Physiol. 2010, 588:1527-1540.
303. Voskuyl R.A., Albus H. Spontaneous epileptiform discharges in hippocampal slices induced by 4-aminopyridine. Brain Res. 1985, 342:54-66.
304. Vreugdenhil M., Bracci E., Jefferys J.G. Layer-specific pyramidal cell oscillations evoked by tetanic stimulation in the rat hippocampal area CA1 in vitro and in vivo. J. Physiol. 2005, 562:149-164.
305. Walther H., Lambert J.D., Jones R.S., Heinemann U., Hamon B. Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett. 1986, 69:156-161.
306. Wang X.J., Buzsáki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 1996, 16:6402-6413.
307. Wendling F., Bartolomei F., Bellanger J.J., Chauvel P. Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition. Eur. J. Neurosci. 2002, 15:1499-1508.
308. White J.A., Chow C.C., Ritt J., Soto-Treviño C., Kopell N. Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J. Comput. Neurosci. 1998, 5:5-16.
309. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 1995, 373:612-615.
310. Whittington M.A., Stanford I.M., Colling S.B., Jefferys J.G., Traub R.D. Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J. Physiol. 1997, 502:591-607.
311. Whittington M.A., Traub R.D. Inhibitory interneurons and network oscillations in vitro. TINS 2003, 26:676-682.
312. Williams S., Vachon P., Lacaille J.C. Monosynaptic GABA-mediated inhibitory postsynaptic potentials in CA1 pyramidal of hyperexcitable hippocampal slices from kainic acid-treated rats. Neuroscience 1993, 52:541-554.
313. Wilson C.L., Engel J. Electrical stimulation of the human epileptic limbic cortex. Electrical and Magnetic Stimulation of the Brain and Spinal Cord 1993, 103-113. Raven Press, New York. O. Devinski, A. Bekic, M. Dogali (Eds.).
314. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., Lohman A.H.M. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 1989, 33:161-253.
315. Witter M.P. Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 1993, 3:33-44.
316. Wittner L., Miles R. Factors defining a pacemaker region for synchrony in the hippocampus. J. Physiol. 2007, 584:867-883.
317. Wong R.K., Prince D.A. Dendritic mechanisms underlying penicillin-induced epileptiform activity. Science 1979, 204:1228-1231.
318. Wong R.K., Stewart M. Different firing patterns generated in dendrites and somata of CA1 pyramidal neurones in guinea-pig hippocampus. J. Physiol. 1992, 457:675-687.
319. Wong R.K., Traub R.D., Miles R. Cellular basis of neuronal synchrony in epilepsy. Adv. Neurol. 1986, 44:583-592.
320. Wozny C., Kivi A., Lehmann T.N., Dehnicke C., Heinemann U., Behr J. Comment on " On the origin of interictal activity in human temporal lobe epilepsy in vitro" Science 2003, 301:463.
321. Wozny C., Gabriel S., Jandova K., Schulze K., Heinemann U., Behr J. Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol. Dis. 2005, 19:451-460.
322. Wozny C., Knopp A., Lehmann T.N., Heinemann U., Behr J. The subiculum: a potential site of ictogenesis in human temporal lobe epilepsy. Epilepsia 2005, 46(Suppl 5):17-21.
323. Yeung J.Y., Canning K.J., Zhu G., Pennefather P., MacDonald J.F., Orser B.A. Tonically activated GABAA receptors in hippocampal neurons are high-affinity, low-conductance sensors for extracellular GABA. Mol. Pharmacol. 2003, 63:2-8.
324. Ylinen A., Bragin A., Nádasdy Z., Jandó G., Szabó I., Sik A., Buzsáki G. Sharp wave-associated high-frequency oscillation (200Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 1995, 15:30-46.
325. A, slow synaptic inhibition in mouse hippocampus. J. Neurophysiol. 2009, 101:1179-1191.
326. Ziburkus J., Cressman J.R., Barreto E., Schiff S.J. Interneuron and pyramidal cell interplay during in vitro seizure-like events. J. Neurophysiol. 2006, 95:3948-3954.
327. Zuckermann E.C., Glaser G.H. Hippocampal epileptic activity induced by localized ventricular perfusion with high-potassium cerebrospinal fluid. Exp. Neurol. 1968, 20:87-110.