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Current Neuropharmacology

Author(s): Maxime Lévesque, David Ragsdale and Massimo Avoli*

DOI: 10.2174/1570159X17666181127124803

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Evolving Mechanistic Concepts of Epileptiform Synchronization and their Relevance in Curing Focal Epileptic Disorders

Page: [830 - 842] Pages: 13

  • * (Excluding Mailing and Handling)

Abstract

The synchronized activity of neuronal networks under physiological conditions is mirrored by specific oscillatory patterns of the EEG that are associated with different behavioral states and cognitive functions. Excessive synchronization can, however, lead to focal epileptiform activity characterized by interictal and ictal discharges in epileptic patients and animal models. This review focusses on studies that have addressed epileptiform synchronization in temporal lobe regions by employing in vitro and in vivo recording techniques. First, we consider the role of ionotropic and metabotropic excitatory glutamatergic transmission in seizure generation as well as the paradoxical role of GABAA signaling in initiating and perhaps maintaining focal seizure activity. Second, we address non-synaptic mechanisms (which include voltage-gated ionic currents and gap junctions) in the generation of epileptiform synchronization. For each mechanism, we discuss the actions of antiepileptic drugs that are presumably modulating excitatory or inhibitory signaling and voltage-gated currents to prevent seizures in epileptic patients. These findings provide insights into the mechanisms of seizure initiation and maintenance, thus leading to the development of specific pharmacological treatments for focal epileptic disorders.

Keywords: Epileptiform synchronization, mesial temporal lobe epilepsy, interictal spikes, seizures, anti-epileptic drugs, excitatory transmission, inhibitory transmission, voltage-gated channels.

Graphical Abstract

[1]
Niedermeyer, E.; da Silva, F.H.L. Electroencephalography: Basic Principles, Clinical Applications, and Related Fields; Lippincott Williams & Wilkins, 2005.
[2]
Steriade, M.; Gloor, P.; Llinás, R.R.; Lopes de Silva, F.H.; Mesulam, M.M. Report of IFCN committee on basic Mechanisms. Basic mechanisms of cerebral rhythmic activities. Electroencephalogr. Clin. Neurophysiol., 1990, 76(6), 481-508.
[http://dx.doi.org/10. 1016/0013-4694(90)90001-Z] [PMID: 1701118]
[3]
Buzsáki, G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus, 2015, 25(10), 1073-1188.
[http://dx.doi.org/10.1002/hipo.22488] [PMID: 26135716]
[4]
Jefferys, J.G.R.; Jiruska, P.; de Curtis, M.; Avoli, M. Limbic network Synchronization and temporal lobe epilepsy. Jasper’s Basic mechanisms of the Epilepsies; Noebels, J.; Avoli, M.; Rogawski, M.; Olsen, R.; Delgado-Escueta, A., Eds.; National Center for Biotechnology Information (US): Bethesda (MD), 2012
[http://dx.doi.org/10.1093/med/9780199746545.003.0014]
[5]
Avoli, M.; de Curtis, M.; Gnatkovsky, V.; Gotman, J.; Köhling, R.; Lévesque, M.; Manseau, F.; Shiri, Z.; Williams, S. Specific imbalance of excitatory/inhibitory signaling establishes seizure onset pattern in temporal lobe epilepsy. J. Neurophysiol., 2016, 115(6), 3229-3237.
[http://dx.doi.org/10.1152/jn.01128.2015] [PMID: 27075542]
[6]
Gloor, P.; Fariello, R.G. Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci., 1988, 11(2), 63-68.
[http://dx.doi.org/10.1016/0166-2236(88)90166-X] [PMID: 2465601]
[7]
Timofeev, I.; Steriade, M. Neocortical seizures: initiation, development and cessation. Neuroscience, 2004, 123(2), 299-336.
[http://dx.doi.org/10.1016/j.neuroscience.2003.08.051] [PMID: 14698741]
[8]
Beenhakker, M.P.; Huguenard, J.R. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron, 2009, 62(5), 612-632.
[http://dx.doi.org/10.1016/j.neuron.2009.05.015] [PMID: 19524522]
[9]
Crunelli, V.; Leresche, N.; Cope, D.W. GABA-A Receptor function in typical absence seizures. Jasper’s Basic mechanisms of the epilepsies; Noebels, J.; Avoli, M.; Rogawski, M.; Olsen, R.; Delgado- Escueta, A., Eds.; National center for biotechnology information (US): Bethesda (MD), 2012.
[10]
Engel, J., Jr Introduction to temporal lobe epilepsy. Epilepsy Res., 1996, 26(1), 141-150.
[http://dx.doi.org/10.1016/S0920-1211(96) 00043-5] [PMID: 8985696]
[11]
Gloor, P. The Temporal Lobe and Limbic System; Oxford University Press: USA, 1997.
[12]
Engel, J., Jr; McDermott, M.P.; Wiebe, S.; Langfitt, J.T.; Stern, J.M.; Dewar, S.; Sperling, M.R.; Gardiner, I.; Erba, G.; Fried, I.; Jacobs, M.; Vinters, H.V.; Mintzer, S.; Kieburtz, K. Early surgical therapy for drug-resistant temporal lobe epilepsy: A randomized trial. JAMA, 2012, 307(9), 922-930.
[http://dx.doi.org/10.1001/jama.2012.220] [PMID: 22396514]
[13]
Buzsáki, G.; Silva, F.L. High frequency oscillations in the intact brain. Prog. Neurobiol., 2012, 98(3), 241-249.
[http://dx.doi.org/ 10.1016/j.pneurobio.2012.02.004] [PMID: 22449727]
[14]
Bragin, A.; Engel, J., Jr; Wilson, C.L.; Fried, I.; Buzsáki, G. High-frequency oscillations in human brain. Hippocampus, 1999, 9(2), 137-142.
[http://dx.doi.org/10.1002/(SICI)1098-1063(1999)9:2 <137:AID-HIPO5>3.0.CO;2-0]
[15]
Staba, R.J.; Wilson, C.L.; Bragin, A.; Jhung, D.; Fried, I.; Engel, J., Jr High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol., 2004, 56(1), 108-115.
[http://dx.doi.org/10.1002/ana.20164] [PMID: 15236407]
[16]
Bragin, A.; Engel, J., Jr; Wilson, C.L.; Fried, I.; Mathern, G.W. Hippocampal and entorhinal cortex high-frequency oscillations (100--500 Hz) in human epileptic brain and in kainic acid--treated rats with chronic seizures. Epilepsia, 1999, 40(2), 127-137.
[PMID: 9952257] [http://dx.doi.org/http://10.1111/j.1528-1157.1999.tb02065.x ]
[17]
Lévesque, M.; Bortel, A.; Gotman, J.; Avoli, M. High-frequency (80-500 Hz) oscillations and epileptogenesis in temporal lobe epilepsy. Neurobiol. Dis., 2011, 42(3), 231-241.
[http://dx.doi.org/ 10.1016/j.nbd.2011.01.007] [PMID: 21238589]
[18]
Lévesque, M.; Salami, P.; Gotman, J.; Avoli, M. Two seizure-onset types reveal specific patterns of high-frequency oscillations in a model of temporal lobe epilepsy. J. Neurosci., 2012, 32(38), 13264-13272.
[http://dx.doi.org/10.1523/JNEUROSCI.5086-11.2012] [PMID: 22993442]
[19]
Jirsch, J.D.; Urrestarazu, E.; LeVan, P.; Olivier, A.; Dubeau, F.; Gotman, J. High-frequency oscillations during human focal seizures. Brain, 2006, 129(Pt 6), 1593-1608.
[http://dx.doi.org/10. 1093/brain/awl085]
[20]
Urrestarazu, E.; Jirsch, J.D.; LeVan, P.; Hall, J.; Avoli, M.; Dubeau, F.; Gotman, J. High-frequency intracerebral EEG activity (100-500 Hz) following interictal spikes. Epilepsia, 2006, 47(9), 1465-1476.
[http://dx.doi.org/10.1111/j.1528-1167.2006.00618.x] [PMID: 16981862]
[21]
Zijlmans, M.; Jacobs, J.; Kahn, Y.U.; Zelmann, R.; Dubeau, F.; Gotman, J. Ictal and interictal high frequency oscillations in patients with focal epilepsy. Clin. Neurophysiol., 2011, 122(4), 664-671.
[http://dx.doi.org/10.1016/j.clinph.2010.09.021] [PMID: 21030302]
[22]
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.
[http://dx.doi.org/10.1016/0006-8993(73)90647-1] [PMID: 4573428]
[23]
Li, C.L. Cortical intracellular potentials and their responses to strychnine. J. Neurophysiol., 1959, 22(4), 436-450.
[http://dx.doi.org/10.1152/jn.1959.22.4.436] [PMID: 13673295]
[24]
Goldensohn, E.S.; Purpura, D.P. Intracellular potentials of cortical neurons during focal epileptogenic discharges. Science, 1963, 139(3557), 840-842.
[http://dx.doi.org/10.1126/science.139.3557. 840] [PMID: 13948714]
[25]
Matsumoto, H.; Marsan, C.A. Cortical cellular phenomena in experimental epilepsy: Interictal manifestations. Exp. Neurol., 1964, 9, 286-304.
[http://dx.doi.org/10.1016/0014-4886(64)90025-1] [PMID: 14145629]
[26]
Prince, D.A. Inhibition in “epileptic” neurons. Exp. Neurol., 1968, 21(3), 307-321.
[http://dx.doi.org/10.1016/0014-4886(68)90043-5] [PMID: 5673646]
[27]
Dichter, M.; Spencer, W.A. Penicillin-induced interictal discharges from the cat hippocampus. I. Characteristics and topographical features. J. Neurophysiol., 1969, 32(5), 649-662.
[http://dx.doi.org/ 10.1152/jn.1969.32.5.649] [PMID: 4309021]
[28]
Dichter, M.; Spencer, W.A. Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction. J. Neurophysiol., 1969, 32(5), 663-687.
[http://dx.doi.org/10.1152/jn.1969.32.5.663] [PMID: 4309022]
[29]
Dingledine, R.; Gjerstad, L. Reduced inhibition during epileptiform activity in the in vitro hippocampal slice. J. Physiol., 1980, 305, 297-313.
[http://dx.doi.org/10.1113/jphysiol.1980.sp013364] [PMID: 7441555]
[30]
Schwartzkroin, P.A.; Prince, D.A. Changes in excitatory and inhibitory synaptic potentials leading to epileptogenic activity. Brain Res., 1980, 183(1), 61-76.
[http://dx.doi.org/10.1016/0006-8993(80)90119-5] [PMID: 6244050]
[31]
Traub, R.D.; Wong, R.K. Cellular mechanism of neuronal synchronization in epilepsy. Science, 1982, 216(4547), 745-747.
[PMID: 7079735] [http://dx.doi.org/http://10.1126/science.7079735]
[32]
Johnston, D.; Brown, T.H. Giant synaptic potential hypothesis for epileptiform activity. Science, 1981, 211(4479), 294-297.
[http://dx.doi.org/10.1126/science.7444469] [PMID: 7444469]
[33]
Rutecki, P.A.; Lebeda, F.J.; Johnston, D. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J. Neurophysiol., 1985, 54(5), 1363-1374.
[http://dx.doi.org/10. 1152/jn.1985.54.5.1363] [PMID: 2416891]
[34]
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(6), 1911-1924.
[http://dx.doi.org/10.1152/jn.1987.57.6.1911] [PMID: 3037040]
[35]
Rutecki, P.A.; Lebeda, F.J.; Johnston, D. Epileptiform activity in the hippocampus produced by tetra ethyl ammonium. J. Neurophysiol., 1990, 64(4), 1077-1088.
[http://dx.doi.org/10.1152/jn. 1990.64.4.1077] [PMID: 2258736]
[36]
Swann, J.W.; Brady, R.J. Penicillin-induced epileptogenesis in immature rat CA3 hippocampal pyramidal cells. Brain Res., 1984, 314(2), 243-254.
[http://dx.doi.org/10.1016/0165-3806(84)90046-4] [PMID: 6704751]
[37]
Avoli, M.; de Curtis, M. GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity. Prog. Neurobiol., 2011, 95(2), 104-132.
[http://dx.doi.org/10.1016/j. pneurobio.2011.07.003] [PMID: 21802488]
[38]
Dzhala, V.I.; Staley, K.J. Mechanisms of fast ripples in the hippocampus. J. Neurosci., 2004, 24(40), 8896-8906.
[http://dx.doi.org/ 10.1523/JNEUROSCI.3112-04.2004] [PMID: 15470156]
[39]
Collingridge, G. L.; Lodge, D.; Mayer, M.; Turrigiano, G.; Frenguelli, B. G. Ionotropic glutamate receptors: Still exciting after all these years Neuropharmacology, 2017, 112((Pt A)), 1-3.
[40]
Zhu, S.; Gouaux, E. Structure and symmetry inform gating principles of ionotropic glutamate receptors., Neuropharmacology, 2017, 112(Pt A), 11-15.
[http://dx.doi.org/10.1016/j.neuropharm.2016.08.034]
[41]
Huberfeld, G.; Menendez de la Prida, L.; Pallud, J.; Cohen, I.; Le Van, Q.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(5), 627-634.
[http://dx.doi.org/10.1038/nn.2790] [PMID: 21460834]
[42]
Doherty, J.; Dingledine, R. The roles of metabotropic glutamate receptors in seizures and epilepsy. Curr. Drug Targets CNS Neurol. Disord., 2002, 1(3), 251-260.
[http://dx.doi.org/10.2174/1568007023339355] [PMID: 12769618]
[43]
Wong, R.K.; Bianchi, R.; Taylor, G.W.; Merlin, L.R. Role of metabotropic glutamate receptors in epilepsy. Adv. Neurol., 1999, 79, 685-698.
[PMID: 10514855]
[44]
Jones, R.S.; Heinemann, U. Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J. Neurophysiol., 1988, 59(5), 1476-1496.
[http://dx.doi.org/10.1152/jn.1988.59.5.1476] [PMID: 2898511]
[45]
Hwa, G.G.; Avoli, M. The involvement of excitatory amino acids in neocortical epileptogenesis: NMDA and non-NMDA receptors. Exp. Brain Res., 1991, 86(2), 248-256.
[http://dx.doi.org/10.1007/BF00228949] [PMID: 1684548]
[46]
Benini, R.; D’Antuono, M.; Pralong, E.; Avoli, M. Involvement of amygdala networks in epileptiform synchronization in vitro. Neuroscience, 2003, 120(1), 75-84.
[http://dx.doi.org/10.1016/S0306-4522(03)00262-8] [PMID: 12849742]
[47]
Sudbury, J.R.; Avoli, M. Epileptiform synchronization in the rat insular and perirhinal cortices in vitro. Eur. J. Neurosci., 2007, 26(12), 3571-3582.
[http://dx.doi.org/10.1111/j.1460-9568.2007. 05962.x] [PMID: 18052975]
[48]
Panuccio, G.; Curia, G.; Colosimo, A.; Cruccu, G.; Avoli, M. Epileptiform synchronization in the cingulate cortex. Epilepsia, 2009, 50(3), 521-536.
[http://dx.doi.org/10.1111/j.1528-1167.2008.01779. x] [PMID: 19178556]
[49]
Panuccio, G.; Sanchez, G.; Lévesque, M.; Salami, P.; de Curtis, M.; Avoli, M. On the ictogenic properties of the piriform cortex in vitro. Epilepsia, 2012, 53(3), 459-468.
[http://dx.doi.org/10.1111/j.1528-1167.2012.03408.x] [PMID: 22372627]
[50]
Witkin, J.M.; Li, J.; Gilmour, G.; Mitchell, S.N.; Carter, G.; Gleason, S.D.; Seidel, W.F.; Eastwood, B.J.; McCarthy, A.; Porter, W.J.; Reel, J.; Gardinier, K.M.; Kato, A.S.; Wafford, K.A. Electroencephalographic, cognitive, and neurochemical effects of LY3130481 (CERC-611), a selective antagonist of TARP-γ8-associated AMPA receptors. Neuropharmacology, 2017, 126, 257-270.
[http://dx.doi.org/10.1016/j.neuropharm.2017.07.028] [PMID: 28757050]
[51]
Zhuo, C.; Jiang, R.; Li, G.; Shao, M.; Chen, C.; Chen, G.; Tian, H.; Li, J.; Xue, R.; Jiang, D. Efficacy and tolerability of second and third generation anti-epileptic drugs in refractory epilepsy: A network meta-analysis. Sci. Rep., 2017, 7(1), 2535.
[http://dx.doi.org/10.1038/s41598-017-02525-2] [PMID: 28566726]
[52]
Hanada, T.; Hashizume, Y.; Tokuhara, N.; Takenaka, O.; Kohmura, N.; Ogasawara, A.; Hatakeyama, S.; Ohgoh, M.; Ueno, M.; Nishizawa, Y. Perampanel: a novel, orally active, noncompetitive AMPA-receptor antagonist that reduces seizure activity in rodent models of epilepsy. Epilepsia, 2011, 52(7), 1331-1340.
[http://dx.doi.org/10.1111/j.1528-1167.2011.03109.x] [PMID: 21635236]
[53]
Rogawski, M.A.; Hanada, T. Preclinical pharmacology of perampanel, a selective non-competitive AMPA receptor antagonist. Acta Neurol. Scand. Suppl., 2013, (197), 19-24.
[http://dx.doi.org/10. 1111/ane.12100] [PMID: 23480152]
[54]
Kato, A.S.; Burris, K.D.; Gardinier, K.M.; Gernert, D.L.; Porter, W.J.; Reel, J.; Ding, C.; Tu, Y.; Schober, D.A.; Lee, M.R.; Heinz, B.A.; Fitch, T.E.; Gleason, S.D.; Catlow, J.T.; Yu, H.; Fitzjohn, S.M.; Pasqui, F.; Wang, H.; Qian, Y.; Sher, E.; Zwart, R.; Wafford, K.A.; Rasmussen, K.; Ornstein, P.L.; Isaac, J.T.; Nisenbaum, E.S.; Bredt, D.S.; Witkin, J.M. Forebrain-selective AMPA-receptor antagonism guided by TARP γ-8 as an antiepileptic mechanism. Nat. Med., 2016, 22(12), 1496-1501.
[http://dx.doi.org/10.1038/nm.4221] [PMID: 27820603]
[55]
Olney, J.W.; Labruyere, J.; Wang, G.; Wozniak, D.F.; Price, M.T.; Sesma, M.A. NMDA antagonist neurotoxicity: Mechanism and prevention. Science, 1991, 254(5037), 1515-1518.
[PMID: 1835799] [http://dx.doi.org/http://10.1126/science.1835799]
[56]
Gryder, D.S.; Rogawski, M.A. Selective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J. Neurosci., 2003, 23(18), 7069-7074.
[PMID: 12904467] [http://dx.doi.org/http://10.1523/JNEUROSCI.23-18-07069.2003]
[57]
Kaminski, R.M.; Banerjee, M.; Rogawski, M.A. Topiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist. Neuropharmacology, 2004, 46(8), 1097-1104.
[http://dx.doi.org/10.1016/j.neuropharm.2004.02.010] [PMID: 15111016]
[58]
Braga, M.F.M.; Aroniadou-Anderjaska, V.; Li, H.; Rogawski, M.A. Topiramate reduces excitability in the basolateral amygdala by selectively inhibiting GluK1 (GluR5) kainate receptors on interneurons and positively modulating GABAA receptors on principal neurons. J. Pharmacol. Exp. Ther., 2009, 330(2), 558-566.
[http://dx.doi.org/10.1124/jpet.109.153908] [PMID: 19417176]
[59]
Subramaniam, S.; Rho, J.M.; Penix, L.; Donevan, S.D.; Fielding, R.P.; Rogawski, M.A. Felbamate block of the N-methyl-D-aspartate receptor. J. Pharmacol. Exp. Ther., 1995, 273(2), 878-886.
[PMID: 7752093]
[60]
Yang, J.; Wetterstrand, C.; Jones, R.S.G. Felbamate but not phenytoin or gabapentin reduces glutamate release by blocking presynaptic NMDA receptors in the entorhinal cortex. Epilepsy Res., 2007, 77(2-3), 157-164.
[http://dx.doi.org/10.1016/j.eplepsyres.2007.09. 005] [PMID: 17980555]
[61]
Bianchi, R.; Wong, R.K.S.; Merlin, L.R. Glutamate receptors in epilepsy: Group I mGluR-mediated epileptogenesis. Jasper’s Basic mechanisms of the epilepsies, 2012.
[62]
Ghauri, M.; Chapman, A.G.; Meldrum, B.S. Convulsant and anticonvulsant actions of agonists and antagonists of group III mGluRs. Neuroreport, 1996, 7(9), 1469-1474.
[http://dx.doi.org/ 10.1097/00001756-199606170-00005] [PMID: 8856700]
[63]
Kłodzińska, A.; Chojnacka-Wójcik, E.; Pilc, A. Selective group II glutamate metabotropic receptor agonist LY354740 attenuates pentetrazole- and picrotoxin-induced seizures. Pol. J. Pharmacol., 1999, 51(6), 543-545.
[PMID: 10817535]
[64]
Wong, R.K.S.; Chuang, S-C.; Bianchi, R. Metabotropic glutamate receptors and epileptogenesis. Epilepsy Curr., 2002, 2(3), 81-85.
[http://dx.doi.org/10.1046/j.1535-7597.2002.00031.x] [PMID: 15309152]
[65]
Park, J-Y.; Remy, S.; Varela, J.; Cooper, D.C.; Chung, S.; Kang, H-W.; Lee, J-H.; Spruston, N. A post-burst after depolarization is mediated by group i metabotropic glutamate receptor-dependent upregulation of Ca(v)2.3 R-type calcium channels in CA1 pyramidal neurons. PLoS Biol., 2010, 8(11), e1000534.
[http://dx.doi.org/10.1371/journal.pbio.1000534] [PMID: 21103408]
[66]
Congar, P.; Leinekugel, X.; Ben-Ari, Y.; Crépel, V. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J. Neurosci., 1997, 17(14), 5366-5379.
[http://dx.doi.org/10.1523/JNEUROSCI.17-14-05366.1997] [PMID: 9204921]
[67]
Kawasaki, H.; Palmieri, C.; Avoli, M. Muscarinic receptor activation induces depolarizing plateau potentials in bursting neurons of the rat subiculum. J. Neurophysiol., 1999, 82(5), 2590-2601.
[http://dx.doi.org/10.1152/jn.1999.82.5.2590] [PMID: 10561429]
[68]
Klink, R.; Alonso, A. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol., 1997, 77(4), 1829-1843.
[http://dx.doi.org/10.1152/jn.1997.77.4.1829] [PMID: 9114239]
[69]
Klink, R.; Alonso, A. Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J. Neurophysiol., 1997, 77(4), 1813-1828.
[http://dx.doi.org/10.1152/jn.1997.77.4.1813] [PMID: 9114238]
[70]
D’Antuono, M.; Kawasaki, H.; Palmieri, C.; Curia, G.; Biagini, G.; Avoli, M. Antiepileptic drugs and muscarinic receptor-dependent excitation in the rat subiculum. Neuropharmacology, 2007, 52(5), 1291-1302.
[http://dx.doi.org/10.1016/j.neuropharm.2007.01.008] [PMID: 17337018]
[71]
Avoli, M.; Krnjević, K. The long and winding road to gamma-Amino-Butyric acid as neurotransmitter. Can. J. Neurol. Sci., 2016, 43(2), 219-226.
[http://dx.doi.org/10.1017/cjn.2015.333] [PMID: 26763167]
[72]
Coursin, D.B. Convulsive seizures in infants with pyridoxine-deficient diet. J. Am. Med. Assoc., 1954, 154(5), 406-408.
[PMID: 13117629] [http://dx.doi.org/http://10.1001/jama.1954.02940390030009] [PMID: 13117629]
[73]
Hawkins, J.E., Jr; 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(6), 481-484.
[http://dx.doi.org/10.1016/0009-8981(57)90049-9] [PMID: 13500579]
[74]
Ben-Ari, Y.; Krnjević, K.; Reinhardt, W. Hippocampal seizures and failure of inhibition. Can. J. Physiol. Pharmacol., 1979, 57(12), 1462-1466.
[http://dx.doi.org/10.1139/y79-218]
[75]
Kostopoulos, G.; Avoli, M.; Gloor, P. Participation of cortical recurrent inhibition in the genesis of spike and wave discharges in feline generalized penicillin epilepsy. Brain Res., 1983, 267(1), 101-112.
[http://dx.doi.org/10.1016/0006-8993(83)91043-0] [PMID: 6860937]
[76]
Sloviter, R.S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science, 1987, 235(4784), 73-76.
[http://dx.doi.org/10.1126/science.2879352] [PMID: 2879352]
[77]
Williamson, A.; Telfeian, A.E.; Spencer, D.D. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J. Neurophysiol., 1995, 74(1), 378-387.
[http://dx.doi.org/10.1152/jn.1995.74.1.378] [PMID: 7472339]
[78]
McDonald, J.W.; Garofalo, E.A.; Hood, T.; Sackellares, J.C.; Gilman, S.; McKeever, P.E.; Troncoso, J.C.; Johnston, M.V. Altered excitatory and inhibitory amino acid receptor binding in hippocampus of patients with temporal lobe epilepsy. Ann. Neurol., 1991, 29(5), 529-541.
[http://dx.doi.org/10.1002/ana.410290513] [PMID: 1650160]
[79]
Johnson, E.W.; de Lanerolle, N.C.; Kim, J.H.; Sundaresan, S.; Spencer, D.D.; Mattson, R.H.; Zoghbi, S.S.; Baldwin, R.M.; Hoffer, P.B.; Seibyl, J.P. “Central” and “peripheral” benzodiazepine receptors: opposite changes in human epileptogenic tissue. Neurology, 1992, 42(4), 811-815.
[http://dx.doi.org/10.1212/WNL.42. 4.811] [PMID: 1314342]
[80]
Olsen, R.W.; Bureau, M.; Houser, C.R.; Delgado-Escueta, A.V.; Richards, J.G.; Möhler, H. GABA/benzodiazepine receptors in human focal epilepsy. Epilepsy Res. Suppl., 1992, 8, 383-391.
[PMID: 1329826] [PMID: 1329826]
[81]
Rice, A.; Rafiq, A.; Shapiro, S.M.; Jakoi, E.R.; Coulter, D.A.; DeLorenzo, 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. USA, 1996, 93(18), 9665-9669.
[http://dx.doi.org/10.1073/pnas. 93.18.9665] [PMID: 8790388]
[82]
Kamphuis, W.; De Rijk, T.C.; Lopes da Silva, F.H. Expression of GABAA receptor subunit mRNAs in hippocampal pyramidal and granular neurons in the kindling model of epileptogenesis: An in situ hybridization study. Brain Res. Mol. Brain Res., 1995, 31(1-2), 33-47.
[http://dx.doi.org/10.1016/0169-328X(95)00022-K] [PMID: 7476032]
[83]
Mody, I.; Lambert, J.D.; Heinemann, U. Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J. Neurophysiol., 1987, 57(3), 869-888.
[http://dx.doi.org/10.1152/jn.1987.57.3.869] [PMID: 3031235]
[84]
Tancredi, V.; Hwa, G.G.; Zona, C.; Brancati, A.; Avoli, M. Low magnesium epileptogenesis in the rat hippocampal slice: electrophysiological and pharmacological features. Brain Res., 1990, 511(2), 280-290.
[http://dx.doi.org/10.1016/0006-8993(90)90173-9] [PMID: 1970748]
[85]
Dickson, C.T.; Alonso, A. Muscarinic induction of synchronous population activity in the entorhinal cortex. J. Neurosci., 1997, 17(17), 6729-6744.
[http://dx.doi.org/10.1523/JNEUROSCI.17-17-06729.1997] [PMID: 9254685]
[86]
Michelson, H.B.; Wong, R.K. Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J. Physiol., 1994, 477(Pt 1), 35-45.
[http://dx.doi.org/10.1113/jphysiol.1994.sp020169] [PMID: 8071887]
[87]
Perreault, P.; Avoli, M. 4-aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. J. Neurosci., 1992, 12(1), 104-115.
[http://dx.doi.org/10.1523/JNEUROSCI.12-01-00104.1992] [PMID: 1309571]
[88]
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., 1996, 16(12), 3912-3924.
[http://dx.doi.org/10.1523/JNEUROSCI. 16-12-03912.1996] [PMID: 8656285]
[89]
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., 1996, 493(Pt 3), 707-717.
[http://dx.doi.org/10.1113/jphysiol.1996.sp021416] [PMID: 8799893]
[90]
Morris, M.E.; Obrocea, G.V.; Avoli, M. Extracellular K+ accumulations and synchronous GABA-mediated potentials evoked by 4-aminopyridine in the adult rat hippocampus. Exp. Brain Res., 1996, 109(1), 71-82.
[http://dx.doi.org/10.1007/BF00228628] [PMID: 8740210]
[91]
Barolet, A.W.; Morris, M.E. Changes in extracellular K+ evoked by GABA, THIP and baclofen in the guinea-pig hippocampal slice. Exp. Brain Res., 1991, 84(3), 591-598.
[http://dx.doi.org/10.1007/BF00230971] [PMID: 1650707]
[92]
Di Cristo, G.; Awad, P.N.; Hamidi, S.; Avoli, M. KCC2, epileptiform synchronization, and epileptic disorders. Prog. Neurobiol., 2018, 162, 1-16.
[http://dx.doi.org/10.1016/j.pneurobio.2017.11. 002] [PMID: 29197650]
[93]
Viitanen, T.; Ruusuvuori, E.; Kaila, K.; Voipio, J. The K+-Cl cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J. Physiol., 2010, 588(Pt 9), 1527-1540.
[http://dx.doi.org/10.1113/jphysiol.2009.181826] [PMID: 20211979]
[94]
Grover, L.M.; Lambert, N.A.; Schwartzkroin, P.A.; Teyler, T.J. Role of HCO3- ions in depolarizing GABAA receptor-mediated responses in pyramidal cells of rat hippocampus. J. Neurophysiol., 1993, 69(5), 1541-1555.
[http://dx.doi.org/10.1152/jn.1993.69.5.1541] [PMID: 8389828]
[95]
Kaila, K. Ionic basis of GABAA receptor channel function in the nervous system. Prog. Neurobiol., 1994, 42(4), 489-537.
[http://dx.doi.org/10.1016/0301-0082(94)90049-3] [PMID: 7522334]
[96]
Staley, K.J.; Soldo, B.L.; Proctor, W.R. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science, 1995, 269(5226), 977-981.
[http://dx.doi.org/10.1126/science.7638623] [PMID: 7638623]
[97]
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(11), 4110-4118.
[http://dx.doi.org/10.1046/j.1460-9568.1999.00837.x] [PMID: 10583499]
[98]
Köhling, R.; Vreugdenhil, M.; Bracci, E.; Jefferys, J.G. Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J. Neurosci., 2000, 20(18), 6820-6829.
[PMID: 10995826] [http://dx.doi.org/http://10.1523/JNEUROSCI.20-18-06820.2000] [PMID: 10995826]
[99]
Timofeev, I.; Grenier, F.; Steriade, M. The role of chloride-dependent inhibition and the activity of fast-spiking neurons during cortical spike-wave electrographic seizures. Neuroscience, 2002, 114(4), 1115-1132.
[PMID: 12379264]
[100]
D’Antuono, M.; Louvel, J.; Köhling, R.; Mattia, D.; Bernasconi, A.; Olivier, A.; Turak, B.; Devaux, A.; Pumain, R.; Avoli, M. GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain, 2004, 127(Pt 7), 1626-1640.
[http://dx.doi.org/10.1093/brain/awh181] [PMID: 15175227]
[101]
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(2), 477-494.
[http://dx.doi.org/10.1113/jphysiol.2007.143065] [PMID: 17991696]
[102]
Gnatkovsky, V.; Librizzi, L.; Trombin, F.; de Curtis, M. Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann. Neurol., 2008, 64(6), 674-686.
[http://dx.doi.org/10.1002/ana.21519] [PMID: 19107991]
[103]
Fujiwara-Tsukamoto, Y.; Isomura, Y.; Imanishi, M.; Ninomiya, T.; Tsukada, M.; Yanagawa, Y.; Fukai, T.; Takada, M. Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J. Neurosci., 2010, 30(41), 13679-13689.
[http://dx.doi.org/ 10.1523/JNEUROSCI.1523-10.2010] [PMID: 20943908]
[104]
Uva, L.; Breschi, G.L.; Gnatkovsky, V.; Taverna, S.; de Curtis, M. Synchronous inhibitory potentials precede seizure-like events in acute models of focal limbic seizures. J. Neurosci., 2015, 35(7), 3048-3055.
[http://dx.doi.org/10.1523/JNEUROSCI.3692-14.2015] [PMID: 25698742]
[105]
Librizzi, L.; Losi, G.; Marcon, I.; Sessolo, M.; Scalmani, P.; Carmignoto, G.; de Curtis, M. Interneuronal network activity at the onset of seizure-like events in entorhinal cortex slices. J. Neurosci., 2017, 37(43), 10398-10407.
[http://dx.doi.org/10.1523/JNEUROSCI. 3906-16.2017] [PMID: 28947576]
[106]
Shiri, Z.; Manseau, F.; Lévesque, M.; Williams, S.; Avoli, M. Interneuron activity leads to initiation of low-voltage fast-onset seizures. Ann. Neurol., 2015, 77(3), 541-546.
[http://dx.doi.org/10. 1002/ana.24342] [PMID: 25546300]
[107]
Yekhlef, L.; Breschi, G.L.; Lagostena, L.; Russo, G.; Taverna, S. Selective activation of parvalbumin- or somatostatin-expressing interneurons triggers epileptic seizurelike activity in mouse medial entorhinal cortex. J. Neurophysiol., 2015, 113(5), 1616-1630.
[http://dx.doi.org/10.1152/jn.00841.2014] [PMID: 25505119]
[108]
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(4), 563-572.
[PMID: 12367602] [http://dx.doi.org/http://10.1016/S0028-3908(02) 00156-9] [PMID: 12367602]
[109]
Grasse, D.W.; Karunakaran, S.; Moxon, K.A. Neuronal synchrony and the transition to spontaneous seizures. Exp. Neurol., 2013, 248, 72-84.
[http://dx.doi.org/10.1016/j.expneurol.2013.05.004] [PMID: 23707218]
[110]
Fujita, S.; Toyoda, I.; Thamattoor, A.K.; Buckmaster, P.S. Preictal activity of subicular, CA1, and dentate gyrus principal neurons in the dorsal hippocampus before spontaneous seizures in a rat model of temporal lobe epilepsy. J. Neurosci., 2014, 34(50), 16671-16687.
[http://dx.doi.org/10.1523/JNEUROSCI.0584-14.2014] [PMID: 25505320]
[111]
Toyoda, I.; Fujita, S.; Thamattoor, A.K.; Buckmaster, P.S. Unit Activity of hippocampal interneurons before spontaneous seizures in an animal model of temporal lobe epilepsy. J. Neurosci., 2015, 35(16), 6600-6618.
[http://dx.doi.org/10.1523/JNEUROSCI. 4786-14.2015] [PMID: 25904809]
[112]
Truccolo, W.; Donoghue, J.A.; Hochberg, L.R.; Eskandar, E.N.; Madsen, J.R.; Anderson, W.S.; Brown, E.N.; Halgren, E.; Cash, S.S. Single-neuron dynamics in human focal epilepsy. Nat. Neurosci., 2011, 14(5), 635-641.
[http://dx.doi.org/10.1038/nn.2782] [PMID: 21441925]
[113]
Schevon, C.A.; Weiss, S.A.; McKhann, G., Jr; Goodman, R.R.; Yuste, R.; Emerson, R.G.; Trevelyan, A.J. Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun., 2012, 3, 1060.
[http://dx.doi.org/10.1038/ncomms2056] [PMID: 22968706]
[114]
Rogawski, M.A.; Löscher, W. The neurobiology of antiepileptic drugs. Nat. Rev. Neurosci., 2004, 5(7), 553-564.
[http://dx.doi.org/ 10.1038/nrn1430] [PMID: 15208697]
[115]
Brodie, M.J. Tiagabine pharmacology in profile. Epilepsia, 1995, 36(Suppl. 6), S7-S9.
[http://dx.doi.org/10.1111/j.1528-1157. 1995.tb06015.x] [PMID: 8595791]
[116]
Pollack, M.H.; Roy-Byrne, P.P.; Van Ameringen, M.; Snyder, H.; Brown, C.; Ondrasik, J.; Rickels, K. The selective GABA reuptake inhibitor tiagabine for the treatment of generalized anxiety disorder: results of a placebo-controlled study. J. Clin. Psychiatry, 2005, 66(11), 1401-1408.
[http://dx.doi.org/10.4088/JCP.v66n1109] [PMID: 16420077]
[117]
Lloyd, K.G.; Morselli, P.L.; Depoortere, H.; Fournier, V.; Zivkovic, B.; Scatton, B.; Broekkamp, C.; Worms, P.; Bartholini, G. The potential use of GABA agonists in psychiatric disorders: evidence from studies with progabide in animal models and clinical trials. Pharmacol. Biochem. Behav., 1983, 18(6), 957-966.
[http://dx.doi.org/10.1016/S0091-3057(83)80021-5] [PMID: 6351106]
[118]
Loiseau, P.; Bossi, L.; Guyot, M.; Orofiamma, B.; Morselli, P.L. Double-blind crossover trial of progabide versus placebo in severe epilepsies. Epilepsia, 1983, 24(6), 703-715.
[http://dx.doi.org/10. 1111/j.1528-1157.1983.tb04633.x] [PMID: 6357772]
[119]
Taylor, C.P. Mechanisms of action of gabapentin. Rev. Neurol. (Paris), 1997, 153(Suppl. 1), S39-S45.
[PMID: 9686247]
[120]
Pang, T.; Hirsch, L.J. Treatment of convulsive and nonconvulsive status epilepticus. Curr. Treat. Options Neurol., 2005, 7(4), 247-259.
[http://dx.doi.org/10.1007/s11940-005-0035-x] [PMID: 15967088]
[121]
Costa, E.; Guidotti, A.; Mao, C.C. Evidence for involvement of GABA in the action of benzodiazepines: studies on rat cerebellum. Adv. Biochem. Psychopharmacol., 1975, (14), 113-130.
[PMID: 242198] [PMID: 242198]
[122]
Choi, D.W.; Farb, D.H.; Fischbach, G.D. Chlordiazepoxide selectively augments GABA action in spinal cord cell cultures. Nature, 1977, 269(5626), 342-344.
[http://dx.doi.org/10.1038/269342a0] [PMID: 561893]
[123]
Olsen, R.W. Allosteric ligands and their binding sites define γ-aminobutyric acid (GABA) type A receptor subtypes. Adv. Pharmacol., 2015, 73, 167-202.
[http://dx.doi.org/10.1016/bs.apha. 2014.11.005] [PMID: 25637441]
[124]
Watts, A.E.; Jefferys, J.G. Effects of carbamazepine and baclofen on 4-aminopyridine-induced epileptic activity in rat hippocampal slices. Br. J. Pharmacol., 1993, 108(3), 819-823.
[PMID: 8467367] [http://dx.doi.org/http://10.1111/j.1476-5381.1993.tb12884.x]
[125]
Motalli, R.; Louvel, J.; Tancredi, V.; Kurcewicz, I.; Wan-Chow-Wah, D.; Pumain, R.; Avoli, M. GABA(B) receptor activation promotes seizure activity in the juvenile rat hippocampus. J. Neurophysiol., 1999, 82(2), 638-647.
[http://dx.doi.org/10.1152/jn. 1999.82.2.638] [PMID: 10444662]
[126]
Mott, D.D.; Bragdon, A.C.; Lewis, D.V.; Wilson, W.A. Baclofen has a proepileptic effect in the rat dentate gyrus. J. Pharmacol. Exp. Ther., 1989, 249(3), 721-725.
[PMID: 2543809] [PMID: 2543809]
[127]
Motalli, R.; D’Antuono, M.; Louvel, J.; Kurcewicz, I.; D’Arcangelo, G.; Tancredi, V.; Manfredi, M.; Pumain, R.; Avoli, M. Epileptiform synchronization and GABA(B) receptor antagonism in the juvenile rat hippocampus. J. Pharmacol. Exp. Ther., 2002, 303(3), 1102-1113.
[http://dx.doi.org/10.1124/jpet.102.040782] [PMID: 12438533]
[128]
Hille, B. Ion Channels of excitable membranes: 9780878933211: Medicine & Health Science Books @ Amazon.com https://www. amazon.com/Channels-Excitable-Membranes-Bertil-Hille/dp/ 0878933212 (accessed Jun 20, 2018)
[129]
Crill, W.E. Persistent sodium current in mammalian central neurons. Annu. Rev. Physiol., 1996, 58, 349-362.
[http://dx.doi.org/10.1146/annurev.ph.58.030196.002025] [PMID: 8815799]
[130]
Magistretti, J.; Ragsdale, D.S.; Alonso, A. High conductance sustained single-channel activity responsible for the low-threshold persistent Na(+) current in entorhinal cortex neurons. J. Neurosci., 1999, 19(17), 7334-7341.
[PMID: 10460240]
[131]
Mantegazza, M.; Curia, G.; Biagini, G.; Ragsdale, D.S.; Avoli, M. Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol., 2010, 9(4), 413-424.
[http://dx.doi.org/10.1016/S1474-4422(10)70059-4] [PMID: 20298965]
[132]
Kaplan, D.I.; Isom, L.L.; Petrou, S. Role of sodium channels in epilepsy. Cold Spring Harb. Perspect. Med., 2016, 6(6), a022814.
[http://dx.doi.org/10.1101/cshperspect.a022814] [PMID: 27143702]
[133]
Agrawal, N.; Alonso, A.; Ragsdale, D.S. Increased persistent sodium currents in rat entorhinal cortex layer V neurons in a post-status epilepticus model of temporal lobe epilepsy. Epilepsia, 2003, 44(12), 1601-1604.
[http://dx.doi.org/10.1111/j.0013-9580.2003. 23103.x] [PMID: 14636336]
[134]
Blumenfeld, H.; Lampert, A.; Klein, J.P.; Mission, J.; Chen, M.C.; Rivera, M.; Dib-Hajj, S.; Brennan, A.R.; Hains, B.C.; Waxman, S.G. Role of hippocampal sodium channel Nav1.6 in kindling epileptogenesis. Epilepsia, 2009, 50(1), 44-55.
[http://dx.doi.org/10. 1111/j.1528-1167.2008.01710.x] [PMID: 18637833]
[135]
Vreugdenhil, M.; Hoogland, G.; van Veelen, C.W.M.; Wadman, W.J. Persistent sodium current in subicular neurons isolated from patients with temporal lobe epilepsy. Eur. J. Neurosci., 2004, 19(10), 2769-2778.
[http://dx.doi.org/10.1111/j.1460-9568.2004. 03400.x] [PMID: 15147310]
[136]
Kearney, J.A.; Plummer, N.W.; Smith, M.R.; Kapur, J.; Cummins, T.R.; Waxman, S.G.; Goldin, A.L.; Meisler, M.H. A gain-of-function mutation in the sodium channel gene Scn2a results in seizures and behavioral abnormalities. Neuroscience, 2001, 102(2), 307-317.
[http://dx.doi.org/10.1016/S0306-4522(00)00479-6] [PMID: 11166117]
[137]
Stafstrom, C.E. Persistent sodium current and its role in epilepsy. Epilepsy Curr., 2007, 7(1), 15-22.
[http://dx.doi.org/10.1111/j.1535-7511.2007.00156.x] [PMID: 17304346]
[138]
Curia, G.; Longo, D.; Biagini, G.; Jones, R.S.G.; Avoli, M. The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods, 2008, 172(2), 143-157.
[http://dx.doi.org/10.1016/j.jneumeth. 2008.04.019] [PMID: 18550176]
[139]
Ragsdale, D.S.; Scheuer, T.; Catterall, W.A. Frequency and voltage-dependent inhibition of type IIA Na+ channels, expressed in a mammalian cell line, by local anesthetic, antiarrhythmic, and anticonvulsant drugs. Mol. Pharmacol., 1991, 40(5), 756-765.
[PMID: 1658608]
[140]
Poolos, N.P.; Migliore, M.; Johnston, D. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat. Neurosci., 2002, 5(8), 767-774.
[http://dx.doi.org/ 10.1038/nn891] [PMID: 12118259]
[141]
Poolos, N.P. Hyperpolarization-activated cyclic nucleotide-gated (HCN) ion channelopathy in epilepsy. Jasper’s basic mechanisms of the epilepsiesNoebels, J.; Avoli, M.; Rogawski, M.; Olsen, R.; Delgado-Escueta, A., Eds National center for biotechnology Information (US): Bethesda (MD), 2012.
[142]
Surges, R.; Freiman, T.M.; Feuerstein, T.J. Gabapentin increases the hyperpolarization-activated cation current Ih in rat CA1 pyramidal cells. Epilepsia, 2003, 44(2), 150-156.
[PMID: 12558567] [http://dx.doi.org/http://10.1046/j.1528-1157.2003.36802.x]
[143]
Stefani, A.; Spadoni, F.; Siniscalchi, A.; Bernardi, G. Lamotrigine inhibits Ca2+ currents in cortical neurons: functional implications. Eur. J. Pharmacol., 1996, 307(1), 113-116.
[PMID: 8831112] [http://dx.doi.org/http://10.1016/0014-2999(96)00265-8]
[144]
Catterall, W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol., 2011, 3(8), a003947.
[http://dx.doi.org/10.1101/cshperspect.a003947] [PMID: 21746798]
[145]
Lynch, B.A.; Lambeng, N.; Nocka, K.; Kensel-Hammes, P.; Bajjalieh, S.M.; Matagne, A.; Fuks, B. The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc. Natl. Acad. Sci. USA, 2004, 101(26), 9861-9866.
[http://dx.doi.org/10.1073/pnas.0308208101] [PMID: 15210974]
[146]
Vogl, C.; Mochida, S.; Wolff, C.; Whalley, B.J.; Stephens, G.J. The synaptic vesicle glycoprotein 2A ligand levetiracetam inhibits presynaptic Ca2+ channels through an intracellular pathway. Mol. Pharmacol., 2012, 82(2), 199-208.
[http://dx.doi.org/10.1124/mol. 111.076687] [PMID: 22554805]
[147]
Löscher, W.; Hönack, D.; Rundfeldt, C. Antiepileptogenic effects of the novel anticonvulsant levetiracetam (ucb L059) in the kindling model of temporal lobe epilepsy. J. Pharmacol. Exp. Ther., 1998, 284(2), 474-479.
[PMID: 9454787]
[148]
Vinogradova, L.V.; van Rijn, C.M. Anticonvulsive and antiepileptogenic effects of levetiracetam in the audiogenic kindling model. Epilepsia, 2008, 49(7), 1160-1168.
[http://dx.doi.org/10.1111/j.1528-1167.2008.01594.x] [PMID: 18397292]
[149]
Yan, H-D.; Ji-qun, C.; Ishihara, K.; Nagayama, T.; Serikawa, T.; Sasa, M. Separation of antiepileptogenic and antiseizure effects of levetiracetam in the spontaneously epileptic rat (SER). Epilepsia, 2005, 46(8), 1170-1177.
[http://dx.doi.org/10.1111/j.1528-1167. 2005.35204.x] [PMID: 16060925]
[150]
Sugaya, Y.; Maru, E.; Kudo, K.; Shibasaki, T.; Kato, N. Levetiracetam suppresses development of spontaneous EEG seizures and aberrant neurogenesis following kainate-induced status epilepticus. Brain Res., 2010, 1352, 187-199.
[http://dx.doi.org/ 10.1016/j.brainres.2010.06.061] [PMID: 20599805]
[151]
Lévesque, M.; Behr, C.; Avoli, M. The anti-ictogenic effects of levetiracetam are mirrored by interictal spiking and high-frequency oscillation changes in a model of temporal lobe epilepsy. Seizure, 2015, 25, 18-25.
[http://dx.doi.org/10.1016/j.seizure.2014.11.008] [PMID: 25645630]
[152]
Pisani, A.; Bonsi, P.; Martella, G.; De Persis, C.; Costa, C.; Pisani, F.; Bernardi, G.; Calabresi, P. Intracellular calcium increase in epileptiform activity: modulation by levetiracetam and lamotrigine. Epilepsia, 2004, 45(7), 719-728.
[http://dx.doi.org/10.1111/j.0013-9580.2004.02204.x] [PMID: 15230693]
[153]
Mazzocchetti, P.; Tantucci, M.; Bastioli, G.; Calabrese, V.; Di Filippo, M.; Tozzi, A.; Calabresi, P.; Costa, C. Lacosamide protects striatal and hippocampal neurons from in vitro ischemia without altering physiological synaptic plasticity. Neuropharmacology, 2018, 135, 424-430.
[http://dx.doi.org/10.1016/j.neuropharm.2018. 03.040] [PMID: 29614316]
[154]
Zona, C.; Tancredi, V.; Palma, E.; Pirrone, G.C.; Avoli, M. Potassium currents in rat cortical neurons in culture are enhanced by the antiepileptic drug carbamazepine. Can. J. Physiol. Pharmacol., 1990, 68(4), 545-547.
[http://dx.doi.org/10.1139/y90-079] [PMID: 2328457]
[155]
Zona, C.; Tancredi, V.; Longone, P.; D’Arcangelo, G.; D’Antuono, M.; Manfredi, M.; Avoli, M. Neocortical potassium currents are enhanced by the antiepileptic drug lamotrigine. Epilepsia, 2002, 43(7), 685-690.
[http://dx.doi.org/10.1046/j.1528-1157.2002. 51401.x] [PMID: 12102669]
[156]
Pumain, R.; Menini, C.; Heinemann, U.; Louvel, J.; Silva-Barrat, C. Chemical synaptic transmission is not necessary for epileptic seizures to persist in the baboon Papio papio. Exp. Neurol., 1985, 89(1), 250-258.
[http://dx.doi.org/10.1016/0014-4886(85)90280-8] [PMID: 2988992]
[157]
Bruzzone, R.; Hormuzdi, S.G.; Barbe, M.T.; Herb, A.; Monyer, H. Pannexins, a family of gap junction proteins expressed in brain. Proc. Natl. Acad. Sci. USA, 2003, 100(23), 13644-13649.
[http://dx.doi.org/10.1073/pnas.2233464100] [PMID: 14597722]
[158]
Söhl, G.; Maxeiner, S.; Willecke, K. Expression and functions of neuronal gap junctions. Nat. Rev. Neurosci., 2005, 6(3), 191-200.
[http://dx.doi.org/10.1038/nrn1627] [PMID: 15738956]
[159]
Dermietzel, R.; Spray, D.C. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci., 1993, 16(5), 186-192.
[http://dx.doi.org/10.1016/0166-2236(93)90151-B] [PMID: 7685944]
[160]
Bennett, M.V.L.; Zukin, R.S. Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron, 2004, 41(4), 495-511.
[http://dx.doi.org/10.1016/S0896-6273(04)00043-1] [PMID: 14980200]
[161]
Nakase, T.; Naus, C.C.G. Gap junctions and neurological disorders of the central nervous system. Biochim. Biophys. Acta, 2004, 1662(1-2), 149-158.
[http://dx.doi.org/10.1016/j.bbamem.2004.01. 009] [http://dx.doi.org/http://10.1016/j.bbamem.2004.01.009]
[162]
Mylvaganam, S.; Ramani, M.; Krawczyk, M.; Carlen, P.L. Roles of gap junctions, connexins, and pannexins in epilepsy. Front. Physiol., 2014, 5, 172.
[http://dx.doi.org/10.3389/fphys.2014.00172] [PMID: 24847276]
[163]
Draguhn, A.; Traub, R.D.; Schmitz, D.; Jefferys, J.G.R. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature, 1998, 394(6689), 189-192.
[http://dx.doi.org/10. 1038/28184] [PMID: 9671303]
[164]
Maier, N.; Güldenagel, M.; Söhl, G.; Siegmund, H.; Willecke, K.; Draguhn, A. Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J. Physiol., 2002, 541(Pt 2), 521-528.
[http://dx.doi.org/10.1113/jphysiol.2002.017624] [PMID: 12042356]
[165]
Simon, A.; Traub, R.D.; Vladimirov, N.; Jenkins, A.; Nicholson, C.; Whittaker, R.G.; Schofield, I.; Clowry, G.J.; Cunningham, M.O.; Whittington, M.A. Gap junction networks can generate both ripple-like and fast ripple-like oscillations. Eur. J. Neurosci., 2014, 39(1), 46-60.
[http://dx.doi.org/10.1111/ejn.12386] [PMID: 24118191]
[166]
Ventura-Mejia, C.; Medina-Ceja, L. Decreased fast ripples in the hippocampus of rats with spontaneous recurrent seizures treated with carbenoxolone and quinine. BioMed Res. Int., 2014, 2014, 282490.
[http://dx.doi.org/10.1155/2014/282490]
[167]
Carlen, P.L.; Skinner, F.; Zhang, L.; Naus, C.; Kushnir, M.; Perez Velazquez, J.L. The role of gap junctions in seizures. Brain Res. Brain Res. Rev., 2000, 32(1), 235-241.
[PMID: 10751673] [http://dx.doi.org/http://10.1016/S0165-0173(99)00084-3]
[168]
Naus, C.C.; Bechberger, J.F.; Paul, D.L. Gap junction gene expression in human seizure disorder. Exp. Neurol., 1991, 111(2), 198-203.
[http://dx.doi.org/10.1016/0014-4886(91)90007-Y] [PMID: 1846600]
[169]
Aronica, E.; Gorter, J.A.; Jansen, G.H.; Leenstra, S.; Yankaya, B.; Troost, D. Expression of connexin 43 and connexin 32 gap-junction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex. Acta Neuropathol., 2001, 101(5), 449-459.
[PMID: 11484816]
[170]
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. Effects of gap junction blockers on human neocortical synchronization. Neurobiol. Dis., 2006, 22(3), 496-508.
[http://dx.doi.org/10.1016/j.nbd.2005.12.011] [PMID: 16478664]
[171]
Kurata, Y.; Marszalec, W.; Yeh, J.Z.; Narahashi, T. Agonist and potentiation actions of n-octanol on gamma-aminobutyric acid type A receptors. Mol. Pharmacol., 1999, 55(6), 1011-1019.
[PMID: 10347242]
[172]
Vessey, J.P.; Lalonde, M.R.; Mizan, H.A.; Welch, N.C.; Kelly, M.E.M.; Barnes, S. Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina. J. Neurophysiol., 2004, 92(2), 1252-1256.
[http://dx.doi.org/10.1152/jn.00148.2004] [PMID: 15028741]