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Current Neuropharmacology

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ISSN (Online): 1875-6190

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Review Article

GABAB Receptors: are they Missing in Action in Focal Epilepsy Research?

Author(s): Massimo Avoli* and Maxime Lévesque

Volume 20, Issue 9, 2022

Published on: 30 March, 2022

Page: [1704 - 1716] Pages: 13

DOI: 10.2174/1570159X19666210823102332

Price: $65

Abstract

GABA, the key inhibitory neurotransmitter in the adult forebrain, activates pre- and postsynaptic receptors that have been categorized as GABAA, which directly open ligand-gated (or receptor-operated) ion-channels, and GABAB, which are metabotropic since they operate through second messengers. Over the last three decades, several studies have addressed the role of GABAB receptors in the pathophysiology of generalized and focal epileptic disorders. Here, we will address their involvement in focal epileptic disorders by mainly reviewing in vitro studies that have shown: (i) how either enhancing or decreasing GABAB receptor function can favour epileptiform synchronization and thus ictogenesis, although with different features; (ii) the surprising ability of GABAB receptor antagonism to disclose ictal-like activity when the excitatory ionotropic transmission is abolished; and (iii) their contribution to controlling seizure-like discharges during repetitive electrical stimuli delivered in limbic structures. In spite of this evidence, the role of GABAB receptor function in focal epileptic disorders has been attracting less interest when compared to the numerous studies that have addressed GABAA receptor signaling. Therefore, the main aim of our mini-review is to revive interest in the function of GABAB receptors in focal epilepsy research.

Keywords: GABAB receptor signaling, focal epileptic disorders, in vitro epileptiform synchronization, ictal discharges, interictal discharges, limbic structures.

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[1]
Bowery, N.; Enna, S.J.; Olsen, R.W. Six decades of GABA. Biochem. Pharmacol., 2004, 68(8), 1477-1478.
[http://dx.doi.org/10.1016/j.bcp.2004.07.033] [PMID: 15451389]
[2]
Craig, M.T.; McBain, C.J. The emerging role of GABAB receptors as regulators of network dynamics: fast actions from a ‘slow’ receptor? Curr. Opin. Neurobiol., 2014, 26, 15-21.
[http://dx.doi.org/10.1016/j.conb.2013.10.002] [PMID: 24650499]
[3]
Farrant, M.; Kaila, K. The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog. Brain Res., 2007, 160, 59-87.
[http://dx.doi.org/10.1016/S0079-6123(06)60005-8] [PMID: 17499109]
[4]
Frangaj, A.; Fan, Q. R. Structural biology of GABAB receptor. Neuropharmacology, 2018, 136(Pt A), 68-79.
[http://dx.doi.org/10.1016/j.neuropharm.2017.10.011]
[5]
Martin, D.L.; Olsen, R.W. GABA in the nervous system: The view at fifty years. J. Neurol. Sci., Availalble from: https://www.jns-journal.com/article/S0022-510X(01)00582-2/fulltext [Accessed 2021 -04 -30]
[6]
Bettler, B.; Kaupmann, K.; Mosbacher, J.; Gassmann, M. Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev., 2004, 84(3), 835-867.
[http://dx.doi.org/10.1152/physrev.00036.2003] [PMID: 15269338]
[7]
Evenseth, L.S.M.; Gabrielsen, M.; Sylte, I. The GABAB receptor-structure, ligand binding and drug development. Molecules, 2020, 25(13), E3093.
[http://dx.doi.org/10.3390/molecules25133093] [PMID: 32646032]
[8]
Rose, T.R.; Wickman, K. Mechanisms and regulation of neuronal GABAB receptor-dependent signaling. Curr. Top. Behav. Neurosci., 2020.
[http://dx.doi.org/10.1007/7854_2020_129] [PMID: 32808092]
[9]
Molony, C.J.; Parmelee, A.H. Convulsions in young infants as a result of pyridoxine (vitamin B6) deficiency. J. Am. Med. Assoc., 1954, 154(5), 405-406.
[http://dx.doi.org/10.1001/jama.1954.02940390029008] [PMID: 13117628]
[10]
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]
[11]
Krnjević, K. GABA mediated inhibitory mechanisms in relation to epileptic discharge. In: Basic mechanisms of neuronal hyperexcitability; Liss: New York, 1983, pp. 249-280.
[12]
Houser, C.R. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem. Res., 1991, 16(3), 295-308.
[http://dx.doi.org/10.1007/BF00966093] [PMID: 1780031]
[13]
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]
[14]
Elahian, B.; Lado, N.E.; Mankin, E.; Vangala, S.; Misra, A.; Moxon, K.; Fried, I.; Sharan, A.; Yeasin, M.; Staba, R.; Bragin, A.; Avoli, M.; Sperling, M.R.; Engel, J., Jr; Weiss, S.A. Low-voltage fast seizures in humans begin with increased interneuron firing. Ann. Neurol., 2018, 84(4), 588-600.
[http://dx.doi.org/10.1002/ana.25325] [PMID: 30179277]
[15]
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]
[16]
Magloire, V.; Cornford, J.; Lieb, A.; Kullmann, D.M.; Pavlov, I. KCC2 overexpression prevents the paradoxical seizure-promoting action of somatic inhibition. Nat. Commun., 2019, 10(1), 1225.
[http://dx.doi.org/10.1038/s41467-019-08933-4] [PMID: 30874549]
[17]
Neumann, A.R.; Raedt, R.; Steenland, H.W.; Sprengers, M.; Bzymek, K.; Navratilova, Z.; Mesina, L.; Xie, J.; Lapointe, V.; Kloosterman, F.; Vonck, K.; Boon, P.A.J.M.; Soltesz, I.; McNaughton, B.L.; Luczak, A. Involvement of fast-spiking cells in ictal sequences during spontaneous seizures in rats with chronic temporal lobe epilepsy. Brain, 2017, 140(9), 2355-2369.
[http://dx.doi.org/10.1093/brain/awx179] [PMID: 29050390]
[18]
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(2), 108-115.
[http://dx.doi.org/10.1016/j.tins.2004.11.011] [PMID: 15667934]
[19]
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. USA, 1997, 94(22), 12151-12156.
[http://dx.doi.org/10.1073/pnas.94.22.12151] [PMID: 9342378]
[20]
Müller, J.; Timmermann, A.; Henning, L.; Müller, H.; Steinhäuser, C.; Bedner, P. Astrocytic GABA accumulation in experimental temporal lobe epilepsy. Front. Neurol., 2020, 11, 614923.
[http://dx.doi.org/10.3389/fneur.2020.614923] [PMID: 33391173]
[21]
Avoli, M.; Louvel, J.; Drapeau, C.; Pumain, R.; Kurcewicz, I. GABAA-mediated inhibition and in vitro epileptogenesis in the human neocortex. J. Neurophysiol., 1995, 73(2), 468-484.
[http://dx.doi.org/10.1152/jn.1995.73.2.468] [PMID: 7760112]
[22]
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(7), 2562-2574.
[http://dx.doi.org/10.1523/JNEUROSCI.09-07-02562.1989] [PMID: 2501460]
[23]
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(37), 9866-9873.
[http://dx.doi.org/10.1523/JNEUROSCI.2761-07.2007] [PMID: 17855601]
[24]
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]
[25]
Cǎlin, A.; Stancu, M.; Zagrean, A-M.; Jefferys, J.G.R.; Ilie, A.S.; Akerman, C.J. Chemogenetic recruitment of specific interneurons suppresses seizure activity. Front. Cell. Neurosci., 2018, 12, 293.
[http://dx.doi.org/10.3389/fncel.2018.00293] [PMID: 30233328]
[26]
Krook-Magnuson, E.; Armstrong, C.; Oijala, M.; Soltesz, I. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat. Commun., 2013, 4, 1376.
[http://dx.doi.org/10.1038/ncomms2376] [PMID: 23340416]
[27]
Lévesque, M.; Chen, L-Y.; Etter, G.; Shiri, Z.; Wang, S.; Williams, S.; Avoli, M. Paradoxical effects of optogenetic stimulation in mesial temporal lobe epilepsy. Ann. Neurol., 2019, 86(5), 714-728.
[http://dx.doi.org/10.1002/ana.25572] [PMID: 31393618]
[28]
Shiri, Z.; Manseau, F.; Lévesque, M.; Williams, S.; Avoli, M. Activation of specific neuronal networks leads to different seizure onset types. Ann. Neurol., 2016, 79(3), 354-365.
[http://dx.doi.org/10.1002/ana.24570] [PMID: 26605509]
[29]
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]
[30]
Kaila, K.; Price, T.J.; Payne, J.A.; Puskarjov, M.; Voipio, J. Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat. Rev. Neurosci., 2014, 15(10), 637-654.
[http://dx.doi.org/10.1038/nrn3819] [PMID: 25234263]
[31]
Connelly, W.M.; Fyson, S.J.; Errington, A.C.; McCafferty, C.P.; Cope, D.W.; Di Giovanni, G.; Crunelli, V. GABAB receptors regulate extrasynaptic gabaa receptors. J. Neurosci., 2013, 33(9), 3780-3785.
[http://dx.doi.org/10.1523/JNEUROSCI.4989-12.2013] [PMID: 23447590]
[32]
Vertkin, I.; Styr, B.; Slomowitz, E.; Ofir, N.; Shapira, I.; Berner, D.; Fedorova, T.; Laviv, T.; Barak-Broner, N.; Greitzer-Antes, D.; Gassmann, M.; Bettler, B.; Lotan, I.; Slutsky, I. GABAB receptor deficiency causes failure of neuronal homeostasis in hippocampal networks. Proc. Natl. Acad. Sci. USA, 2015, 112(25), E3291-E3299.
[http://dx.doi.org/10.1073/pnas.1424810112] [PMID: 26056260]
[33]
Vigot, R.; Barbieri, S.; Bräuner-Osborne, H.; Turecek, R.; Shigemoto, R.; Zhang, Y-P.; Luján, R.; Jacobson, L.H.; Biermann, B.; Fritschy, J-M.; Vacher, C-M.; Müller, M.; Sansig, G.; Guetg, N.; Cryan, J.F.; Kaupmann, K.; Gassmann, M.; Oertner, T.G.; Bettler, B. Differential compartmentalization and distinct functions of GABAB receptor variants. Neuron, 2006, 50(4), 589-601.
[http://dx.doi.org/10.1016/j.neuron.2006.04.014] [PMID: 16701209]
[34]
Andrade, R.; Malenka, R.C.; Nicoll, R.A.A.A. G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science, 1986, 234(4781), 1261-1265.
[http://dx.doi.org/10.1126/science.2430334] [PMID: 2430334]
[35]
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(5), 1441-1454.
[http://dx.doi.org/10.1152/jn.1991.66.5.1441] [PMID: 1684988]
[36]
Newberry, N.R.; Nicoll, R.A. Comparison of the action of baclofen with gamma-aminobutyric acid on rat hippocampal pyramidal cells in vitro. J. Physiol., 1985, 360, 161-185.
[http://dx.doi.org/10.1113/jphysiol.1985.sp015610] [PMID: 3989713]
[37]
Davies, C.H.; Davies, S.N.; Collingridge, G.L. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol., 1990, 424, 513-531.
[http://dx.doi.org/10.1113/jphysiol.1990.sp018080] [PMID: 2167975]
[38]
Davies, C.H.; Collingridge, G.L. The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. J. Physiol., 1993, 472, 245-265.
[http://dx.doi.org/10.1113/jphysiol.1993.sp019945] [PMID: 8145143]
[39]
Harrison, N.L. On the presynaptic action of baclofen at inhibitory synapses between cultured rat hippocampal neurones. J. Physiol., 1990, 422, 433-446.
[http://dx.doi.org/10.1113/jphysiol.1990.sp017993] [PMID: 2352187]
[40]
Scholz, K.P.; Miller, R.J. GABAB receptor-mediated inhibition of Ca2+ currents and synaptic transmission in cultured rat hippocampal neurones. J. Physiol., 1991, 444, 669-686.
[http://dx.doi.org/10.1113/jphysiol.1991.sp018900] [PMID: 1668352]
[41]
Jones, K.A.; Borowsky, B.; Tamm, J.A.; Craig, D.A.; Durkin, M.M.; Dai, M.; Yao, W.J.; Johnson, M.; Gunwaldsen, C.; Huang, L.Y.; Tang, C.; Shen, Q.; Salon, J.A.; Morse, K.; Laz, T.; Smith, K.E.; Nagarathnam, D.; Noble, S.A.; Branchek, T.A.; Gerald, C. GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature, 1998, 396(6712), 674-679.
[http://dx.doi.org/10.1038/25348] [PMID: 9872315]
[42]
Kaupmann, K.; Malitschek, B.; Schuler, V.; Heid, J.; Froestl, W.; Beck, P.; Mosbacher, J.; Bischoff, S.; Kulik, A.; Shigemoto, R.; Karschin, A.; Bettler, B. GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature, 1998, 396(6712), 683-687.
[http://dx.doi.org/10.1038/25360] [PMID: 9872317]
[43]
Kaupmann, K.; Huggel, K.; Heid, J.; Flor, P.J.; Bischoff, S.; Mickel, S.J.; McMaster, G.; Angst, C.; Bittiger, H.; Froestl, W.; Bettler, B. Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature, 1997, 386(6622), 239-246.
[http://dx.doi.org/10.1038/386239a0] [PMID: 9069281]
[44]
Prosser, H.M.; Gill, C.H.; Hirst, W.D.; Grau, E.; Robbins, M.; Calver, A.; Soffin, E.M.; Farmer, C.E.; Lanneau, C.; Gray, J.; Schenck, E.; Warmerdam, B.S.; Clapham, C.; Reavill, C.; Rogers, D.C.; Stean, T.; Upton, N.; Humphreys, K.; Randall, A.; Geppert, M.; Davies, C.H.; Pangalos, M.N. Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice. Mol. Cell. Neurosci., 2001, 17(6), 1059-1070.
[http://dx.doi.org/10.1006/mcne.2001.0995] [PMID: 11414794]
[45]
Schuler, V.; Lüscher, C.; Blanchet, C.; Klix, N.; Sansig, G.; Klebs, K.; Schmutz, M.; Heid, J.; Gentry, C.; Urban, L.; Fox, A.; Spooren, W.; Jaton, A.L.; Vigouret, J.; Pozza, M.; Kelly, P.H.; Mosbacher, J.; Froestl, W.; Käslin, E.; Korn, R.; Bischoff, S.; Kaupmann, K.; van der Putten, H.; Bettler, B. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron, 2001, 31(1), 47-58.
[http://dx.doi.org/10.1016/S0896-6273(01)00345-2] [PMID: 11498050]
[46]
Bowery, N.G.; Parry, K.; Boehrer, A.; Mathivet, P.; Marescaux, C.; Bernasconi, R. Pertussis toxin decreases absence seizures and GABA(B) receptor binding in thalamus of a genetically prone rat (GAERS). Neuropharmacology, 1999, 38(11), 1691-1697.
[http://dx.doi.org/10.1016/S0028-3908(99)00118-5] [PMID: 10587085]
[47]
Han, H.A.; Cortez, M.A.; Snead, O.C. GABAB receptor and absence epilepsy. In: Jasper’s basic mechanisms of the epilepsies; Noebels, J. L.; Avoli, M.; Rogawski, M. A.; Olsen, R. W.; Delgado- Escueta, A. V., Eds.; National Center for Biotechnology Information (US): Bethesda (MD), 2012.
[http://dx.doi.org/10.1093/med/9780199746545.003.0019]
[48]
Liu, Z.; Vergnes, M.; Depaulis, A.; Marescaux, C. Involvement of intrathalamic GABAB neurotransmission in the control of absence seizures in the rat. Neuroscience, 1992, 48(1), 87-93.
[http://dx.doi.org/10.1016/0306-4522(92)90340-8] [PMID: 1316571]
[49]
Dugladze, T.; Maziashvili, N.; Börgers, C.; Gurgenidze, S.; Häussler, U.; Winkelmann, A.; Haas, C.A.; Meier, J.C.; Vida, I.; Kopell, N.J.; Gloveli, T. GABA(B) autoreceptor-mediated cell type-specific reduction of inhibition in epileptic mice. Proc. Natl. Acad. Sci. USA, 2013, 110(37), 15073-15078.
[http://dx.doi.org/10.1073/pnas.1313505110] [PMID: 23980149]
[50]
Straessle, A.; Loup, F.; Arabadzisz, D.; Ohning, G.V.; Fritschy, J-M. Rapid and long-term alterations of hippocampal GABAB receptors in a mouse model of temporal lobe epilepsy. Eur. J. Neurosci., 2003, 18(8), 2213-2226.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02964.x] [PMID: 14622182]
[51]
Swartzwelder, H.S.; Lewis, D.V.; Anderson, W.W.; Wilson, W.A. Seizure-like events in brain slices: suppression by interictal activity. Brain Res., 1987, 410(2), 362-366.
[http://dx.doi.org/10.1016/0006-8993(87)90339-8] [PMID: 3594246]
[52]
Misgeld, U.; Bijak, M.; Jarolimek, W. A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog. Neurobiol., 1995, 46(4), 423-462.
[http://dx.doi.org/10.1016/0301-0082(95)00012-K] [PMID: 8532848]
[53]
Jones, R.S. Ictal epileptiform events induced by removal of extracellular magnesium in slices of entorhinal cortex are blocked by baclofen. Exp. Neurol., 1989, 104(2), 155-161.
[http://dx.doi.org/10.1016/S0014-4886(89)80009-3] [PMID: 2651139]
[54]
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]
[55]
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.
[http://dx.doi.org/10.1111/j.1476-5381.1993.tb12884.x] [PMID: 8467367]
[56]
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]
[57]
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]
[58]
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(3), 1018-1029.
[http://dx.doi.org/10.1152/jn.1993.70.3.1018] [PMID: 7901344]
[59]
Gerrard, L.B.; Tantirigama, M.L.S.; Bekkers, J.M. Pre- and postsynaptic activation of GABAB receptors modulates principal cell excitation in the piriform cortex. Front. Cell. Neurosci., 2018, 12, 28.
[http://dx.doi.org/10.3389/fncel.2018.00028] [PMID: 29459821]
[60]
Barbarosie, M.; Louvel, J.; D’Antuono, M.; Kurcewicz, I.; Avoli, M. Masking synchronous GABA-mediated potentials controls limbic seizures. Epilepsia, 2002, 43(12), 1469-1479.
[http://dx.doi.org/10.1046/j.1528-1157.2002.17402.x] [PMID: 12460247]
[61]
Barbarosie, M.; Avoli, M. CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J. Neurosci., 1997, 17(23), 9308-9314.
[http://dx.doi.org/10.1523/JNEUROSCI.17-23-09308.1997] [PMID: 9364076]
[62]
Avoli, M.; Benini, R.; de Guzman, P.; Omar, A. GABA(B) receptor activation and limbic network ictogenesis. Neuropharmacology, 2004, 46(1), 43-51.
[http://dx.doi.org/10.1016/S0028-3908(03)00307-1] [PMID: 14654096]
[63]
Van Rijn, C.M.; Van Berlo, M.J.; Feenstra, M.G.; Schoofs, M.L.; Hommes, O.R.R.R. (-)-baclofen: focal epilepsy after intracortical administration in the rat. Epilepsy Res., 1987, 1(6), 321-327.
[http://dx.doi.org/10.1016/0920-1211(87)90056-8] [PMID: 3143555]
[64]
Kofler, M.; Kronenberg, M.F.; Rifici, C.; Saltuari, L.; Bauer, G. Epileptic seizures associated with intrathecal baclofen application. Neurology, 1994, 44(1), 25-27.
[http://dx.doi.org/10.1212/WNL.44.1.25] [PMID: 8290085]
[65]
Rolland, B.; Deheul, S.; Danel, T.; Bordet, R.; Cottencin, O. A case of de novo seizures following a probable interaction of high-dose baclofen with alcohol. Alcohol Alcohol., 2012, 47(5), 577-580.
[http://dx.doi.org/10.1093/alcalc/ags076] [PMID: 22753796]
[66]
Rush, J.M.; Gibberd, F.B. Baclofen-induced epilepsy. J. R. Soc. Med., 1990, 83(2), 115-116.
[http://dx.doi.org/10.1177/014107689008300220] [PMID: 2319536]
[67]
Schuele, S.U.; Kellinghaus, C.; Shook, S.J.; Boulis, N.; Bethoux, F.A.; Loddenkemper, T. Incidence of seizures in patients with multiple sclerosis treated with intrathecal baclofen. Neurology, 2005, 64(6), 1086-1087.
[http://dx.doi.org/10.1212/01.WNL.0000154639.35941.21] [PMID: 15781838]
[68]
Olpe, H.R.; Karlsson, G.; Pozza, M.F.; Brugger, F.; Steinmann, M.; Van Riezen, H.; Fagg, G.; Hall, R.G.; Froestl, W.; Bittiger, H. CGP 35348: a centrally active blocker of GABAB receptors. Eur. J. Pharmacol., 1990, 187(1), 27-38.
[http://dx.doi.org/10.1016/0014-2999(90)90337-6] [PMID: 2176979]
[69]
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]
[70]
Thuault, S.J.; Brown, J.T.; Calver, A.R.; Collingridge, G.L.; Randall, A.; Davies, C.H. Mechanisms contributing to the exacerbated epileptiform activity in hippocampal slices expressing a C-terminal truncated GABA(B2) receptor subunit. Epilepsy Res., 2005, 65(1-2), 41-51.
[http://dx.doi.org/10.1016/j.eplepsyres.2005.04.004] [PMID: 15979855]
[71]
Karlsson, G.; Kolb, C.; Hausdorf, A.; Portet, C.; Schmutz, M.; Olpe, H.R. GABAB receptors in various in vitro and in vivo models of epilepsy: a study with the GABAB receptor blocker CGP 35348. Neuroscience, 1992, 47(1), 63-68.
[http://dx.doi.org/10.1016/0306-4522(92)90120-Q] [PMID: 1315938]
[72]
McCormick, D.A. GABA as an inhibitory neurotransmitter in human cerebral cortex. J. Neurophysiol., 1989, 62(5), 1018-1027.
[http://dx.doi.org/10.1152/jn.1989.62.5.1018] [PMID: 2573696]
[73]
Scanziani, M.; Debanne, D.; Müller, M.; Gähwiler, B.H.; Thompson, S.M. Role of excitatory amino acid and GABAB receptors in the generation of epileptiform activity in disinhibited hippocampal slice cultures. Neuroscience, 1994, 61(4), 823-832.
[http://dx.doi.org/10.1016/0306-4522(94)90405-7] [PMID: 7838381]
[74]
Sutor, B.; Luhmann, H.J. Involvement of GABA(B) receptors in convulsant-induced epileptiform activity in rat neocortex in vitro. Eur. J. Neurosci., 1998, 10(11), 3417-3427.
[http://dx.doi.org/10.1046/j.1460-9568.1998.00351.x] [PMID: 9824455]
[75]
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.
[http://dx.doi.org/10.1016/S0028-3908(02)00156-9] [PMID: 12367602]
[76]
Ainsworth, M.; Lee, S.; Kaiser, M.; Simonotto, J.; Kopell, N.J.; Whittington, M.A. GABAB receptor-mediated, layer-specific synaptic plasticity reorganizes gamma-frequency neocortical response to stimulation. Proc. Natl. Acad. Sci. USA, 2016, 113(19), E2721-E2729.
[http://dx.doi.org/10.1073/pnas.1605243113] [PMID: 27118845]
[77]
Orts-Del’Immagine, A.; Pugh, J.R. Activity-dependent plasticity of presynaptic GABAB receptors at parallel fiber synapses. Synapse, 2018, 72(5), e22027.
[http://dx.doi.org/10.1002/syn.22027] [PMID: 29360168]
[78]
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]
[79]
Levinson, S.; Tran, C.H.; Barry, J.; Viker, B.; Levine, M.S.; Vinters, H.V.; Mathern, G.W.; Cepeda, C. Paroxysmal discharges in tissue slices from pediatric epilepsy surgery patients: Critical role of GABAB receptors in the generation of ictal activity. Front. Cell. Neurosci., 2020, 14, 54.
[http://dx.doi.org/10.3389/fncel.2020.00054] [PMID: 32265658]
[80]
Billinton, A.; Baird, V.H.; Thom, M.; Duncan, J.S.; Upton, N.; Bowery, N.G. GABA(B) receptor autoradiography in hippocampal sclerosis associated with human temporal lobe epilepsy. Br. J. Pharmacol., 2001, 132(2), 475-480.
[http://dx.doi.org/10.1038/sj.bjp.0703854] [PMID: 11159697]
[81]
Billinton, A.; Baird, V.H.; Thom, M.; Duncan, J.S.; Upton, N.; Bowery, N.G. GABA(B(1)) mRNA expression in hippocampal sclerosis associated with human temporal lobe epilepsy. Brain Res. Mol. Brain Res., 2001, 86(1-2), 84-89.
[http://dx.doi.org/10.1016/S0169-328X(00)00271-0] [PMID: 11165375]
[82]
Muñoz, A.; Arellano, J.I.; DeFelipe, J. GABABR1 receptor protein expression in human mesial temporal cortex: changes in temporal lobe epilepsy. J. Comp. Neurol., 2002, 449(2), 166-179.
[http://dx.doi.org/10.1002/cne.10287] [PMID: 12115687]
[83]
Princivalle, A.P.; Duncan, J.S.; Thom, M.; Bowery, N.G. GABA(B1a), GABA(B1b) AND GABA(B2) mRNA variants expression in hippocampus resected from patients with temporal lobe epilepsy. Neuroscience, 2003, 122(4), 975-984.
[http://dx.doi.org/10.1016/j.neuroscience.2003.08.044] [PMID: 14643764]
[84]
Deisz, R.A. GABA(B) receptor-mediated effects in human and rat neocortical neurones in vitro. Neuropharmacology, 1999, 38(11), 1755-1766.
[http://dx.doi.org/10.1016/S0028-3908(99)00136-7] [PMID: 10587091]
[85]
Teichgräber, L.A.; Lehmann, T-N.; Meencke, H-J.; Weiss, T.; Nitsch, R.; Deisz, R.A. Impaired function of GABA(B) receptors in tissues from pharmacoresistant epilepsy patients. Epilepsia, 2009, 50(7), 1697-1716.
[http://dx.doi.org/10.1111/j.1528-1167.2009.02094.x] [PMID: 19453710]
[86]
Buhl, E.H.; Otis, T.S.; Mody, I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science, 1996, 271(5247), 369-373.
[http://dx.doi.org/10.1126/science.271.5247.369] [PMID: 8553076]
[87]
Haas, K.Z.; Sperber, E.F.; Moshé, S.L.; Stanton, P.K. Kainic acid-induced seizures enhance dentate gyrus inhibition by downregulation of GABA(B) receptors. J. Neurosci., 1996, 16(13), 4250-4260.
[http://dx.doi.org/10.1523/JNEUROSCI.16-13-04250.1996] [PMID: 8753886]
[88]
Asprodini, E.K.; Rainnie, D.G.; Shinnick-Gallagher, P. Epileptogenesis reduces the sensitivity of presynaptic gamma-aminobutyric acidB receptors on glutamatergic afferents in the amygdala. J. Pharmacol. Exp. Ther., 1992, 262(3), 1011-1021.
[PMID: 1326620]
[89]
Wu, C.; Leung, L.S. Partial hippocampal kindling decreases efficacy of presynaptic GABAB autoreceptors in CA1. J. Neurosci., 1997, 17(23), 9261-9269.
[http://dx.doi.org/10.1523/JNEUROSCI.17-23-09261.1997] [PMID: 9364072]
[90]
Mangan, P.S.; Lothman, E.W. Profound disturbances of pre- and postsynaptic GABAB-receptor-mediated processes in region CA1 in a chronic model of temporal lobe epilepsy. J. Neurophysiol., 1996, 76(2), 1282-1296.
[http://dx.doi.org/10.1152/jn.1996.76.2.1282] [PMID: 8871236]
[91]
Chandler, K.E.; Princivalle, A.P.; Fabian-Fine, R.; Bowery, N.G.; Kullmann, D.M.; Walker, M.C. Plasticity of GABA(B) receptor-mediated heterosynaptic interactions at mossy fibers after status epilepticus. J. Neurosci., 2003, 23(36), 11382-11391.
[http://dx.doi.org/10.1523/JNEUROSCI.23-36-11382.2003] [PMID: 14673002]
[92]
de Curtis, M.; Avanzini, G. Interictal spikes in focal epileptogenesis. Prog. Neurobiol., 2001, 63(5), 541-567.
[http://dx.doi.org/10.1016/S0301-0082(00)00026-5] [PMID: 11164621]
[93]
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]
[94]
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]
[95]
Schiller, Y.; Bankirer, Y. Cellular mechanisms underlying antiepileptic effects of low- and high-frequency electrical stimulation in acute epilepsy in neocortical brain slices in vitro. J. Neurophysiol., 2007, 97(3), 1887-1902.
[http://dx.doi.org/10.1152/jn.00514.2006] [PMID: 17151229]
[96]
Tang, Y.; Durand, D.M. A novel electrical stimulation paradigm for the suppression of epileptiform activity in an in vivo model of mesial temporal lobe status epilepticus. Int. J. Neural Syst., 2012, 22(3), 1250006.
[http://dx.doi.org/10.1142/S0129065712500062] [PMID: 23627622]
[97]
Paschen, E.; Elgueta, C.; Heining, K.; Vieira, D.M.; Kleis, P.; Orcinha, C.; Häussler, U.; Bartos, M.; Egert, U.; Janz, P.; Haas, C.A. Hippocampal low-frequency stimulation prevents seizure generation in a mouse model of mesial temporal lobe epilepsy. eLife, 2020, 9, e54518.
[http://dx.doi.org/10.7554/eLife.54518] [PMID: 33349333]
[98]
Koubeissi, M.Z.; Kahriman, E.; Syed, T.U.; Miller, J.; Durand, D.M. Low-frequency electrical stimulation of a fiber tract in temporal lobe epilepsy. Ann. Neurol., 2013, 74(2), 223-231.
[http://dx.doi.org/10.1002/ana.23915] [PMID: 23613463]
[99]
Tergau, F.; Naumann, U.; Paulus, W.; Steinhoff, B.J. Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet, 1999, 353(9171), 2209.
[http://dx.doi.org/10.1016/S0140-6736(99)01301-X] [PMID: 10392988]
[100]
Theodore, W.H.; Fisher, R.S. Brain stimulation for epilepsy. Lancet Neurol., 2004, 3(2), 111-118.
[http://dx.doi.org/10.1016/S1474-4422(03)00664-1] [PMID: 14747003]
[101]
Toprani, S.; Durand, D.M. Long-lasting hyperpolarization underlies seizure reduction by low frequency deep brain electrical stimulation. J. Physiol., 2013, 591(22), 5765-5790.
[http://dx.doi.org/10.1113/jphysiol.2013.253757] [PMID: 23981713]
[102]
Kano, T.; Inaba, Y.; D’Antuono, M.; Biagini, G.; Lévesque, M.; Avoli, M. Blockade of in vitro ictogenesis by low frequency stimulation coincides with increased epileptiform response latency. J. Neurophysiol., 2015.
[http://dx.doi.org/10.1152/jn.00248.2015]
[103]
Smirnova, E.Y.; Chizhov, A.V.; Zaitsev, A.V. Presynaptic GABAB receptors underlie the antiepileptic effect of low-frequency electrical stimulation in the 4-aminopyridine model of epilepsy in brain slices of young rats. Brain Stimul., 2020, 13(5), 1387-1395.
[http://dx.doi.org/10.1016/j.brs.2020.07.013] [PMID: 32717394]
[104]
Gomez, C.D.; Acharjee, S.; Lewis, M.L.; Read, J.; Pittman, Q.J. Increased excitatory synaptic transmission associated with adult seizure vulnerability induced by early-life inflammation in mice. J. Neurosci., 2021, 41(20), 4367-4377.
[http://dx.doi.org/10.1523/JNEUROSCI.2667-20.2021] [PMID: 33827934]
[105]
Pagès, N.; Maurois, P.; Bac, P.; Meza-Toledo, S.; Peralta-Cruz, J.; Chamorro-Cevallos, G.; Cristóbal-Luna, J.M.; Vamecq, J. Anticonvulsive profile of two GABAB receptor antagonists on acute seizure mice models. Epilepsy Res., 2021, 174, 106644.
[http://dx.doi.org/10.1016/j.eplepsyres.2021.106644] [PMID: 33932748]
[106]
Augier, E. Recent advances in the potential of positive allosteric modulators of the GABAB receptor to treat alcohol use disorder. Alcohol Alcohol., 2021, 56(2), 139-148.
[http://dx.doi.org/10.1093/alcalc/agab003] [PMID: 33561865]
[107]
Augier, E.; Dulman, R.S.; Damadzic, R.; Pilling, A.; Hamilton, J.P.; Heilig, M. The GABAB positive allosteric modulator ADX71441 attenuates alcohol self-administration and relapse to alcohol seeking in rats. Neuropsychopharmacology, 2017, 42(9), 1789-1799.
[http://dx.doi.org/10.1038/npp.2017.53] [PMID: 28294133]
[108]
Fatemi, S.H.; Folsom, T.D.; Thuras, P.D. GABAA and GABAB receptor dysregulation in superior frontal cortex of subjects with schizophrenia and bipolar disorder. Synapse, 2017, 71(7)
[http://dx.doi.org/10.1002/syn.21973] [PMID: 28316115]
[109]
Heaney, C.F.; Kinney, J.W. Role of GABA(B) receptors in learning and memory and neurological disorders. Neurosci. Biobehav. Rev., 2016, 63, 1-28.
[http://dx.doi.org/10.1016/j.neubiorev.2016.01.007] [PMID: 26814961]
[110]
Pizzo, R.; O’Leary, O. F.; Cryan, J. F. Elucidation of the neural circuits activated by a gabab receptor positive modulator: Relevance to anxiety. Neuropharmacology, 2018, 136(Pt A), 129-145.
[http://dx.doi.org/10.1016/j.neuropharm.2017.07.021]

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