Spontaneous epileptiform activity mediated by GABAA receptors and gap junctions in the rat hippocampal slice following long-term exposure to GABAB antagonists

Neuropharmacology

Volumn 43, Issue 4, 2002, Pages 563-572

  Uusisaari, Marylka ^a   Smirnov, Sergei ^a   Voipio, Juha ^a   Kaila, Kai ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Carbonic anhydrase; GABAB receptors; Gap junctions; Hypersynchrony; Nonsynaptic; Quinine

Indexed keywords

2 AMINO 4 PHOSPHONOBUTYRIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; BACLOFEN; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; CARBONATE DEHYDRATASE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; OCTANOL; POTASSIUM ION; QUINIDINE; QUININE;

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; DOWN REGULATION; EPILEPTIC DISCHARGE; FEMALE; GAP JUNCTION; HIPPOCAMPUS; HYPERPOLARIZATION; LONG TERM EXPOSURE; MALE; NEUROTOXICITY; NONHUMAN; PH; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; CARBONIC ANHYDRASE INHIBITORS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EPILEPSY; FEMALE; GABA ANTAGONISTS; GAP JUNCTIONS; HIPPOCAMPUS; HYDROGEN-ION CONCENTRATION; INTERNEURONS; MALE; MEMBRANE POTENTIALS; ORGANOPHOSPHORUS COMPOUNDS; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PROPANOLAMINES; QUINOXALINES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B;

EID: 0036753760     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(02)00156-9     Document Type: Article

References (75)

1. Aram J.A., Lodge D. Epileptiform activity induced by alkalosis in rat neocortical slices: block by antagonists of N-methyl-D-aspartate. Neuroscience Letters. 83:1987;345-350.
2. Ault B., Nadler J.V. Anticonvulsant-like actions of baclofen in the rat hippocampal slice. British Journal of Pharmacology. 78:1983;701-708.
3. Avoli M. GABA-mediated synchronous potentials and seizure generation. Epilepsia. 37:1996;1035-1042.
4. Buhl E.H., Otis T.S., Mody I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science. 271:1996;369-373.
5. Bracci E., Vreugdenhil M., Hack S.P., Jefferys J.G. On the synchronizing mechanisms of tetanically induced hippocampal oscillations. Journal of Neuroscience. 19:1999;8104-8113.
6. Busa W.B., Nuccitelli R. Metabolic regulation via intracellular pH. American Journal of Physiology. 246:1984;R409-R438.
7. Capogna M., Gahwiler B.H., Thompson S.M. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. Journal of Physiology. 470:1993;539-558.
8. Chen K., Aradi I., Thon N., Eghbal-Ahmadi M., Baram T.Z., Soltesz I. Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nature Medicine. 7:2001;331-337.
9. Cobb S.R., Manuel N.A., Morton R.A., Gill C.H., Collingridge G.L., Davies C.H. Regulation of depolarizing GABAa receptor-mediated synaptic potentials by synaptic activation of GABAb autoreceptors in the rat hippocampus. Neuropharmacology. 38:1999;1723-1732.
10. Cohen G.A., Doze V.A., Madison D.V. Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron. 9:1992;325-335.
11. Cohen I., Miles R. Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus. Journal of Physiology Pt 2. 524:2000;485-502.
12. 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. Nature Neuroscience. 4:2001;52-62.
13. Dalby N.O., Mody I. The process of epileptogenesis: a pathophysiological approach. Current Opinion in Neurology. 14:2001;187-192.
14. Davies C.H., Collingridge G.L. The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. Journal of Physiology (London). 472:1993;245-265.
15. de Curtis M., Avanzini G. Interictal spikes in focal epileptogenesis. Progress in Neurobiology. 63:2001;541-567.
16. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron. 31:2001;477-485.
17. Galarreta M., Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature. 402:1999;72-75.
18. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 402:1999;75-79.
19. A receptor-mediated responses in pyramidal cells of rat hippocampus. Journal of Neurophysiology. 69:1993;1541-1555.
20. Gulyas A.I., Sik A., Payne J.A., Kaila K., Freund T.F. The KCl cotransporter KCC2 is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. European Journal of Neuroscience. 13:2001;2205-2217.
21. Heinemann U., Stabel J., Rausche G. Activity-dependent ionic changes and neuronal plasticity in rat hippocampus. Progress in Brain Research. 83:1990;197-214.
22. Herrero A.I., Del Olmo N., Gonzalez-Escalada J.R., Solis J.M. Two new actions of topiramate: inhibition of depolarizing GABA(A)-mediated responses and activation of a potassium conductance. Neuropharmacology. 42:2002;210-220.
23. Higashima M., Kinoshita H., Yamaguchi N., Koshino Y. Activation of GABAergic function necessary for after-discharge generation in rat hippocampal slices. Neuroscience Letters. 207:1996;101-104.
24. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.H., Whittington M.A., Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron. 31:2001;487-495.
25. Jefferys J.G. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiological Reviews. 75:1995;689-723.
26. Jefferys J.G., Traub R.D. Electrophysiological substrates for focal epilepsies. Progress in Brain Research. 116:1998;351-358.
27. Jensen K., Jensen M.S., Lambert J.D. Post-tetanic potentiation of GABAergic IPSCs in cultured rat hippocampal neurones. Journal of Physiology Pt 1. 519:1999;71-84.
28. Jensen M.S., Cherubini E., Yaari Y. Opponent effects of potassium on GABAA-mediated postsynaptic inhibition in the rat hippocampus. Journal of Neurophysiology. 69:1993;764-771.
29. Jensen M.S., Yaari Y. The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Annals of Neurology. 24:1988;591-598.
30. Kaila K., Lamsa K., Smirnov S., Taira T., Voipio J. Long-lasting GABA-mediated depolarization evoked by high-frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K+ transient. Journal of Neuroscience. 17:1997;7662-7672.
31. Katona I., Sperlágh B., Sík A., Käfalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. Journal of Neuroscience. 19:1999;4544-4558.
32. Köhling R., Schmidinger A., Hülsmann S., Vanhatalo S., Lücke A., Straub H., Speckmann E.J., Tuxhorn I., Wolf P., Lahl R., Pannek H., Oppel F., Greiner C., Moskopp D., Wassmann H. Anoxic terminal negative DC-shift in human neocortical slices in vitro. Brain Research. 741:1996;174-179.
33. Lamsa K., Kaila K. Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. Journal of Neurophysiology. 78:1997;2582-2591.
34. LeBeau, F.E., Towers, S.K., Traub, R.D., Whittington, M.A., Buhl, E.H., 2002. Transient fast hippocampal network oscillations in vitro by potassium transients. Journal of Physiology, in press.
35. Maier, N., Güldenagel, M, Söhl, G, Siegmund, H., Willecke, K, Draguhn, A., 2002. Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. Journal of Physiology, in press.
36. B-receptor-mediated processes in region CA1 in a chronic model of temporal lobe epilepsy. Journal of Neurophysiology. 76:1996;1282-1296.
37. Manuel N.A., Davies C.H. Pharmacological modulation of GABA(A) receptor-mediated postsynaptic potentials in the CA1 region of the rat hippocampus. British Journal of Pharmacology. 125:1998;1529-1542.
38. Maren T.H. Use of inhibitors in physiological studies of carbonic anhydrase. American Journal of Physiology. 232:1977;F291-F297.
39. McCormick D.A., Contreras D. On the cellular and network bases of epileptic seizures. Annual Review of Physiology. 63:2001;815-846.
40. A receptors in the hippocampus. Science. 253:1991;1420-1423.
41. B receptors and the effects of baclofen in the mammalian central nervous system. Progress in Neurobiology. 46:1995;423-462.
42. Mott D.D., Bragdon A.C., Lewis D.V., Wilson W.A. Baclofen has a proepileptic effect in the rat dentate gyrus. Journal of Pharmacology and Experimental Therapeutics. 249:1989;721-725.
43. B receptors. International Review of Neurobiology. 36:1994;97-223.
44. Nusser Z., Hajos N., Somogyi P., Mody I. Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature. 395:1998;172-177.
45. Pasternack M., Voipio J., Kaila K. Intracellular carbonic anhydrase activity and its role in GABA-induced acidosis in isolated rat hippocampal pyramidal neurones. Acta Physiolica Scandinavica. 148:1993;229-231.
46. Perez-Velazquez J.L., Valiante T.A., Carlen P.L. Modulation of gap junctional mechanisms during calcium-free induced field burst activity: a possible role for electrotonic coupling in epileptogenesis. Journal of Neuroscience. 14:1994;4308-4317.
47. Perreault P., Avoli M. 4-aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. Journal of Neuroscience. 12:1992;104-115.
48. Pitler T.A., Alger B.E. Depolarization-induced suppression of GABAergic inhibition in rat hippocampal pyramidal cells: G protein involvement in a presynaptic mechanism. Neuron. 13:1994;1447-1455.
49. 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. Molecular and Cellular Neurosciences. 17:2001;1059-1070.
50. Ratzliff A.H., Santhakumar V., Howard A., Soltesz I. Mossy cells in epilepsy: rigor mortis or vigor mortis? Trends in Neuroscience. 25:2002;140-144.
51. Reiss W.G., Oles K.S. Acetazolamide in the treatment of seizures. Annals of Pharmacotherapy. 30:1996;514-519.
52. Scanziani M. GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron. 25:2000;673-681.
53. Schuler V., Luscher C., Blanchet C., Klix N., Sansig G., Klebs K., Schmutz M., Heid J., Gentry C., Urban L., Fox A., Spooren W., Jaton A., Vigouret J., Pozza M., Kelly P.H., Mosbacher J., Froestl W., Kaslin E., Korn R., Bischoff S., Kaupmann K., Bettler B. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic gaba(b) responses in mice lacking gaba(b(1)). Neuron. 31:2001;47-58.
54. Schutz W., Freissmuth M. Reverse intrinsic activity of antagonists on G protein-coupled receptors. Trends in Pharmacological Science. 13:1992;376-380.
55. Sinha S.R., Saggau P. Imaging of 4-ap-induced, gaba(a)-dependent spontaneous synchronized activity mediated by the hippocampal interneuron network. Journal of Neurophysiology. 86:2001;381-391.
56. 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. Journal of Neuroscience. 19:1999;9252-9260.
57. Somjen G.G., Tombaugh G.C. pH Modulation of Neuronal Excitability and Central Nervous System Functions. Kaila K., Ransom B., pH and Brain Function. 1998;373-393 Wiley-Liss, New York.
58. Spray D.C., Scemes E. Effects of Intracellular pH (and Ca2+) on Gap Junction Channels. Kaila K., Ransom B., pH and Brain function. 1998;477-489 Wiley-Liss, New York.
59. Spray D.C., White R.L., Mazet F., Bennett M.V. Regulation of gap junctional conductance. American Journal of Physiology. 248:1985;H753-H764.
60. Srinivas M., Hopperstad M.G., Spray D.C. Quinine blocks specific gap junction channel subtypes. Proceedings of the National Academy of Sciences USA. 98:2001;10942-10947.
61. A receptors. See comments Science. 269:1995;977-981.
62. A receptors. Journal of Neurophysiology. 70:1993;976-984.
63. Stringer J.L. A comparison of topiramate and acetazolamide on seizure duration and paired-pulse inhibition in the dentate gyrus of the rat. Epilepsy Research. 40:2000;147-153.
64. Taira T., Lamsa K., Kaila K. Post-tetanic excitation mediated by GABA(A) receptors in rat CA1 pyramidal neurons. Journal of Neurophysiology. 77:1997;2213-2218.
65. Tamas G., Buhl E.H., Lorincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nature Neuroscience. 3:2000;366-371.
66. Thompson S.M., Gähwiler B.H. Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. Journal of Neurophysiology. 61:1989;512-523.
67. Trudeau L.E., Emery D.G., Haydon P.G. Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron. 17:1996;789-797.
68. Venance L., Rozov A., Blatow M., Burnashev N., Feldmeyer D., Monyer H. Connexin expression in electrically coupled postnatal rat brain neurons. Proceedings of the National Academy of Sciences USA. 97:2000;10260-10265.
69. Vergnes M., Boehrer A., Simler S., Bernasconi R., Marescaux C. Opposite effects of GABAB receptor antagonists on absences and convulsive seizures. European Journal of Pharmacology. 332:1997;245-255.
70. Voipio J., Kaila K. GABAergic excitation and K(+)-mediated volume transmission in the hippocampus. Progress in Brain Research. 125:2000;329-338.
71. Voipio J., Paalasmaa P., Taira T., Kaila K. Pharmacological characterization of extracellular pH transients evoked by selective synaptic and exogenous activation of AMPA, NMDA, and GABAA receptors in the rat hippocampal slice. Journal of Neurophysiology. 74:1995;633-642.
72. Voipio J., Pasternack M., MacLeod K.T. Ion-sensitive microelectrodes: microelectrode techniques. Ogden D., The Plymouth Workshop Handbook. 1994;275-316 The Company of Biologists, Cambridge, UK.
73. Wilson R.I., Kunos G., Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron. 31:2001;453-462.
74. Wilson R.I., Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 410:2001;588-592.
75. Yang Q., Michelson H.B. Gap junctions synchronize the firing of inhibitory interneurons in guinea pig hippocampus. Brain Research. 907:2001;139-143.