Involvement of electrical coupling in the in vivo ictal epileptiform activity induced by 4-aminopyridine in the neocortex

Neuroscience

Volumn 115, Issue 4, 2002, Pages 1067-1078

  Szente, M ^a   Gajda, Z ^a   Said Ali, K ^a   Hermesz, E ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Connexins; Gap junctions; Intracellular recordings; Primary ictal discharges; Secondary ictal discharges

Indexed keywords

4 AMINOPYRIDINE; CARBENOXOLONE; CONNEXIN 32; CONNEXIN 43; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL SYNCHRONIZATION; CONTROLLED STUDY; DRUG EFFECT; EPILEPTIC DISCHARGE; FEMALE; GAP JUNCTION; INTRACELLULAR RECORDING; MALE; NEOCORTEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE; SYNAPTIC TRANSMISSION;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; CARBENOXOLONE; CONNEXIN 43; CONNEXINS; CORTICAL SYNCHRONIZATION; EPILEPSY; FEMALE; GAP JUNCTIONS; MALE; NEOCORTEX; NEURONS; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, WISTAR; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

EID: 0037121622     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00533-X     Document Type: Article

References (73)

1. Alvarez-Maubecin V., García-Hernandez F., Williams J.T., Bockstaele E.L.V. Functional coupling between neurones and glia. J. Neurosci. 20:2000;4091-4098.
2. Amzica F., Steriade M. Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex. J. Neurosci. 20:2000;6648-6665.
3. Baranyi A., Szente M.B., Woody C.D. Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cats: I Patterns of firing activity and synaptic responses. J. Neurophysiol. 69:1993;1850-1864.
4. Belliveau D.J., Naus C.C.G. Differential localization of gap junction mRNAs in developing rat brain. Dev. Neurosci. 17:1995;81-96.
5. Benardo L.S. Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J. Neurophysiol. 77:1997;3134-3144.
6. Bennett M.V.L. Gap junctions as electrical synapses. J. Neurocytol. 26:1997;349-366.
7. Bennett, M.V.L., Spray, D.C., 1985. Gap Junctions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8. 2+ model of epileptiform activity. J. Neurophysiol. 82:1999;2262-2270.
9. Boda B., Szente M.B. Anticonvulsive effects of stimulation of substantia nigra pars reticulata on neocortical seizures. Brain Res. 574:1992;237-243.
10. Carlen P.L., Skinner F., Zhang L., Naus C., Kushnir M., Perez Velazquez J.L. The role of gap junctions in seizures. Brain Res. Rev. 32:2000;235-241.
11. Chen J.C.T., Chesler M. Extracellular alkaline shifts in rat hippocampal slice are mediated by NMDA and non-NMDA receptors. Neurophysiology. 68:1992;342-344.
12. Chesler M., Kaila K. Modulation of pH by neuronal activity. Trends Neurosci. 15:1992;396-401.
13. Connors B.W., Gutnick M.J. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48:1982;1302-1320.
14. de Curtis M., Manfridi A., Biella G. Activity dependent pH shift and periodic recurrence of spontaneous interictal spikes in a model of focal epileptogenesis. J. Neurosci. 18:1998;543-7551.
15. 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.
16. Dermietzel, R., 1996. Molecular diversity and plasticity of gap junctions in the nervous system. In: Spray, D.C., Dermietzel, R. (Eds.), Gap Junctions in the Nervous System. Landes Bioscience, New York, pp. 13-38.
17. Dermietzel R., Hertzberg E.L., Kessler J.A., Spray D.C. Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J. Neurosci. 11:1991;1421-1432.
18. Draguhn A., Traub R.D., Schmitz D., Jefferys J.G.R. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature. 394:1998;189-192.
19. Dudek, F.E., Andrew, R.D., MacVicar, B.A., Snow, R.T., Taylor, C.P., 1983. Recent evidence for and possible significance of gap junctions and electrotonic synapses in the mammalian brain. In: Basic Mechanisms of Neuronal Hyperexcitability. Alan R. Liss, New York, pp. 31-37.
20. Dudek, F.E., Patrylo, P.R., Wuarin, J.P., 1999. Mechanisms of neuronal synchronization during epileptiform activity. In: Delgado-Escueta, A.V., Wilson, W.A., Olsen, R.W., Porter, R.J. (Eds.), Basic Mechanisms of Epilepsy Vol. 79. Lippincott Williams and Wilkins, Philadelphia, PA, pp. 699-708.
21. Elisevich K., Rempler S., Smith B., Edvardsen K. Hippocampal connexin43 expression in human complex partial seizure disorder. Exp. Neurol. 45:1997;154-164.
22. Emmi A., Wenzel H.J., Schwartzkroin P.A., Taglialatela M., Castaldo P., Bianchi L., Nerbonne J., Robertson G.A., Janigro D. Do glia have heart? Expression and functional role for Ether-A-Go-Go currents in hippocampal astrocytes. J. Neurosci. 20:2000;3915-3925.
23. Fukuda T., Kosaka T. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J. Neurosci. 20:2000;1519-1528.
24. Fukuda T., Kosaka T. The dual network of GABAergic interneurons linked by both chemical and electrical synapses: a possible infrastructure of the cerebral cortex. Neurosci. Res. 38:2000;123-130.
25. Galarreta M., Hestrin S.A. Network of fast spiking cells in the neocortex connected by electrical synapses. Nature. 402:1999;72-78.
26. Giaume C., Fromaget C., Aoumari A., Cordier J., Glowinski J., Gros D. Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron. 61:1991;133-143.
27. Haas H.L., Jefferys J.G.R. Low-calcium field burst discharges of CA1 pyramidal neurons in rat hippocampal slices. J. Physiol. Lond. 354:1984;185-201.
28. Jefferys J.G.R. Nonsynaptic modulation of neuronal activity in the brain: Electric currents and extracellular ions. Physiol. Rev. 75:1995;689-723.
29. Jensen M.S., Azouz R., Yaari Y. Spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. Lond. 492:(Pt 1):1996;199-210.
30. Jensen M.S., Yaari Y. Role of intrinsic burst firing, potassium accumulation and electrical coupling in the elevated potassium model of hippocampal epilepsy. J. Neurophysiol. 77:1997;1224-1233.
31. Kandel, E.R., Siegebaum, S.A., 1999. Overview of synaptic transmission. In: Kandel, E.R., Schwartz, J.H., Jessel, T.M. (Eds.), Principle of Neural Science. McGraw-Hill, New York, p. 180.
32. Li J., Hertzberg E.L., Nagy J.I. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J. Comp. Neurol. 379:1997;571-591.
33. Li J., Shen H., Naus C.C.G., Zhang L., Carlen P.L. Upregulation of gap junction connexin 32 with epileptiform activity in the isolated mouse hippocampus. Neuroscience. 105:2001;589-598.
34. MacVicar B.A., Dudek F.E. Electrotonic coupling between pyramidal cells: A direct demonstration in rat hippocampal slices. Science. 213:1981;782-785.
35. MacVicar B.A., Jahnsen H. Uncoupling of CA3 pyramidal neurons by proprionaze. Brain Res. 330:1985;141-145.
36. Mambetisaeva E.T., Gire V., Evans W.H. Multiple connexin expression in peripheral nerve, Schwann cells, and Schwannoma cells. J. Neurosci. Res. 57:1999;166-175.
37. Micevych P.E., Abelson L. Distribution of mRNAs coding for liver and heart gap junction proteins in the rat central nervous system. J. Comp. Neurol. 305:1991;96-118.
38. Michelson H.B., Wong R.K.S. Synchronisation of inhibitory neurons in the guinea-pig hippocampus in vitro. J. Physiol. Lond. 477:1994;35-45.
39. Nadarajah B., Jones A.M., Evans W.H., Parnavelas J.G. Differential expression of connexins during neocortical development and neuronal circuit formation. J. Neurosci. 17:1997;3096-3111.
40. Nadarajah B., Thomiaidou D., Evans W.H., Parnavelas J.G. Gap junction in the adult cerebral cortex: regional differences in their distribution and cellular expression of connexins. J. Comp. Neurol. 376:1996;326-342.
41. Nagy J.I., Yamamoto T., Sawchuk M.A., Nance D.M., Hertzberg E.L. Quantitative immunohistochemical and biochemical correlates of connexin43 localization in rat brain. Glia. 51:1992;1-9.
42. Nagy, J.I., Yamamoto, T., Shiosaka, S., Dewar, K., Whittaker, M., Hertzberg, E.L., 1988. Immunohistochemical localization of gap junction protein in rat CNS: A preliminary account. In: Hertzberg, E.L., Johnson, R.G. (Eds.), Gap Junctions. Alan R. Liss, New York, pp. 375-389.
43. Naus C., Bochberger J., Paul D. Gap junction gene expression in human seizure disorders. Exp. Neurol. 111:1991;198-203.
44. Noctor C.S., Flint A.F., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glia cells establish radial units in neocortex. Nature. 409:2001;714-719.
45. Perez Velazquez J.L., Carlen P.L. Gap junctions, synchrony and seizures. Trends Neurosci. 23:2000;68-74.
46. Perez Velazquez J.L., Valiante T.A., Carlen P.L. Modulation of gap junction mechanisms during calcium-free induced field burst activity: A possible role for electrotonic coupling in epileptogenesis. J. Neurosci. 147:1994;4308-4317.
47. Rash J.E., Yasumura T., Dudek E.F., Nagy J.I. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 21:2001;1983-2000.
48. Ross F.M., Gwyn P., Spanswick D., Davies S.N. Carbenoxolone depresses epileptiform activity in the CA1 region of rat hippocampal slices. Neuroscience. 100:2000;789-796.
49. Schwartzkroin P.A., Prince D.A. Penicillin-induced epileptiform activity in the hippocampal in vitro preparation. Ann. Neurol. 1:1977;463-469.
50. Schweitzer J.S., Wang H., Xiong Z.O., Stringer J.L. pH Sensitivity of non-synaptic field bursts in the dentate gyrus. J. Neurophysiol. 84:2000;927-933.
51. Scobey R.P., Gabor A.J. Ectopic action-potential generation in epileptic cortex. J. Neurophysiol. 38:1975;383-394.
52. Shiosaka S., Yamamoto T., Hertzberg E.L., Nagy J.I. Gap junction protein in rat hippocampus: correlative light and electron microscope immunohistochemical localization. J. Comp. Neurol. 281:1989;282-297.
53. Simburger E., Stang A., Kremer M., Dermietzel R. Expression of connexin43 mRNA in adult rodent brain. Histochem. Cell. Biol. 1072:1997;127-137.
54. Sohl G., Guldenagel M., Beck H., Teubner B., Traub O., Gutierrez R., Heinemann U., Willecke K. Expression of connexin genes in hippocampus of kainate-treated and kindled rats under conditions of experimental epilepsy. Brain Res. Mol. Brain Res. 83:2000;44-51.
55. Somjen G.G. Acidification of interstitial fluid in hippocampal formation caused by seizures and spreading depression. Brain Res. 311:1984;186-188.
56. Spencer W.A., Kandel E.R. Electrophysiology of hippocampal neurons: fast prepotentials. J. Neurophysiol. 24:1961;272-285.
57. Spray D.C., Harris A.L., Bennett M.V.L. Gap junction conductance is a simple and sensitive function of intracellular pH. Science. 211:1981;712-715.
58. Stasheff S.F., Hines M., Wilson W. Axon terminal hyperexcitability associated with epileptogenesis in vitro. I. Origin of epileptic spikes. J. Neurophysiol. 70:1993;961-975.
59. A receptors. J. Neurophysiol. 70:1993;976-984.
60. Szabadics J., Lorincz A., Tamas G. β and α frequency synchronization by dendritic GABAergic Synapses and gap junctions in a network of cortical interneurons. J. Neurosci. 21:2001;5824-5831.
61. Szente M.B., Baranyi A. Mechanism of aminopyridine-induced ictal seizure activity in the cat neocortex. Brain Res. 441:1987;368-373.
62. Szente M.B., Baranyi A. Properties of depolarizing plateau potentials in aminopyridine-induced ictal seizure foci of cat motor cortex. Brain Res. 495:1989;261-270.
63. Szente M.B., Boda B. Cellular mechanisms of neocortical secondary epileptogenesis. Brain Res. 648:1994;203-214.
64. Szente M.B., Pongrácz F. Aminopyridine-induced seizure activity. EEG Clin. Neurophysiol. 46:1979;605-608.
65. Tamas G., Buhl E.H., Lorincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3:2000;366-371.
66. Taylor C.P., Dudek F.E. Synchronous neuronal afterdischarges in rat hippocampal slices without active chemical synapses. Science. 218:1982;810-812.
67. Traub R.D., Bibbig A.A. Model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J. Neurosci. 20:2000;2086-2093.
68. Traub R.D., Bibbig R.A., Piechotta A., Draguhn R., Schmitz D. Synaptic and nonsynaptic contributions to giant ipsps and ectopic spikes induced by 4-aminopyridine in the hippocampus in vitro. J. Neurophys. 85:2001;1246-1256.
69. Traub R.D., Schmitz D., Jefferys J.G.R., Draughun A. High frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axo-axinal gap junctions. Neuroscience. 92:1999;407-426.
70. Traub R.D., Whittington M.A., Buhl E.H., LeBeau F.E., Bibbig A., Boyd S., Cross H., Baldeweg T. A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia. 42:2001;153-170.
71. Walz W. pH shift evoked by neuronal stimulation in slices of rat hippocampus. Can. J. Physiol. Pharmacol. 67:1989;577-581.
72. Xiong Z.Q., Saggau P., Stringer J.L. Activity-dependent intracellular acidification correlates with the duration of seizure activity. J. Neurosci. 204:2000;1290-1296.
73. Yamamoto T., Ochalski A., Hertzberg E.L., Nagy J.I. On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. J. Comp. Neurol. 3024:1990;853-883.