How inhibition influences seizure propagation

Neuropharmacology

Volumn 69, Issue , 2013, Pages 45-54

  Trevelyan, Andrew J ^a   Schevon, Catherine A ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Columbia University ^*  (United States)

Author keywords

Basket cell; EEG; Epilepsy; Ictal; Inhibition; Interictal; Neocortex; Pyramidal cell

Indexed keywords

GAP JUNCTION PROTEIN;

CLINICAL PRACTICE; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; GABAERGIC SYSTEM; GAP JUNCTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERNEURON; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SEIZURE; SPATIOTEMPORAL ANALYSIS; VOLTAGE CLAMP;

ANIMALS; ANTICONVULSANTS; ELECTRICAL SYNAPSES; ELECTROPHYSIOLOGY; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; HUMANS; INTERNEURONS; NERVE NET; NEURAL INHIBITION; SEIZURES; SYNAPSES;

EID: 84875252853     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.015     Document Type: Review

References (100)

1. B. Albowitz, and U. Kuhnt Spread of epileptiform potentials in the neocortical slice: recordings with voltage-sensitive dyes Brain Res. 631 1993 329 333
2. B.V. Atallah, W. Bruns, M. Carandini, and M. Scanziani Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli Neuron 73 2012 159 170
3. J.L. Bem, L. Kerr, and D. Stuerchler Mefloquine prophylaxis: an overview of spontaneous reports of severe psychiatric reactions and convulsions J. Trop. Med. Hyg. 95 1992 167 179
4. V. Braitenberg, and A. Schuz Cortex: Statistics and Geometry of Neuronal Connectivity second ed. 1998 Springer-Verlag Berlin, Heidelberg, New York
5. Y.T. Chang, P.C. Chen, I.J. Tsai, F.C. Sung, Z.N. Chin, H.T. Kuo, C.H. Tsai, and I.C. Chou Bidirectional relation between schizophrenia and epilepsy: a population-based retrospective cohort study Epilepsia 52 2011 2036 2042
6. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, and R. Miles On the origin of interictal activity in human temporal lobe epilepsy in vitro Science 298 2002 1418 1421
7. B.W. Connors Initiation of synchronized neuronal bursting in neocortex Nature 310 1984 685 687
8. R. Cossart, C. Dinocourt, J.C. Hirsch, A. Merchan-Perez, J. De Felipe, Y. Ben-Ari, M. Esclapez, and C. Bernard Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy Nat. Neurosci. 4 2001 52 62
9. D.R. Curtis, A.W. Duggan, D. Felix, and G.A. Johnston GABA, bicuculline and central inhibition Nature 226 1970 1222 1224
10. M. de Curtis, and G. Avanzini Interictal spikes in focal epileptogenesis Prog. Neurobiol. 63 2001 541 567
11. M.R. Deans, J.R. Gibson, C. Sellitto, B.W. Connors, and D.L. Paul Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36 Neuron 31 2001 477 485
12. M. Dichter, and W.A. Spencer Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction J. Neurophysiol. 32 1969 663 687
13. M. Dichter, and W.A. Spencer Penicillin-induced interictal discharges from the cat hippocampus. I. Characteristics and topographical features J. Neurophysiol. 32 1969 649 662
14. R.J. Douglas, H. Markram, and K.A.C. Martin Neocortex G.M. Shepherd, The Synaptic Organisation of the Brain fifth ed. 2004 Oxford University Press Oxford 499 558
15. A. Draguhn, R.D. Traub, D. Schmitz, and J.G. Jefferys Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro Nature 394 1998 189 192
16. V.I. Dzhala, K.V. Kuchibhotla, J.C. Glykys, K.T. Kahle, W.B. Swiercz, G. Feng, T. Kuner, G.J. Augustine, B.J. Bacskai, and K.J. Staley Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures J. Neurosci. 30 2010 11745 11761
17. T. Fukuda Structural organization of the gap junction network in the cerebral cortex Neuroscientist 13 2007 199 207
18. T. Fukuda, and T. Kosaka Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus J. Neurosci. 20 2000 1519 1528
19. T. Fukuda, and T. Kosaka 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
20. T. Fukuda, and T. Kosaka Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat Neuroscience 120 2003 5 20
21. T. Fukuda, T. Kosaka, W. Singer, and R.A. Galuske Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network J. Neurosci. 26 2006 3434 3443
22. Z. Gajda, E. Gyengesi, E. Hermesz, K.S. Ali, and M. Szente Involvement of gap junctions in the manifestation and control of the duration of seizures in rats in vivo Epilepsia 44 2003 1596 1600
23. M. Galarreta, and S. Hestrin Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex Nat. Neurosci. 1 1998 587 594
24. M. Galarreta, and S. Hestrin A network of fast-spiking cells in the neocortex connected by electrical synapses Nature 402 1999 72 75
25. M. Galarreta, F. Erdelyi, G. Szabo, and S. Hestrin Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors J. Neurosci. 24 2004 9770 9778
26. J.R. Geiger, T. Melcher, D.S. Koh, B. Sakmann, P.H. Seeburg, P. Jonas, and H. Monyer Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS Neuron 15 1995 193 204
27. J.R. Gibson, M. Beierlein, and B.W. Connors Two networks of electrically coupled inhibitory neurons in neocortex Nature 402 1999 75 79
28. S. Gigout, J. Louvel, H. Kawasaki, M. D'Antuono, V. Armand, I. Kurcewicz, A. Olivier, J. Laschet, B. Turak, B. Devaux, R. Pumain, and M. Avoli Effects of gap junction blockers on human neocortical synchronization Neurobiol. Dis. 22 2006 496 508
29. E.S. Goldensohn, and A.M. Salazar Temporal and spatial distribution of intracellular potentials during generation and spread of epileptogenic discharges Adv. Neurol. 44 1986 559 582
30. E.G. Gray Axo-somatic and axo-dendritic synapses in the cerebral cortex: an electron microscopic study J. Anat. 93 1959 420 433
31. F. Grenier, I. Timofeev, and M. Steriade Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates J. Neurophysiol. 86 2001 1884 1898
32. F. Grenier, I. Timofeev, and M. Steriade Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates J. Neurophysiol. 89 2003 841 852
33. M.S. Grubb, and J. Burrone Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability Nature 465 2010 1070 1074
34. A. Hempelmann, A. Heils, and T. Sander Confirmatory evidence for an association of the connexin-36 gene with juvenile myoclonic epilepsy Epilepsy Res. 71 2006 223 228
35. L.R. Hochberg, M.D. Serruya, G.M. Friehs, J.A. Mukand, M. Saleh, A.H. Caplan, A. Branner, D. Chen, R.D. Penn, and J.P. Donoghue Neuronal ensemble control of prosthetic devices by a human with tetraplegia Nature 442 2006 164 171
36. P.A. House, J.D. MacDonald, P.A. Tresco, and R.A. Normann Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations Neurosurg. Focus 20 2006 E4
37. G. Huberfeld, L. Wittner, S. Clemenceau, M. Baulac, K. Kaila, R. Miles, and C. Rivera Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy J. Neurosci. 27 2007 9866 9873
38. J. Jack, D. Noble, and R.W. Tsien Electric Current Flow in Excitable Cells second ed. 1983 OUP Oxford
39. Y. Kawaguchi Distinct firing patterns of neuronal subtypes in cortical synchronized activities J. Neurosci. 21 2001 7261 7272
40. K.X. Li, Y.M. Lu, Z.H. Xu, J. Zhang, J.M. Zhu, J.M. Zhang, S.X. Cao, X.J. Chen, Z. Chen, J.H. Luo, S. Duan, and X.M. Li Neuregulin 1 regulates excitability of fast-spiking neurons through Kv1.1 and acts in epilepsy Nat. Neurosci. 15 2012 267 273
41. F. Liang, and E.G. Jones Zif268 and fos-like immunoreactivity in tetanus toxin-induced epilepsy: reciprocal changes in the epileptic focus and the surround Brain Res. 778 1997 281 292
42. F. Liang, L.D. Le, and E.G. Jones Reciprocal up- and down-regulation of BDNF mRNA in tetanus toxin-induced epileptic focus and inhibitory surround in cerebral cortex Cereb. Cortex 8 1998 481 491
43. M. Lovett-Barron, G.F. Turi, P. Kaifosh, P.H. Lee, F. Bolze, X.H. Sun, J.F. Nicoud, B.V. Zemelman, S.M. Sternson, and A. Losonczy Regulation of neuronal input transformations by tunable dendritic inhibition Nat. Neurosci. 15 2012 423 430
44. I. Marchionni, and G. Maccaferri Quantitative dynamics and spatial profile of perisomatic GABAergic input during epileptiform synchronization in the CA1 hippocampus J. Physiol. 587 2009 5691 5708
45. H. Matsumoto, and C.A. Marsan Cortical cellular phenomena in experimental epilepsy: ictal manifestations Exp. Neurol. 9 1964 305 326
46. D.A. McCormick, and D. Contreras On the cellular and network bases of epileptic seizures Annu. Rev. Physiol. 63 2001 815 846
47. M. Megias, Z. Emri, T.F. Freund, and A.I. Gulyas Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells Neuroscience 102 2001 527 540
48. L. Menendez de la Prida, and A.J. Trevelyan Cellular mechanisms of high frequency oscillations in epilepsy: on the diverse sources of pathological activities Epilepsy Res. 2011
49. H.B. Michelson, and R.K. Wong Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro J. Physiol. 477 1994 35 45
50. S.B. Nelson, and G.G. Turrigiano Synaptic depression: a key player in the cortical balancing act Nat. Neurosci. 1 1998 539 541
51. K.E. Nilsen, A.R. Kelso, and H.R. Cock Antiepileptic effect of gap-junction blockers in a rat model of refractory focal cortical epilepsy Epilepsia 47 2006 1169 1175
52. A. Peters, and E.G. Jones Classification of cortical neurons A. Peters, E.G. Jones, Cerebral Cortex 1984 Plenum Press London 107 121
53. A. Peters, D.A. Kara, and K.M. Harriman The neuronal composition of area 17 of rat visual cortex. III. Numerical considerations J. Comp. Neurol. 238 1985 263 274
54. D.J. Pinto, S.L. Patrick, W.C. Huang, and B.W. Connors Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms J. Neurosci. 25 2005 8131 8140
55. F. Pouille, O. Watkinson, M. Scanziani, and A.J. Trevelyan Differential control of pyramidal neurons' dynamic range by somatic and dendritic inhibition 2008 Abstract Viewer and Itinerary Planner. Online. Edition 2008 Society for Neuroscience Washington, DC
56. T.P.S. Powell, and V. Mountcastle Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture Bull. Johns Hopkins Hosp. 105 1959 133 162
57. D.A. Prince, and B.J. Wilder Control mechanisms in cortical epileptogenic foci. "Surround" inhibition Arch. Neurol. 16 1967 194 202
58. P. Qin, H. Xu, T.M. Laursen, M. Vestergaard, and P.B. Mortensen Risk for schizophrenia and schizophrenia-like psychosis among patients with epilepsy: population based cohort study BMJ 331 2005 23
59. C. Rivera, J. Voipio, J.A. Payne, E. Ruusuvuori, H. Lahtinen, K. Lamsa, U. Pirvola, M. Saarma, and K. Kaila The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation Nature 397 1999 251 255
60. E.T. Rolls, S.M. Stringer, and T.P. Trappenberg A unified model of spatial and episodic memory Proc. Biol. Sci. 269 2002 1087 1093
61. B. Rouveix, F. Bricaire, C. Michon, G. Franssen, J. Lebras, J. Bernard, F. Ajana, and J.L. Vienne Mefloquine and an acute brain syndrome Ann. Intern. Med. 110 1989 577 578
62. N. Sakae, N. Yamasaki, K. Kitaichi, T. Fukuda, M. Yamada, H. Yoshikawa, T. Hiranita, Y. Tatsumi, J. Kira, T. Yamamoto, T. Miyakawa, and K.I. Nakayama Mice lacking the schizophrenia-associated protein FEZ1 manifest hyperactivity and enhanced responsiveness to psychostimulants Hum. Mol. Genet. 17 2008 3191 3203
63. C.A. Schevon, A.J. Trevelyan, C.E. Schroeder, R.R. Goodman, G. McKhann Jr., and R.G. Emerson Spatial characterization of interictal high frequency oscillations in epileptic neocortex Brain 132 2009 3047 3059
64. J. Schiller, G. Major, H.J. Koester, and Y. Schiller NMDA spikes in basal dendrites of cortical pyramidal neurons Nature 404 2000 285 289
65. A. Schuz, and G. Palm Density of neurons and synapses in the cerebral cortex of the mouse J. Comp. Neurol. 286 1989 442 455
66. T.H. Schwartz Optical imaging of epileptiform events in visual cortex in response to patterned photic stimulation Cereb. Cortex 13 2003 1287 1298
67. T.H. Schwartz, and T. Bonhoeffer In vivo optical mapping of epileptic foci and surround inhibition in ferret cerebral cortex Nat. Med. 7 2001 1063 1067
68. Y. Shu, A. Hasenstaub, and D.A. McCormick Turning on and off recurrent balanced cortical activity Nature 423 2003 288 293
69. E. Slater, A.W. Beard, and E. Glithero The schizophrenialike psychoses of epilepsy Br. J. Psychiatry 109 1963 95 150
70. J.J. Sloper, and T.P. Powell Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex Proc. R. Soc. Lond. B Biol. Sci. 203 1978 39 47
71. R.S. Sloviter Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy Science 235 1987 73 76
72. K.J. Staley, B.L. Soldo, and W.R. Proctor Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors Science 269 1995 977 981
73. M. Steriade, D. Contreras, and F. Amzica Synchronized sleep oscillations and their paroxysmal developments Trends Neurosci. 17 1994 199 208
74. M. Steriade, F. Amzica, D. Neckelmann, and I. Timofeev Spike-wave complexes and fast components of cortically generated seizures. II. Extra- and intracellular patterns J. Neurophysiol. 80 1998 1456 1479
75. D. Tadin, J.S. Lappin, L.A. Gilroy, and R. Blake Perceptual consequences of centre-surround antagonism in visual motion processing Nature 424 2003 312 315
76. D. Tadin, J. Kim, M.L. Doop, C. Gibson, J.S. Lappin, R. Blake, and S. Park Weakened center-surround interactions in visual motion processing in schizophrenia J. Neurosci. 26 2006 11403 11412
77. G.H. Tan, Y.Y. Liu, X.L. Hu, D.M. Yin, L. Mei, and Z.Q. Xiong Neuregulin 1 represses limbic epileptogenesis through ErbB4 in parvalbumin-expressing interneurons Nat. Neurosci. 15 2012 258 266
78. S.M. Thompson, and B.H. Gahwiler Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons J. Neurophysiol. 61 1989 512 523
79. S.M. Thompson, and B.H. Gahwiler Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro J. Neurophysiol. 61 1989 501 511
80. G.F. Tian, H. Azmi, T. Takano, Q. Xu, W. Peng, J. Lin, N. Oberheim, N. Lou, X. Wang, H.R. Zielke, J. Kang, and M. Nedergaard An astrocytic basis of epilepsy Nat. Med. 11 2005 973 981
81. I. Timofeev, and M. Steriade Neocortical seizures: initiation, development and cessation Neuroscience 123 2004 299 336
82. I. Timofeev, F. Grenier, and M. Steriade The role of chloride-dependent inhibition and the activity of fast-spiking neurons during cortical spike-wave electrographic seizures Neuroscience 114 2002 1115 1132
83. R.D. Traub, and R. Miles Neuronal Networks of the Hippocampus 1991 Cambridge University Press Cambridge, UK
84. R.D. Traub, and A. Bibbig 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
85. A.J. Trevelyan The direct relationship between inhibitory currents and local field potentials J. Neurosci. 29 2009 15299 15307
86. A.J. Trevelyan, and R.M. Yuste Imaging seizure propagation in vitro S.C. Baraban, Animal Models of Epilepsy: Methods and Innovations second ed. 2009 Humana Press 1051 1056
87. A.J. Trevelyan, D. Sussillo, and R. Yuste Feedforward inhibition contributes to the control of epileptiform propagation speed J. Neurosci. 27 2007 3383 3387
88. A.J. Trevelyan, D. Sussillo, B.O. Watson, and R. Yuste Modular propagation of epileptiform activity: evidence for an inhibitory veto in neocortex J. Neurosci. 26 2006 12447 12455
89. A.J. Trevelyan, T. Baldeweg, W. van Drongelen, R. Yuste, and M. Whittington The source of after discharge activity in neocortical tonic-clonic epilepsy J. Neurosci. 27 2007 13513 13519
90. A. Treves, and E.T. Rolls Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network Hippocampus 2 1992 189 199
91. W. Truccolo, J.A. Donoghue, L.R. Hochberg, E.N. Eskandar, J.R. Madsen, W.S. Anderson, E.N. Brown, E. Halgren, and S.S. Cash Single-neuron dynamics in human focal epilepsy Nat. Neurosci. 14 2011 635 641
92. L.J. Voss, G. Jacobson, J.W. Sleigh, A. Steyn-Ross, and M. Steyn-Ross Excitatory effects of gap junction blockers on cerebral cortex seizure-like activity in rats and mice Epilepsia 50 2009 1971 1978
93. E.T. Vu, and F.B. Krasne Evidence for a computational distinction between proximal and distal neuronal inhibition Science 255 1992 1710 1712
94. W.J. Wadman, and M.J. Gutnick Non-uniform propagation of epileptiform discharge in brain slices of rat neocortex Neuroscience 52 1993 255 262
95. A. Waziri, C.A. Schevon, J. Cappell, R.G. Emerson, G.M. McKhann 2nd, and R.R. Goodman Initial surgical experience with a dense cortical microarray in epileptic patients undergoing craniotomy for subdural electrode implantation Neurosurgery 64 2009 540 545 discussion 545
96. M.A. Whittington, R.D. Traub, and J.G. Jefferys Erosion of inhibition contributes to the progression of low magnesium bursts in rat hippocampal slices J. Physiol. 486 Pt 3 1995 723 734
97. B.Y. Wong, and D.A. Prince The lateral spread of ictal discharges in neocortical brain slices Epilepsy Res. 7 1990 29 39
98. F.H. Yu, M. Mantegazza, R.E. Westenbroek, C.A. Robbins, F. Kalume, K.A. Burton, W.J. Spain, G.S. McKnight, T. Scheuer, and W.A. Catterall Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy Nat. Neurosci. 9 2006 1142 1149
99. J. Ziburkus, J.R. Cressman, E. Barreto, and S.J. Schiff Interneuron and pyramidal cell interplay during in vitro seizure-like events J. Neurophysiol. 95 2006 3948 3954
100. V. Zsiros, I. Aradi, and G. Maccaferri Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus J. Physiol. 578 2007 527 544