Heterogeneous firing behavior during ictal-like epileptiform activity in vitro

Journal of Neurophysiology

Volumn 107, Issue 5, 2012, Pages 1379-1392

  Andreasen, Mogens ^a   Nedergaard, Steen ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

Afterdischarge; Hippocampus; M current; Persistent sodium current; Plateau potentials

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; LIDOCAINE ETHOBROMIDE; LINOPIRDINE; PHENYTOIN; RETIGABINE; TETRODOTOXIN;

ACTION POTENTIAL; AFTERDISCHARGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; EPILEPTIC DISCHARGE; HIPPOCAMPAL CA1 REGION; IN VITRO STUDY; ION CURRENT; MALE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; REFRACTORY PERIOD; SEIZURE; SODIUM CURRENT; STIMULUS RESPONSE;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; MALE; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SEIZURES;

EID: 84857310249     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00309.2011     Document Type: Article

References (81)

1. Aiken SP, Lampe BJ, Murphy PA, Brown BS. Reduction of spike frequency adaptation and blockade of M-current in rat CA1 pyramidal neurones by linopirdine (DuP 996), a neurotransmitter release enhancer. Br J Pharmacol 115: 1163-1168, 1995.
2. Anderson WW, Lewis DV, Swartzwelder HS, Wilson WA. Magnesium-free medium activates seizure-like events in the rat hippocampal slice. Brain Res 398: 215-219, 1986.
3. + (Kir) channels antagonize ictal-like epileptiform activity in area CA1 of the rat hippocampus. Hippocampus 17: 1037-1048, 2007.
4. Avoli M, Louvel J, Pumain R, Köhling R. Cellular and molecular mechanisms of epilepsy in the human brain. Prog Neurobiol 77: 166-200, 2005.
5. 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 70: 1018-1029, 1993.
6. Azouz R, Jensen MS, Yaari Y. Muscarinic modulation of intrinsic burst firing in hippocampal neurons. Eur J Neurosci 6: 961-966, 1994.
7. Azouz R, Jensen MS, Yaari Y. Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492: 211-223, 1996.
8. Babb TL, Wilson CL, Isokawa-Akesson M. Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical lobe seizures. Electroencephalogr Clin Neurophysiol 66: 467-482, 1987.
9. Bikson M, Baraban SC, Durand DM. Conditions sufficient for nonsynaptic epileptogenesis in the CA1 region of hippocampal slices. J Neurophysiol 87: 62-71, 2002.
10. Bikson M, Fox JE, Jefferys JG. Neuronal aggregate formation underlies spatiotemporal dynamics of nonsynaptic seizure initiation. J Neurophysiol 89: 2330-2333, 2003.
11. Block BM, Jones SW. Ion permeation and block of M-type delayed rectifier potassium channels. J Gen Physiol 107: 473-488, 1996.
12. Borck C, Jefferys JGR. Seizure-like events in disinhibited ventral slices of adult rat hippocampus. J Neurophysiol 82: 2130-2142, 1999.
13. Bordey A, Sontheimer H. Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 32: 286-303, 1998.
14. Bragin A, Wilson CL, Engel J Jr. Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41: S144-S152, 2000.
15. Chagnac-Amitai Y, Connors BW. Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. J Neurophysiol 62: 1149-1162, 1989.
16. + current of mammalian CNS neurones. Neuroreport 6: 1778-1780, 1995.
17. Chesnut TJ, Swann JW. Epileptiform activity induced by 4-aminopyridine in immature hippocampus. Epilepsy Res 2: 187-195, 1988.
18. Church J, McLennan H. Electrophysiological properties of rat CA1 pyramidal neurones in vitro modified by changes in extracellular bicarbonate. J Physiol 415: 85-108, 1989.
19. Coggan JS, Purnyn SL, Kreulen DL. Muscarinic inhibition of two potassium currents in guinea-pig prevertebral neurons: differentiation by extracellular cesium. Neuroscience 59: 349-361, 1994.
20. Connors BW. Initiation of synchronized neuronal bursting in neocortex. Nature 310: 685-687, 1984.
21. D'Ambrosio R. The role of glial membrane ion channels in seizures and epileptogenesis. Pharmacol Ther 103: 95-108, 2004.
22. D'Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM 2nd, Janigro D. Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 18: 4425-4438, 1998.
23. de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 63: 541-567, 2001.
24. de Curtis M, Gnatkovsky V. Reevaluating the mechanisms of focal ictogenesis: the role of low-voltage fast activity. Epilepsia 50: 2514-2525, 2009.
25. Dudek FE, Yasumura T, Rash JE. "Non-synaptic" mechanisms in seizures and epileptogenesis. Cell Biol Int 22: 793-805, 1998.
26. Franceschetti S, Guatteo E, Panzica F, Sancini G, Wanke E, Avanzini G. Ionic mechanisms underlying burst firing in pyramidal neurons: intracellular study in rat sensorimotor cortex. Brain Res 696: 127-139, 1995.
27. French CR, Sah P, Buckett KJ, Gage PW. A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95: 1139-1157, 1990.
28. Gutnick MJ, Connors BW, Prince DA. Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48: 1321-1335, 1982.
29. Haas HL, Jefferys JGR. Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J Physiol 354: 185-201, 1984.
30. Hinterkeuser S, Schröder W, Hager G, Seifert G, Blümcke I, Elger CE, Schramm J, Steinhäuser C. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 12: 2087-2096, 2000.
31. Hwa GGC, Avoli M. Cesium potentiates epileptiform activities induced by bicuculline methiodide in rat neocortex maintained in vitro. Epilepsia 32: 747-754, 1991.
32. + uptake in glia prevents long-term depression maintenance and causes epileptiform activity. J Neurosci 17: 2813-2824, 1997.
33. Jefferys JGR. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75: 689-723, 1995.
34. Jensen MS, Azouz R, Yaari Y. Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium. J Neurophysiol 71: 831-839, 1994.
35. Jensen MS, Azouz R, Yaari Y. Spike afterdepolarization and burst generation in somata of adult rat hippocampal CA1 pyramidal cells. J Physiol 492: 199-210, 1996.
36. Jensen MS, Yaari Y. The relationship between interictal and ictal paroxysms in an in vitro model of focal hippocampal epilepsy. Ann Neurol 24: 591-598, 1988.
37. Jensen MS, Yaari Y. Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J Neurophysiol 77: 1224-1233, 1997.
38. Kager H, Wadman WJ, Somjen GG. Seizure-like afterdischarges simulated in a model neuron. J Comput Neurosci 22: 105-128, 2007.
39. Köhling R, Vreugdenhill M, Bracci E, Jefferys JGR. Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J Neurosci 20: 6820-6829, 2000.
40. Konnerth A, Heinemann U, Yaari Y. Nonsynaptic epileptogenesis in the mammalian hippocampus in vitro. I. Development of seizure-like activity in low extracellular calcium. J Neurophysiol 56: 409-423, 1986.
41. Kraglund N, Andreasen M, Nedergaard S. Differential influence of nonsynaptic mechanisms in two in vitro models of epileptic field bursts. Brain Res 1324: 85-95, 2010.
42. Lacaille JC, Williams S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36: 349-359, 1990.
43. Main MJ, Cryan JE, Dupere JRB, Cox B, Clare JJ, Burbridge SA. Modulation of KCNQ2/3 potassium channels by the novel anticonvulsant retigabine. Mol Pharmacol 58: 253-262, 2000.
44. Mantegazza M, Curia G, Biagini G, Ragsdale DS, Avoli M. Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol 9: 413-424, 2010.
45. Matsumoto H, Marsan CA. Cortical cellular phenomena in experimental epilepsy: ictal manifestations. Exp Neurol 9: 305-326, 1964.
46. McCormick DA, Contreras D. On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63: 815-846, 2001.
47. McNamara JO, Huang YZ, Leonard AS. Molecular signalling mechanisms underlying epileptogenesis. Sci STKE 2006: re12, 2006.
48. Prince DA. Physiological mechanisms of focal epileptogenesis. Epilepsia 26: S3-S14, 1985.
49. Rafiq A, DeLorenzo RJ, Coulter DA. Generation and propagation of epileptiform discharges in a combined entorhinal cortex/hippocampal slice. J Neurophysiol 70: 1962-1974, 1993.
50. Rafiq A, Zhang YF, DeLorenzo RJ, Coulter DA. Long-duration selfsustained epileptiform activity in the hippocampal-parahippocampal slice: a model of status epilepticus. J Neurophysiol 74: 2028-2042, 1995.
51. Richardson TL, Turner RW, Miller JJ. Extracellular fields influence transmembrane potentials and synchronization of hippocampal neuronal activity. Brain Res 294: 255-262, 1984.
52. 2+- dependent intrinsic bursting in rat pilocarpine model of temporal lobe epilepsy. J Physiol 532: 205-216, 2001.
53. Scharfman HE. The neurobiology of epilepsy. Curr Neurol Neurosci Rep 7: 348-354, 2007.
54. Schnee ME, Brown BS. Selectivity of linopirdine (DuP 996), a neurotransmitter release enhancer, in blocking voltage-dependent and calcium-activated potassium currents in hippocampal neurons. J Pharmacol Exp Ther 286: 709-717, 1998.
55. Schwartzkroin PA. Characteristics of CA1 neurons recorded intracellularly in the hippocampal in vitro slice preparation. Brain Res 85: 423-436, 1975.
56. Segal MM, Douglas AF. Late sodium channel openings underlying epileptiform activity are preferentially diminished by the anticonvulsant phenytoin. J Neurophysiol 77: 3021-3034, 1997.
57. +-current facilitates synchronization of hyperexcitable pyramidal neurons. Brain Res 1252: 76-86, 2009.
58. Skov J, Nedergaard S, Andreasen M. New type of synaptically mediated epileptiform activity independent of known glutamate and GABA receptors. J Neurophysiol 93: 1845-1856, 2005.
59. Somjen GG, Müller M. Potassium-induced enhancement of persistent inward current in hippocampal neurons in isolation and in tissue slices. Brain Res 885: 102-110, 2000.
60. Stafstrom CE. Persistent sodium current and its role in epilepsy. Epilepsy Curr 7: 15-22, 2007.
61. Steinhäuser C, Seifert G. Glial membrane channels and receptors in epilepsy: impact for generation and spread of seizure activity. Eur J Pharmacol 447: 227-237, 2002.
62. Steriade M, Amzica F, Neckelmann D, Timofeev I. Spike-wave complexes and fast components of cortical generated seizures. II. Extra-and intracellular patterns. J Neurophysiol 80: 1456-1479, 1998.
63. Su H, Alroy G, Kirson ED, Yaari Y. Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21: 4173-4182, 2001.
64. Szente M, Boda B. Cellular mechanisms of neocortical secondary epileptogenesis. Brain Res 648: 203-214, 1994.
65. Taylor CP, Dudek FE. Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218: 810-812, 1982.
66. Taylor CP, Dudek FE. Excitation of hippocampal pyramidal cells by an electrical field effect. J Neurophysiol 52: 126-142, 1984.
67. Traub RD, Borck C, Colling SB, Jefferys JG. On the structure of ictal events in vitro. Epilepsia 37: 879-891, 1996.
68. Traub RD, Dudek FE, Taylor CP, Knowles WD. Simulation of hippocampal afterdischarges synchronized by electrical interactions. Neuroscience 14: 1033-1038, 1985.
69. Traub RD, Jefferys JGR, Whittington MA. Networks of pyramidal cells: synchronized bursts. In Fast Oscillations in Cortical Circuits, edited by Traub RD, Jefferys JGR, Whittington MA. Cambridge, MA: MIT Press, 1999.
70. Traub RD, Wong RKS. Cellular mechanism of neuronal synchronization in epilepsy. Science 216: 745-747, 1982.
71. Traynelis SF, Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59: 259-276, 1988.
72. Varona P, Ibarz JM, López-Aguado L, Herreras O. Macroscopic and subcellular factors shaping population spikes. J Neurophysiol 83: 2192-2208, 2000.
73. Wyler AR, Burchiel KJ, Ward AA Jr. Chronic epileptic foci in monkeys: correlation between seizure frequency and proportion of pacemaker epileptic neurons. Epilepsia 19: 475-483, 1978.
74. Wyler AR, Fetz EE, Ward AA Jr. Firing patterns of epileptic and normal neurons in the chronic alumina focus in undrugged monkeys during different behavioral states. Brain Res 98: 1-20, 1975.
75. Wyler AR, Ward AA Jr. Neuronal firing patterns from epileptogenic foci of monkey and human. Adv Neurol 44: 967-989, 1986.
76. Xiong ZQ, Stringer JL. Cesium induces spontaneous epileptiform activity without changing extracellular potassium regulation in rat hippocampus. J Neurophysiol 82: 3339-3346, 1999.
77. Yaari Y, Beck H. "Epileptic neurons" in temporal lobe epilepsy. Brain Pathol 12: 234-239, 2002.
78. Yamada N, Bilkey DK. Kindling-induced persistent alterations in the membrane and synaptic properties of CA1 pyramidal neurons. Brain Res 561: 324-331, 1991.
79. + channels drive spike afterdepolarization and associated bursting in adult CA1 pyramidal cells. J Neurosci 25: 97049720, 2005.
80. Yue C, Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24: 4616-4624, 2004.
81. Yue C, Yaari Y. Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J Neurophysiol 95: 3480-3495, 2006.