Acute alterations of somatodendritic action potential dynamics in hippocampal ca1 pyramidal cells after kainate-induced status epilepticus in mice

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Minge, Daniel ^a   Bähring, Robert ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; KAINIC ACID; N [3,5 BIS(TRIFLUOROMETHYL)PHENYL] N' [2,4 DIBROMO 6 (1H TETRAZOL 5 YL)PHENYL] UREA; POTASSIUM CHANNEL AFFECTING AGENT; POTASSIUM ION; SODIUM ION; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN ELECTROPHYSIOLOGY; CALCIUM IMAGING; CALCIUM SIGNALING; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; DISEASE SIMULATION; EPILEPTIC STATE; EX VIVO STUDY; HIPPOCAMPAL CA1 REGION; LATENT PERIOD; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE POTENTIAL; NEUROIMAGING; NONHUMAN; PYRAMIDAL NERVE CELL; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; HIPPOCAMPUS; IN VITRO STUDY; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; DENDRITES; HIPPOCAMPUS; KAINIC ACID; MICE; MICE, INBRED C57BL; STATUS EPILEPTICUS;

EID: 80055042989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026664     Document Type: Article

References (73)

1. Bean BP, (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465.
2. Hille B, (2001) Ion channels of excitable membranes. Sunderland, MA Sinauer Associates, Inc.
3. Spitzer NC, Kingston PA, Manning TJ, Conklin MW, (2002) Outside and in: development of neuronal excitability. Curr Opin Neurobiol 12: 315-323.
4. Beck H, Yaari Y, (2008) Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci 9: 357-369.
5. Mitterdorfer J, Bean BP, (2002) Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 22: 10106-10115.
6. Storm JF, (1988) Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature 336: 379-381.
7. Connor JA, Stevens CF, (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21-30.
8. Connor JA, Stevens CF, (1971) Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J Physiol 213: 31-53.
9. Williams SR, Toth TI, Turner JP, Hughes SW, Crunelli V, (1997) The 'window' component of the low threshold Ca2+ current produces input signal amplification and bistability in cat and rat thalamocortical neurones. J Physiol 505: 689-705.
10. Maccaferri G, McBain CJ, (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497: 119-130.
11. Kim J, Wei DS, Hoffman DA, (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 569: 41-57.
12. Shao LR, Halvorsrud R, Borg-Graham L, Storm JF, (1999) The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol 521: 135-146.
13. Pedarzani P, McCutcheon JE, Rogge G, Jensen BS, Christophersen P, et al. (2005) Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current IAHP and modulates the firing properties of hippocampal pyramidal neurons. J Biol Chem 280: 41404-41411.
14. Storm JF, (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385: 733-759.
15. Gu N, Vervaeke K, Hu H, Storm JF, (2005) Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715.
16. Magistretti J, Castelli L, Forti L, D'Angelo E, (2006) Kinetic and functional analysis of transient, persistent and resurgent sodium currents in rat cerebellar granule cells in situ: an electrophysiological and modelling study. J Physiol 573: 83-106.
17. Metz AE, Jarsky T, Martina M, Spruston N, (2005) R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J Neurosci 25: 5763-5773.
18. Swensen AM, Bean BP, (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23: 9650-9663.
19. Haj-Dahmane S, Andrade R, (1997) Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons. J Neurophysiol 78: 1983-1989.
20. Stuart GJ, Sakmann B, (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367: 69-72.
21. Waters J, Schaefer A, Sakmann B, (2005) Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog Biophys Mol Biol 87: 145-170.
22. Hoffman DA, Magee JC, Colbert CM, Johnston D, (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875.
23. Dichter MA, (2009) Emerging concepts in the pathogenesis of epilepsy and epileptogenesis. Arch Neurol 66: 443-447.
24. Ben-Ari Y, Cossart R, (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23: 580-587.
25. Curia G, Longo D, Biagini G, Jones RS, Avoli M, (2008) The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172: 143-157.
26. Sloviter RS, (2008) Hippocampal epileptogenesis in animal models of mesial temporal lobe epilepsy with hippocampal sclerosis: the importance of the "latent period" and other concepts. Epilepsia 49: 85-92.
27. Sanabria ER, Su H, Yaari Y, (2001) Initiation of network bursts by Ca2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J Physiol 532: 205-216.
28. Bernard C, Anderson A, Becker A, Poolos NP, Beck H, et al. (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305: 532-535.
29. Covolan L, Mello LE, (2000) Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res 39: 133-152.
30. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, et al. (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16: 1337-1345.
31. Racine RJ, (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32: 281-294.
32. Bischofberger J, Engel D, Li L, Geiger JR, Jonas P, (2006) Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1: 2075-2081.
33. Lugo JN, Barnwell LF, Ren Y, Lee WL, Johnston LD, et al. (2008) Altered phosphorylation and localization of the A-type channel, Kv4.2 in status epilepticus. J Neurochem 106: 1929-1940.
34. Sperk G, (1994) Kainic acid seizures in the rat. Prog Neurobiol 42: 1-32.
35. Chen S, Su H, Yue C, Remy S, Royeck M, et al. (2011) An increase in persistent sodium current contributes to intrinsic neuronal bursting after status epilepticus. J Neurophysiol 105: 117-129.
36. Chen X, Yuan LL, Zhao C, Birnbaum SG, Frick A, et al. (2006) Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurosci 26: 12143-12151.
37. Malin SA, Nerbonne JM, (2000) Elimination of the fast transient in superior cervical ganglion neurons with expression of KV4.2W362F: molecular dissection of IA. J Neurosci 20: 5191-5199.
38. Serodio P, Kentros C, Rudy B, (1994) Identification of molecular components of A-type channels activating at subthreshold potentials. J Neurophysiol 72: 1516-1529.
39. Calloe K, Cordeiro JM, Di Diego JM, Hansen RS, Grunnet M, et al. (2009) A transient outward potassium current activator recapitulates the electrocardiographic manifestations of Brugada syndrome. Cardiovasc Res 81: 686-694.
40. Krishnan GP, Bazhenov M, (2011) Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J Neurosci 31: 8870-8882.
41. Chemin J, Girard C, Duprat F, Lesage F, Romey G, et al. (2003) Mechanisms underlying excitatory effects of group I metabotropic glutamate receptors via inhibition of 2P domain K+ channels. EMBO J 22: 5403-5411.
42. Chen K, Aradi I, Thon N, Eghbal-Ahmadi M, Baram TZ, et al. (2001) Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat Med 7: 331-337.
43. Shin M, Brager D, Jaramillo TC, Johnston D, Chetkovich DM, (2008) Mislocalization of h channel subunits underlies h channelopathy in temporal lobe epilepsy. Neurobiol Dis 32: 26-36.
44. Shah MM, Anderson AE, Leung V, Lin X, Johnston D, (2004) Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44: 495-508.
45. Jones-Davis DM, Macdonald RL, (2003) GABAA receptor function and pharmacology in epilepsy and status epilepticus. Curr Opin Pharmacol 3: 12-18.
46. Wellmer J, Su H, Beck H, Yaari Y, (2002) Long-lasting modification of intrinsic discharge properties in subicular neurons following status epilepticus. Eur J Neurosci 16: 259-266.
47. Yamada N, Bilkey DK, (1991) Kindling-induced persistent alterations in the membrane and synaptic properties of CA1 pyramidal neurons. Brain Res 561: 324-331.
48. Ketelaars SO, Gorter JA, van Vliet EA, Lopes da Silva FH, Wadman WJ, (2001) Sodium currents in isolated rat CA1 pyramidal and dentate granule neurones in the post-status epilepticus model of epilepsy. Neuroscience 105: 109-120.
49. Vreugdenhil M, Faas GC, Wadman WJ, (1998) Sodium currents in isolated rat CA1 neurons after kindling epileptogenesis. Neuroscience 86: 99-107.
50. Ellerkmann RK, Remy S, Chen J, Sochivko D, Elger CE, et al. (2003) Molecular and functional changes in voltage-dependent Na+ channels following pilocarpine-induced status epilepticus in rat dentate granule cells. Neuroscience 119: 323-333.
51. Storm JF, (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83: 161-187.
52. Ermolinsky B, Arshadmansab MF, Pacheco Otalora LF, Zarei MM, Garrido-Sanabria ER, (2008) Deficit of Kcnma1 mRNA expression in the dentate gyrus of epileptic rats. Neuroreport 19: 1291-1294.
53. Pacheco Otalora LF, Hernandez EF, Arshadmansab MF, Francisco S, Willis M, et al. (2008) Down-regulation of BK channel expression in the pilocarpine model of temporal lobe epilepsy. Brain Res 1200: 116-131.
54. Shruti S, Clem RL, Barth AL, (2008) A seizure-induced gain-of-function in BK channels is associated with elevated firing activity in neocortical pyramidal neurons. Neurobiol Dis 30: 323-330.
55. Becker AJ, Pitsch J, Sochivko D, Opitz T, Staniek M, et al. (2008) Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy. J Neurosci 28: 13341-13353.
56. Su H, Sochivko D, Becker A, Chen J, Jiang Y, et al. (2002) Upregulation of a T-type Ca2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J Neurosci 22: 3645-3655.
57. Yaari Y, Yue C, Su H, (2007) Recruitment of apical dendritic T-type Ca2+ channels by backpropagating spikes underlies de novo intrinsic bursting in hippocampal epileptogenesis. J Physiol 580: 435-450.
58. Magee JC, (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1: 181-190.
59. Häusser M, Spruston N, Stuart GJ, (2000) Diversity and dynamics of dendritic signaling. Science 290: 739-744.
60. Lorincz A, Nusser Z, (2010) Molecular identity of dendritic voltage-gated sodium channels. Science 328: 906-909.
61. Magee JC, Johnston D, (1995) Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487: 67-90.
62. Jerng HH, Pfaffinger PJ, Covarrubias M, (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27: 343-369.
63. Remy S, Beck H, Yaari Y, (2010) Plasticity of voltage-gated ion channels in pyramidal cell dendrites. Curr Opin Neurobiol 20: 503-509.
64. Monaghan MM, Menegola M, Vacher H, Rhodes KJ, Trimmer JS, (2008) Altered expression and localization of hippocampal A-type potassium channel subunits in the pilocarpine-induced model of temporal lobe epilepsy. Neuroscience 156: 550-562.
65. Ang CW, Carlson GC, Coulter DA, (2006) Massive and specific dysregulation of direct cortical input to the hippocampus in temporal lobe epilepsy. J Neurosci 26: 11850-11856.
66. Su T, Cong WD, Long YS, Luo AH, Sun WW, et al. (2008) Altered expression of voltage-gated potassium channel 4.2 and voltage-gated potassium channel 4-interacting protein, and changes in intracellular calcium levels following lithium-pilocarpine-induced status epilepticus. Neuroscience 157: 566-576.
67. Francis J, Jugloff DG, Mingo NS, Wallace MC, Jones OT, et al. (1997) Kainic acid-induced generalized seizures alter the regional hippocampal expression of the rat Kv4.2 potassium channel gene. Neurosci Lett 232: 91-94.
68. Tsaur ML, Sheng M, Lowenstein DH, Jan YN, Jan LY, (1992) Differential expression of K+ channel mRNAs in the rat brain and down-regulation in the hippocampus following seizures. Neuron 8: 1055-1067.
69. Pitkänen A, Kharatishvili I, Karhunen H, Lukasiuk K, Immonen R, et al. (2007) Epileptogenesis in experimental models. Epilepsia 48: 13-20.
70. Berger ML, Lefauconnier JM, Tremblay E, Ben-Ari Y, (1986) Limbic seizures induced by systemically applied kainic acid: how much kainic acid reaches the brain? Adv Exp Med Biol 203: 199-209.
71. Löscher W, Brandt C, (2010) Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 62: 668-700.
72. Lundby A, Jespersen T, Schmitt N, Grunnet M, Olesen SP, et al. (2010) Effect of the Ito activator NS5806 on cloned Kv4 channels depends on the accessory protein KChIP2. Br J Pharmacol 160: 2028-2044.
73. Kääb S, Dixon J, Duc J, Ashen D, Nabauer M, et al. (1998) Molecular basis of transient outward potassium current downregulation in human heart failure: a decrease in Kv4.3 mRNA correlates with a reduction in current density. Circulation 98: 1383-1393.