Hyperthermia induces epileptiform discharges in cultured rat cortical neurons

Brain Research

Volumn 1417, Issue , 2011, Pages 87-102

  Wang, Ying Ying ^a   Qin, Jiong ^a   Han, Ying ^a   Cai, Jie ^a   Xing, Guo Gang ^a,b  

^a PEKING UNIVERSITY   (China)

^b BEIJING HOSPITAL   (China)

Author keywords

Cortical neuron; Epileptiform discharge; Febrile seizure; GABA B receptor; Hyperthermia; In vitro

Indexed keywords

BACLOFEN;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; EPILEPTIC DISCHARGE; EVOKED RESPONSE; FEBRILE CONVULSION; FEMALE; HYPERTHERMIA; NERVE CELL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE EXCITABILITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; BACLOFEN; CELLS, CULTURED; CEREBRAL CORTEX; FEVER; FLUORESCENT ANTIBODY TECHNIQUE; GABA-B RECEPTOR AGONISTS; HOT TEMPERATURE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GABA-B; SEIZURES, FEBRILE;

RATTUS;

EID: 80053246235     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.08.027     Document Type: Article

References (94)

1. U. Altrup, and M. Wiemann Paroxysmal depolarization shifts (PDS) induce non-synaptic responses in neighboured neurons (buccal ganglia, Helix pomatia) Brain Res. 972 2003 186 196 (Pubitemid 36507091)
2. P. Andersen, and E.I. Moser Brain temperature and hippocampal function Hippocampus 5 1995 491 498 (Pubitemid 26088284)
3. D.M. Andrade Genetic basis in epilepsies caused by malformations of cortical development and in those with structurally normal brain Hum. Genet. 126 2009 173 193
4. M. Avoli, G.G. Hwa, J.C. Lacaille, A. Olivier, and J.G. Villemure Electrophysiological and repetitive firing properties of neurons in the superficial/middle layers of the human neocortex maintained in vitro Exp. Brain Res. 98 1994 135 144 (Pubitemid 24112931)
5. T.Z. Baram, and S. Shinnar Febrile Seizures 2002 Academic Press San Diego, CA, USA
6. T.Z. Baram, A. Gerth, and L. Schultz Febrile seizures: an appropriate-aged model suitable for long-term studies Brain Res. Dev. Brain Res. 98 1997 265 270 (Pubitemid 27075283)
7. R.A. Bender, and T.Z. Baram Hyperpolarization activated cyclic-nucleotide gated (HCN) channels in developing neuronal networks Prog. Neurobiol. 86 2008 129 140
8. A.T. Berg, S. Shinnar, E.D. Shapiro, M.E. Salomon, E.F. Crain, and W.A. Hauser Risk factors for a first febrile seizure: a matched case-control study Epilepsia 36 1995 334 341
9. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents J. Neurosci. 24 2004 5301 5306 (Pubitemid 38747670)
10. M. Bortolato, R. Frau, M. Orru, M. Fa, C. Dessi, M. Puligheddu, L. Barberini, G. Pillolla, L. Polizzi, F. Santoni, G. Mereu, and F. Marrosu GABAB receptor activation exacerbates spontaneous spike-and-wave discharges in DBA/2J mice Seizure 19 2010 226 231
11. J.T. Brown, C.H. Gill, C.E. Farmer, C. Lanneau, A.D. Randall, M.N. Pangalos, G.L. Collingridge, and C.H. Davies Mechanisms contributing to the exacerbated epileptiform activity in hippocampal slices of GABAB1 receptor subunit knockout mice Epilepsy Res. 57 2003 121 136 (Pubitemid 38167728)
12. S. Burattini, M. Battistelli, and E. Falcieri Morpho-functional features of in-vitro cell death induced by physical agents Curr. Pharm. Des. 16 2010 1376 1386
13. H.Y. Cao, Y.W. Jiang, Z.W. Liu, and X.R. Wu Effect of recurrent epileptiform discharges induced by magnesium-free treatment on developing cortical neurons in vitro Brain Res. Dev. Brain Res. 142 2003 1 6
14. F. Carratala, and M. Moya Febrile convulsions induced by microwaves and the alteration in behavior of albino mouse OF1 Biol Neonate. 60 1991 62 68
15. D.S. Carter, L.S. Deshpande, A. Rafiq, S. Sombati, and R.J. DeLorenzo Characterization of spontaneous recurrent epileptiform discharges in hippocampal-entorhinal cortical slices prepared from chronic epileptic animals Seizure 20 2011 218 224
16. F. Cendes, F. Andermann, F. Dubeau, P. Gloor, A. Evans, M. Jones-Gotman, A. Olivier, E. Andermann, Y. Robitaille, and I. Lopes-Cendes Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study Neurology 43 1993 1083 1087 (Pubitemid 23177700)
17. Y.C. Chang, A.M. Huang, Y.M. Kuo, S.T. Wang, Y.Y. Chang, and C.C. Huang Febrile seizures impair memory and cAMP response-element binding protein activation Ann. Neurol. 54 2003 706 718
18. Y.C. Chang, Y.M. Kuo, A.M. Huang, and C.C. Huang Repetitive febrile seizures in rat pups cause long-lasting deficits in synaptic plasticity and NR2A tyrosine phosphorylation Neurobiol. Dis. 18 2005 466 475
19. K. Chen, I. Aradi, N. Thon, M. Eghbal-Ahmadi, T.Z. Baram, and I. Soltesz Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability Nat. Med. 7 2001 331 337 (Pubitemid 32224349)
20. I. Cohen, G. Huberfeld, and R. Miles Emergence of disinhibition-induced synchrony in the CA3 region of the guinea pig hippocampus in vitro J. Physiol. 570 2006 583 594
21. R.J. DeLorenzo, D.A. Sun, R.E. Blair, and S. Sombati An in vitro model of stroke-induced epilepsy: elucidation of the roles of glutamate and calcium in the induction and maintenance of stroke-induced epileptogenesis Int. Rev. Neurobiol. 81 59-84 2007 59 84
22. J.F. Disterhoft, W.W. Wu, and M. Ohno Biophysical alterations of hippocampal pyramidal neurons in learning, ageing and Alzheimer's disease Ageing Res. Rev. 3 2004 383 406 (Pubitemid 39487897)
23. C.M. Dube, A.L. Brewster, C. Richichi, Q. Zha, and T.Z. Baram Fever, febrile seizures and epilepsy Trends Neurosci. 30 2007 490 496 (Pubitemid 47513235)
24. C.M. Dube, A.L. Brewster, and T.Z. Baram Febrile seizures: mechanisms and relationship to epilepsy Brain Dev. 31 2009 366 371
25. C.M. Dube, J.L. Zhou, M. Hamamura, Q. Zhao, A. Ring, J. Abrahams, K. McIntyre, O. Nalcioglu, T. Shatskih, T.Z. Baram, and G.L. Holmes Cognitive dysfunction after experimental febrile seizures Exp. Neurol. 215 2009 167 177
26. P. Eckerman, K. Scharruhn, and J.M. Horowitz Effects of temperature and acid-base state on hippocampal population spikes in hamsters Am. J. Physiol. 258 1990 R1140 R1146
27. A. Escayg, and A.L. Goldin Sodium channel SCN1A and epilepsy: mutations and mechanisms Epilepsia 2010 1650 1658
28. S.D. Fernandez de, J. Garduno, E. Galvan, and W. Buno Calcium-activated afterhyperpolarizations regulate synchronization and timing of epileptiform bursts in hippocampal CA3 pyramidal neurons J. Neurophysiol. 96 2006 3028 3041 (Pubitemid 44837849)
29. M. Fukuda, T. Morimoto, H. Nagao, and K. Kida Clinical study of epilepsy with severe febrile seizures and seizures induced by hot water bath Brain Dev. 19 1997 212 216 (Pubitemid 27174022)
30. A.L. George, and K.M. Jacobs Altered intrinsic properties of neuronal subtypes in malformed epileptogenic cortex Brain Res. 1374 2011 116 128
31. J.W. Gibbs III, S. Sombati, R.J. DeLorenzo, and D.A. Coulter Physiological and pharmacological alterations in postsynaptic GABA(A) receptor function in a hippocampal culture model of chronic spontaneous seizures J. Neurophysiol. 77 1997 2139 2152 (Pubitemid 27174999)
32. R. Guerrini Genetic malformations of the cerebral cortex and epilepsy Epilepsia 46 Suppl. 1 2005 32 37 (Pubitemid 40365625)
33. R. Guerrini, and R. Carrozzo Epilepsy and genetic malformations of the cerebral cortex Am. J. Med. Genet. 106 2001 160 173
34. Y. Han, J. Qin, X. Chang, Z. Yang, D. Bu, and J. Du Modulating effect of hydrogen sulfide on gamma-aminobutyric acid B receptor in recurrent febrile seizures in rats Neurosci. Res. 53 2005 216 219 (Pubitemid 41219539)
35. Y. Han, J. Qin, X. Chang, Z. Yang, X. Tang, and J. Du Hydrogen sulfide may improve the hippocampal damage induced by recurrent febrile seizures in rats Biochem. Biophys. Res. Commun. 327 2005 431 436 (Pubitemid 40040494)
36. Y. Han, J. Qin, D.F. Bu, X.Z. Chang, and Z.X. Yang Successive alterations of hippocampal gamma-aminobutyric acid B receptor subunits in a rat model of febrile seizure Life Sci. 78 2006 2944 2952
37. W.A. Hauser The prevalence and incidence of convulsive disorders in children Epilepsia 35 Suppl. 2 1994 S1 S6
38. J.G. Heida, and Q.J. Pittman Causal links between brain cytokines and experimental febrile convulsions in the rat Epilepsia 46 2005 1906 1913 (Pubitemid 44922001)
39. J.G. Heida, S.L. Moshe, and Q.J. Pittman The role of interleukin-1beta in febrile seizures Brain Dev. 31 2009 388 393
40. S.A. Helekar, and J.L. Noebels Synchronous hippocampal bursting reveals network excitability defects in an epilepsy gene mutation Proc. Natl. Acad. Sci. U. S. A. 88 1991 4736 4740 (Pubitemid 21914617)
41. D.L. Hjeresen, and J. Diaz Ontogeny of susceptibility to experimental febrile seizures in rats Dev. Psychobiol. 21 1988 261 275
42. D. Holtzman, K. Obana, and J. Olson Hyperthermia-induced seizures in the rat pup: a model for febrile convulsions in children Science 213 1981 1034 1036
43. C.C. Huang, and Y.C. Chang The long-term effects of febrile seizures on the hippocampal neuronal plasticity - clinical and experimental evidence Brain Dev. 31 2009 383 387
44. W. Jiang, T.M. Duong, and N.C. de Lanerolle The neuropathology of hyperthermic seizures in the rat Epilepsia 40 1999 5 19 (Pubitemid 29031747)
45. Q. Jiang, J. Wang, X. Wu, and Y. Jiang Alterations of NR2B and PSD-95 expression after early-life epileptiform discharges in developing neurons Int. J. Dev. Neurosci. 25 2007 165 170 (Pubitemid 46636173)
46. Q. Jiang, Y. Wu, J. Wang, X. Wu, J. Qin, and Y. Jiang Characterization of developing rat cortical neurons after epileptiform discharges Int. J. Dev. Neurosci. 28 2010 455 463
47. D. Khatami, Y. Nam, G. Brewer, and B. Wheeler Effect of bicuculline on the spontaneous and evoked activity of patterned embryonic hippocampal neurons cultured in vitro Conf. Proc. IEEE Eng. Med. Biol. Soc. 6 2004 4059 4062 (Pubitemid 40035141)
48. M.M. Kohl, and O. Paulsen The roles of GABAB receptors in cortical network activity Adv. Pharmacol. 58 2010 205 229
49. R. Koyama, and N. Matsuki Novel etiological and therapeutic strategies for neurodiseases: mechanisms and consequences of febrile seizures: lessons from animal models J. Pharmacol. Sci. 113 2010 14 22
50. H. Kruger, H.J. Luhmann, and U. Heinemann Repetitive spreading depression causes selective suppression of GABAergic function Neuroreport 7 1996 2733 2736 (Pubitemid 26403050)
51. S.E. Kwak, J.E. Kim, S.C. Kim, O.S. Kwon, S.Y. Choi, and T.C. Kang Hyperthermic seizure induces persistent alteration in excitability of the dentate gyrus in immature rats Brain Res. 1216 2008 1 15
52. L.S. Leung, K.J. Canning, and B. Shen Hippocampal afterdischarges after GABA(B)-receptor blockade in the freely moving rat Epilepsia 46 2005 203 216 (Pubitemid 40194664)
53. P. Mares, and H. Kubova What is the role of neurotransmitter systems in cortical seizures? Physiol. Res. 57 Suppl. 3 2008 S111 S120
54. F.H. Marshall The role of GABA(B) receptors in the regulation of excitatory neurotransmission Results Probl. Cell. Differ. 44 2008 87 98
55. 2+ increase in rat cortical neurons in vitro Epilepsia 50 2009 702 710
56. E. Moser, I. Mathiesen, and P. Andersen Association between brain temperature and dentate field potentials in exploring and swimming rats Science 259 1993 1324 1326 (Pubitemid 23100271)
57. B.T. Mossman In vitro approaches for determining mechanisms of toxicity and carcinogenicity by asbestos in the gastrointestinal and respiratory tracts Environ. Health Perspect. 53 1983 155 161 (Pubitemid 14162054)
58. J.C. Oakley, F. Kalume, F.H. Yu, T. Scheuer, and W.A. Catterall Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy Proc. Natl. Acad. Sci. U. S. A. 106 2009 3994 3999
59. M. Ouardouz, P. Lema, P.N. Awad, C.G. Di, and L. Carmant N-methyl-d-aspartate, hyperpolarization-activated cation current (Ih) and gamma-aminobutyric acid conductances govern the risk of epileptogenesis following febrile seizures in rat hippocampus Eur. J. Neurosci. 31 2010 1252 1260
60. C.L. Padgett, and P.A. Slesinger GABAB receptor coupling to G-proteins and ion channels Adv. Pharmacol. 58 2010 123 147
61. Y.Z. Pan, L. Karr, and P. Rutecki Ictal activity induced by group I metabotropic glutamate receptor activation and loss of afterhyperpolarizations Neuropharmacology 59 2010 86 92
62. S.C. Pedder, R.I. Wilcox, J.M. Tuchek, D.D. Johnson, and R.D. Crawford Attenuation of febrile seizures in epileptic chicks by N-methyl-d-aspartate receptor antagonists Can. J. Physiol. Pharmacol. 68 1990 84 88 (Pubitemid 20107601)
63. A. Pinard, R. Seddik, and B. Bettler GABAB receptors: physiological functions and mechanisms of diversity Adv. Pharmacol. 58 2010 231 255
64. L. Qu, and L.S. Leung Mechanisms of hyperthermia-induced depression of GABAergic synaptic transmission in the immature rat hippocampus J. Neurochem. 106 2008 2158 2169
65. L. Qu, and L.S. Leung Effects of temperature elevation on neuronal inhibition in hippocampal neurons of immature and mature rats J. Neurosci. Res. 87 2009 2773 2785
66. L. Qu, X. Liu, C. Wu, and L.S. Leung Hyperthermia decreases GABAergic synaptic transmission in hippocampal neurons of immature rats Neurobiol. Dis. 27 2007 320 327 (Pubitemid 47333191)
67. L. Qu, R. Boyce, and L.S. Leung Seizures in the developing brain result in a long-lasting decrease in GABA(B) inhibitory postsynaptic currents in the rat hippocampus Neurobiol. Dis. 37 2010 704 710
68. A.Y. Reid, M.A. Galic, G.C. Teskey, and Q.J. Pittman Febrile seizures: current views and investigations Can. J. Neurol. Sci. 36 2009 679 686
69. P. Sah, and E.S. Faber Channels underlying neuronal calcium-activated potassium currents Prog. Neurobiol. 66 2002 345 353 (Pubitemid 34518289)
70. 2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy J. Physiol. 532 2001 205 216 (Pubitemid 32303283)
71. M.H. Scantlebury, and J.G. Heida Febrile seizures and temporal lobe epileptogenesis Epilepsy Res. 89 2010 27 33
72. S. Schuchmann, S. Vanhatalo, and K. Kaila Neurobiological and physiological mechanisms of fever-related epileptiform syndromes Brain Dev. 31 2009 378 382
73. M.M. Segal Epileptiform activity in microcultures containing one excitatory hippocampal neuron J. Neurophysiol. 65 1991 761 770
74. M.M. Shah, M. Javadzadeh-Tabatabaie, D.C. Benton, C.R. Ganellin, and D.G. Haylett Enhancement of hippocampal pyramidal cell excitability by the novel selective slow-afterhyperpolarization channel blocker 3- (triphenylmethylaminomethyl)pyridine (UCL2077) Mol. Pharmacol. 70 2006 1494 1502
75. K. Shibasaki, M. Suzuki, A. Mizuno, and M. Tominaga Effects of body temperature on neural activity in the hippocampus: regulation of resting membrane potentials by transient receptor potential vanilloid 4 J. Neurosci. 27 2007 1566 1575 (Pubitemid 46280059)
76. S. Shinnar Febrile seizures and mesial temporal sclerosis Epilepsy Curr. 3 2003 115 118
77. G. Sperk, S. Furtinger, C. Schwarzer, and S. Pirker GABA and its receptors in epilepsy Adv. Exp. Med. Biol. 548 2004 92 103 (Pubitemid 38979616)
78. D.A. Sun, S. Sombati, and R.J. DeLorenzo Glutamate injury-induced epileptogenesis in hippocampal neurons: an in vitro model of stroke-induced "epilepsy" Stroke 32 2001 2344 2350 (Pubitemid 32954807)
79. D.A. Sun, S. Sombati, R.E. Blair, and R.J. DeLorenzo Calcium-dependent epileptogenesis in an in vitro model of stroke-induced "epilepsy" Epilepsia 43 2002 1296 1305 (Pubitemid 35364986)
80. T.M. Szabo, T. Brookings, T. Preuss, and D.S. Faber Effects of temperature acclimation on a central neural circuit and its behavioral output J. Neurophysiol. 100 2008 2997 3008
81. V. Tancredi, G. D'Arcangelo, C. Zona, A. Siniscalchi, and M. Avoli Induction of epileptiform activity by temperature elevation in hippocampal slices from young rats: an in vitro model for febrile seizures? Epilepsia 33 1992 228 234
82. E.A. Thomas, R.J. Hawkins, K.L. Richards, R. Xu, E.V. Gazina, and S. Petrou Heat opens axon initial segment sodium channels: a febrile seizure mechanism? Ann. Neurol. 66 2009 219 226
83. S.M. Thompson, L.M. Masukawa, and D.A. Prince Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro J. Neurosci. 5 1985 817 824 (Pubitemid 15100470)
84. Z. Toth, X.X. Yan, S. Haftoglou, C.E. Ribak, and T.Z. Baram Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model J. Neurosci. 18 1998 4285 4294 (Pubitemid 28243821)
85. M.L. Tsai, and L.S. Leung Decrease of hippocampal GABA B receptor-mediated inhibition after hyperthermia-induced seizures in immature rats Epilepsia 47 2006 277 287
86. S. Verma-Ahuja, M.S. Evans, and J.A. Espinosa Evidence of increased excitability in GEPR hippocampus preceding development of seizure susceptibility Epilepsy Res. 31 1998 161 173 (Pubitemid 28370843)
87. J. Wellmer, H. Su, H. Beck, and Y. Yaari Long-lasting modification of intrinsic discharge properties in subicular neurons following status epilepticus Eur. J. Neurosci. 16 2002 259 266 (Pubitemid 36160246)
88. E. Widjaja, S.Z. Mahmoodabadi, O.C. Snead III, A. Almehdar, and M.L. Smith Widespread cortical thinning in children with frontal lobe epilepsy Epilepsia 2011 10 1167
89. J. Wu, and R.S. Fisher Hyperthermic spreading depressions in the immature rat hippocampal slice J. Neurophysiol. 84 2000 1355 1360
90. J. Wu, S.P. Javedan, K. Ellsworth, K. Smith, and R.S. Fisher Gamma oscillation underlies hyperthermia-induced epileptiform-like spikes in immature rat hippocampal slices BMC Neurosci. 2 2001 18 24
91. Z.C. Xu, Y.M. Chen, P. Xu, H. Liu, Y.L. Xie, and K.B. Zeng Epileptiform discharge upregulates p-ERK1/2, growth-associated protein 43 and synaptophysin in cultured rat hippocampal neurons Seizure 18 2009 680 685
92. L. Yang, F. Li, H. Zhang, W. Ge, C. Mi, R. Sun, and C. Liu Astrocyte activation and memory impairment in the repetitive febrile seizures model Epilepsy Res. 86 2009 209 220
93. + conductances contribute to a slow AHP in thalamic paraventricular nucleus neurons: a novel target for orexin receptors J. Neurophysiol. 104 2010 2052 2062
94. J.M. Ziobro, L.S. Deshpande, and R.J. DeLorenzo An organotypic hippocampal slice culture model of excitotoxic injury induced spontaneous recurrent epileptiform discharges Brain Res. 1371 2011 110 120