Effect of topiramate on cognitive function and single units from hippocampal place cells following status epilepticus

Epilepsy and Behavior

Volumn 14, Issue 1, 2009, Pages 40-47

  Shatskikh, Tatiana ^a   Zhao, Qian ^a   Zhou, Jun Li ^a   Holmes, Gregory L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Epilepsy; Learning; Pilocarpine; Place cells; Seizures; Water maze

Indexed keywords

LITHIUM; PILOCARPINE; SODIUM CHLORIDE; TOPIRAMATE; WATER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; COGNITION; CONTROLLED STUDY; DRUG EFFICACY; EPILEPTIC STATE; HIPPOCAMPUS; IN VIVO STUDY; INTRACELLULAR RECORDING; LEARNING; MALE; MAZE TEST; NERVE CELL MEMBRANE POTENTIAL; NERVE SPROUTING; NEUROPROTECTION; NONHUMAN; PREFRONTAL CORTEX; RAT; TASK PERFORMANCE;

ANIMALS; ANTICONVULSANTS; CONVULSANTS; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; FRUCTOSE; HIPPOCAMPUS; LITHIUM CHLORIDE; MALE; MAZE LEARNING; NEURONS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS;

EID: 58149149770     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2008.09.030     Document Type: Article

References (56)

1. Aicardi J., and Chevrie J.J. Convulsive status epilepticus in infants and children. Epilepsia 11 (1970) 187-197
2. Aicardi J., and Chevrie J.-J. Consequences of status epilepticus in infants and children. In: Delgado-Escueta A.V., Wasterlain C.G., Treiman D.M., and Porter R.J. (Eds). Advances in neurology: vol. 34. Status epilepticus: mechanisms of brain damage and treatment (1983), Raven Press, New York 115-125
3. Van Esch A., Ramlal I.R., van Steensel-Moll H.A., and Steyerberg E.W. Outcome after febrile status epilepticus. Dev Med Child Neurol 38 (1996) 19-24
4. DeLorenzo R.J., Towne A.R., Pellock J.M., and Ko D. Status epilepticus in children, adults, and the elderly. Epilepsia 33 Suppl. 4 (1992) S15-S25
5. Sahin M., Menache C.C., Holmes G.L., and Riviello J.J. Outcome of severe refractory status epilepticus in children. Epilepsia 42 (2001) 1461-1467
6. Working Group on Status Epilepticus. Treatment of convulsive status epilepticus: recommendations of the Epilepsy Foundation of America's Working Group on Status Epilepticus. JAMA 270 (1993) 854-859
7. Jambaque I., Dellatolas G., Dulac O., Ponsot G., and Signoret J.L. Verbal and visual memory impairment in children with epilepsy. Neuropsychologia 31 (1993) 1321-1337
8. Krumholz A., Sung G.Y., Fisher R.S., Barry E., Bergey G.K., and Grattan L.M. Complex partial status epilepticus accompanied by serious morbidity and mortality. Neurology 45 (1995) 1499-1504
9. Kondratyev A., and Gale K. Temporal and spatial patterns of DNA fragmentation following focally or systemically-evoked status epilepticus in rats. Neurosci Lett 310 (2001) 13-16
10. Mello L.E., Cavalheiro E.A., Tan A.M., Pretorius J.K., Babb T.L., and Finch D.M. Granule cell dispersion in relation to mossy fiber sprouting, hippocampal cell loss, silent period and seizure frequency in the pilocarpine model of epilepsy. Epilepsy Res Suppl 9 (1992) 51-59
11. Mello L.E., Cavalheiro E.A., Tan A.M., et al. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34 (1993) 985-995
12. Muramatsu R., Ikegaya Y., Matsuki N., and Koyama R. Early-life status epilepticus induces ectopic granule cells in adult mice dentate gyrus. Exp Neurol 211 (2008) 503-510
13. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., and Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17 (1997) 3727-3738
14. Rice A., Rafiq A., Shapiro S.M., Jakoi E.R., Coulter D.A., and DeLorenzo R.J. Long-lasting reduction of inhibitory function and gamma-aminobutyric acid type A receptor subunit mRNA expression in a model of temporal lobe epilepsy. Proc Natl Acad Sci USA 93 (1996) 9665-9669
15. Brooks-Kayal A.R., Shumate M.D., Jin H., Rikhter T.Y., and Coulter D.A. Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4 (1998) 1166-1172
16. Rogawski M.A., and Loscher W. The neurobiology of antiepileptic drugs. Nat Rev Neurosci 5 (2004) 553-564
17. Perucca E. A pharmacological and clinical review on topiramate, a new antiepileptic drug. Pharmacol Res 35 (1997) 241-256
18. Perucca E., and Bialer M. The clinical pharmacokinetics of the newer antiepileptic drugs: focus on topiramate, zonisamide, and tiagabine. Clin Pharmacokinet 31 (2003) 29-46
19. Shank R.P., Gardocki J.F., Vaught J.L., et al. Topiramate: preclinical evaluation of structurally novel anticonvulsant. Epilepsia 35 (1994) 450-460
20. White H.S., Brown S.D., Woodhead J.H., Skeen G.A., and Wolf H.H. Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold. Epilepsy Res 28 (1997) 167-179
21. Rosenfeld W.E. Topiramate: a review of preclinical, pharmacokinetic, and clinical data. Clin Ther 19 (1997) 1294-1308
22. Sutula T.P. Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res 60 (2004) 161-171
23. Mazarati A., Shin D., Auvin S., and Sankar R. Age-dependent effects of topiramate on the acquisition and the retention of rapid kindling. Epilepsia 48 (2007) 765-773
24. Cha B.H., Silveira D.C., Liu X., Hu Y., and Holmes G.L. Effect of topiramate following recurrent and prolonged seizures during early development. Epilepsy Res 51 (2002) 217-232
25. Muller R.U., Kubie J.L., and Ranck Jr. J.B. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7 (1987) 1935-1950
26. Muller R.U., and Kubie J.L. The effects of changes in the environment on the spatial firing patterns of hippocampal complex-spike cells. J Neurosci 7 (1987) 1951-1968
27. Thompson L.T., and Best P.J. Place cells and silent cells in the hippocampus of freely-behaving rats. J Neurosci 9 (1989) 2382-2390
28. Thompson L.T., and Best P.J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 19 509 (1990) 299-308
29. Liu X., Muller R.U., Huang L.T., et al. Seizure-induced changes in place cell physiology: relationship to spatial memory. J Neurosci 23 (2003) 11505-11515
30. Rutten A., van Albada M., Silveira D.C., et al. Memory impairment following status epilepticus in immature rats: time-course and environmental effects. Eur J Neurosci 16 (2002) 501-513
31. Jones M.W. A comparative review of rodent prefrontal cortex and working memory. Curr Mol Med 2 (2002) 639-647
32. Ragozzino M.E., Adams S., and Kesner R.P. Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav Neurosci 112 (1998) 293-303
33. Morris R.G. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23 (2006) 2829-2846
34. Morris R. Theories of hippocampal function. In: Andersen P., Morris R., Amaral D., Bliss T., and O'Keefe J. (Eds). The hippocampus book (2007), Oxford Univ. Press, Oxford 581-713
35. Zhou J.L., Shatskikh T.N., Liu X., and Holmes G.L. Impaired single cell firing and long-term potentiation parallels memory impairment following recurrent seizures. Eur J Neurosci 25 (2007) 3667-3677
36. Rivard B., Li Y., Lenck-Santini P.P., Poucet B., and Muller R.U. Representation of objects in space by two classes of hippocampal pyramidal cells. J Gen Physiol 124 (2004) 9-25
37. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 4th ed. (1998), Academic Press, San Diego
38. Skaggs W.E., McNaughton B.L., Gothard K.M., and Markus E.J. An information-theoretic approach to deciphering the hippocampal code. In: Hanson S.J., Cowan J.D., and Giles C.L. (Eds). Advances in neural information processing systems (1993), Morgan Kaufmann, San Francisco 1030-1037
39. Rotenberg A., Mayford M., Hawkins R.D., Kandel E.R., and Muller R.U. Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87 (1996) 1351-1361
40. Rotenberg A., Abel T., Hawkins R.D., Kandel E.R., and Muller R.U. Parallel instabilities of long-term potentiation, place cells, and learning caused by decreased protein kinase A activity. J Neurosci 20 (2000) 8096-8102
41. Holmes G.L., Sarkisian M., Ben-Ari Y., and Chevassus-Au-Louis N. Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 404 (1999) 537-553
42. Holmes G.L., Gairsa J.L., Chevassus-Au-Louis N., and Ben-Ari Y. Consequences of neonatal seizures in the rat: morphological and behavioral effects. Ann Neurol 44 (1998) 845-857
43. Cavazos J.E., and Sutula T.P. Progressive neuronal loss induced by kindling: a possible mechanism for mossy fiber synaptic reorganization and hippocampal sclerosis. Brain Res 527 (1990) 1-6
44. Cavazos J.E., Golarai G., and Sutula T.P. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci 11 (1991) 2795-2803
45. Huang L., Cilio M.R., Silveira D.C., et al. Long-term effects of neonatal seizures: a behavioral, electrophysiological, and histological study. Brain Res Dev Brain Res 118 (1999) 99-107
46. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Clarendon, Oxford
47. Muller R. A quarter of a century of place cells. Neuron 17 (1996) 813-822
48. Lenck-Santini P.P., Muller R.U., Save E., and Poucet B. Relationships between place cell firing fields and navigational decisions by rats. J Neurosci 22 (2002) 9035-9047
49. Lenck-Santini P.P., Save E., and Poucet B. Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 11 (2001) 377-390
50. Rigoulot M.A., Koning E., Ferrandon A., and Nehlig A. Neuroprotective properties of topiramate in the lithium-pilocarpine model of epilepsy. J Pharmacol Exp Ther 308 (2004) 787-795
51. Francois J., Koning E., Ferrandon A., and Nehlig A. The combination of topiramate and diazepam is partially neuroprotective in the hippocampus but not antiepileptogenic in the lithium-pilocarpine model of temporal lobe epilepsy. Epilepsy Res 72 (2006) 147-163
52. Park H.J., Kim H.J., Park H.J., et al. Protective effect of topiramate on kainic acid-induced cell death in mice hippocampus. Epilepsia 49 (2008) 163-167
53. Kubera M., Budziszewska B., Jaworska-Feil L., et al. Effect of topiramate on the kainate-induced status epilepticus, lipid peroxidation and immunoreactivity of rats. Pol J Pharmacol 56 (2004) 553-561
54. Frisch C., Kudin A.P., Elger C.E., Kunz W.S., and Helmstaedter C. Amelioration of water maze performance deficits by topiramate applied during pilocarpine-induced status epilepticus is negatively dose-dependent. Epilepsy Res 73 (2007) 173-180
55. Kang H., Sun L.D., Atkins C.M., Soderling T.R., Wilson M.A., and Tonegawa S. An important role of neural activity-dependent CaMKIV signaling in the consolidation of long-term memory. Cell 106 (2001) 771-783
56. Brazhnik E.S., Muller R.U., and Fox S.E. Muscarinic blockade slows and degrades the location-specific firing of hippocampal pyramidal cells. J Neurosci 23 (2003) 611-621