Recurrent excitation in the dentate gyrus of a murine model of temporal lobe epilepsy

Epilepsy Research

Volumn 58, Issue 2-3, 2004, Pages 93-105

  Winokur, Ronald S ^a   Kubal, Timothy ^a   Liu, Dan ^a   Davis, Scott F ^a   Smith, Bret N ^a  

^a Tulane University   (United States)

Author keywords

Glutamate photolysis; Granule cell; Mossy fiber; Mouse; Pilocarpine; Synaptic reorganization

Indexed keywords

BICUCULLINE; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DENTATE GYRUS; ELECTROSTIMULATION; EPILEPTOGENESIS; GRANULE CELL; HIPPOCAMPUS; LATENT PERIOD; MALE; MOUSE; NERVE SPROUTING; NERVE STIMULATION; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; SEIZURE; SYNAPSE; TEMPORAL LOBE EPILEPSY;

ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID ANTAGONISTS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; PILOCARPINE;

EID: 2142824184     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2004.01.002     Document Type: Article

References (42)

1. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 42:1991;351-363
2. Ben-Ari Y. Limbic seizures and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403
3. Ben-Ari Y., Tremblay E., Riche D., Ghilini G., Naquet R. Electroencephalographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience. 6:1981;1361-1391
4. Borges K., Gearing M., McDermott D.L., Smith A.B., Almonte A.G., Wainer B.H., Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp. Neurol. 182:2003;21-34
5. Bouilleret V., Ridoux V., Depaulis A., Marescauz C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology, and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience. 89:1999;717-729
6. Bouilleret V., Schwaller B., Schurmans S., Celio M.R., Fritschy J.M. Neurodegenerative and morphogenic changes in a mouse model of temporal lobe epilepsy do not depend on the expression of the calcium-binding proteins parvalbumin, calbindin, or calretinin. Neuroscience. 97:2000;47-58
7. Buckmaster P.S., Zhang G.F., Yamawaki R. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. J. Neurosci. 22:2002;6650-6658
8. Callaway E.M., Katz L.C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA. 90:1993;7661-7665
9. Cantallops I., Routenberg A. Kainic acid induction of mossy fiber sprouting: dependence on mouse strain. Hippocampus. 10:2000;269-273
10. Cavalheiro E.A., Santos N.F., Priel M.R. The pilocarpine model of epilepsy in mice. Epilepsia. 37:1996;1015-1019
11. Colling S.B., Khana M., Collinge J., Jeffreys J.G.R. Mossy fibre reorganization int eh hippocampus of prion protein null mice. Brain Res. 755:1997;28-35
12. Cronin J., Dudek F.E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474:1988;181-184
13. Davis S.F., Williams K.W., Xu W., Glatzer N.R., Smith B.N. Selective enhancement of synaptic inhibition by hypocretin (orexin) in rat vagal motor neurons: implications for autonomic regulation. J. Neurosci. 23:2003;3844-3854
14. Dudek F.E., Spitz M. Hypothetical mechanisms for the cellular and neurophysiologic basis of secondary epileptogenesis: proposed role of synaptic reorganization. J. Clin. Neurophysiol. 14:1997;90-101
15. Esclapez M., Hirsch J.C., Ben-Ari Y., Bernard C. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J. Comp. Neurol. 408:1999;449-460
16. Franck J.E., Pokorny J., Kunkel D.D., Schwartzkroin P.A. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia. 36:1995;543-558
17. Golarai G., Cavazos J.E., Sutula T.P. Activation of the dentate gyrus by pentylenetetrazol evoked seizures induces mossy fiber synaptic reorganization. Brain Res. 593:1992;257-264
18. Hellier J.L., Patrylo P.R., Buckmaster P.S., Dudek F.E. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res. 31:1998;73-84
19. Lynch M., Sutula T. Recurrent excitatory connectivity in the dentate gyrus of kindled and kainic acid-treated rats. J. Neurophysiol. 83:2000;693-704
20. Mayer M.L., Westbrook G.L., Guthrie P.B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature. 309:1984;261-263
21. McKhann G.M., Wenzel H.J., Robbins C.A., Sosunov A.A., Schwartzkroin P.A. Mouse strain differences in kainic acid sensitivity, seizure behavior, mortality, and hippocampal pathology. Neuroscience. 122:2003;551-561
22. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia. 34:1993;985-995
23. Miles R., Wong R.K.S. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J. Physiol. (Lond.). 373:1986;397-418
24. Molnar P., Nadler J.V. Mossy fiber-granule cell synapses in the normal and epileptic rat dentate gyrus studied with minimal laser photostimulation. J. Neurophysiol. 82:1999;1883-1894
25. Nadler J.V., Perry B.W., Cotman C.W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182:1980;1-9
26. Patrylo P.R., Dudek F.E. Physiological unmasking of new glutamatergic pathways in the dentate gyrus of hippocampal slices from kainate-induced epileptic rats. J. Neurophysiol. 79:1998;418-429
27. Perez Y., Morin F., Beaulieu C., Lacaille J.-C. Axonal sprouting of CA1 pryamidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur. J. Neurosci. 8:1996;736-748
28. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor seizures. Electorencephalogr. Clin. Neurophysiol. 32:1972;281-294
29. Schauwecker P.E., Ramirez J.J., Steward O. Genetic dissection of the signals that induce synaptic reorganization. Exp. Neurol. 161:2000;139-152
30. Schauwecker P.E., Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. 94:1997;4103-4108
31. Shibley H., Smith B.N. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res. 49:2002;109-120
32. Smith B.N., Dudek F.E. Enhanced population responses in the basolateral amygdala of kainate-treated, epileptic rats in vitro. Neurosci. Lett. 222:1997;1-4
33. Smith B.N., Dudek F.E. Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J. Neurophysiol. 85:2001;1-9
34. Smith B.N., Dudek F.E. Network interactions mediated by new excitatory connections between CA1 pyramidal cells in rats with kainate-induced epilepsy. J. Neurophysiol. 87:2002;1655-1658
35. Stanfield B.B. Excessive intra- and supragranular mossy fibers in the dentate gyrus of tottering (tg/tg) mice. Brain Res. 480:1989;294-299
36. Steward O., Schauwecker P.E., Guth L., Zhang Z., Fujiki M., Inman D., Wrathall J., Kempermann G., Gage F.H., Saatman K.E., Raghupathi R., McIntosh T. Genetic approaches to neurotrauma research: opportunities and potential pitfalls of murine models. Exp. Neurol. 157:1999;19-42
37. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26:1989;321-330
38. Tauck D.L., Nadler J.V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5:1985;1016-1022
39. Turski W.A., Cavalheiro E.A., Bortolotto Z.A., Mello L.M., Schwartz M., Turski L. Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 321:1984;237-253
40. Wenzel H.J., Robbins C.A., Tsai L.-H., Schwartzkroin P.A. Abnormal morphological and functional organization of the hippocampus in a p35 mutant model of cortical dysplasia associated with spontaneous seizures. J. Neurosci. 21:2001;983-998
41. Wuarin J.-P., Dudek F.E. Electrographic seizures and new recurrent excitatory circuits in the dentate gyrus of hippocampal slices from kainate-treated epileptic rat. J. Neurosci. 16:1996;4438-4448
42. Wuarin J.-P., Dudek F.E. Excitatory synaptic input to granule cells increases with time after kainate treatment. J. Neurophysiol. 85:2001;1067-1077