Impaired activation of CA3 pyramidal neurons in the epileptic hippocampus

NeuroMolecular Medicine

Volumn 7, Issue 4, 2005, Pages 325-342

  Biagini, Giuseppe ^a   D'Arcangelo, Giovanna ^b   Baldelli, Enrica ^a   D'Antuono, Margherita ^c   Tancredi, Virginia ^b   Avoli, Massimo ^c,d  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c MCGILL UNIVERSITY   (Canada)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Entorhinal cortex; Hippocampus; Immediate early genes; Intrinsic optical signals; Pilocarpine; Temporal lobe epilepsy

Indexed keywords

PILOCARPINE; TRANSCRIPTION FACTOR FOSB;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DENTATE GYRUS; ENTORHINAL CORTEX; EPILEPTIC DISCHARGE; EPILEPTIC STATE; HIPPOCAMPUS; IMMUNOREACTIVITY; LIMBIC SYSTEM; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE INJURY; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SUBICULUM; TEMPORAL LOBE EPILEPSY;

ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENTORHINAL CORTEX; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; NEURAL PATHWAYS; NEURONS; PILOCARPINE; PROTO-ONCOGENE PROTEINS C-FOS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS;

ANIMALIA;

EID: 29244451875     PISSN: 15351084     EISSN: None     Source Type: Journal    
DOI: 10.1385/NMM:7:4:325     Document Type: Article

References (59)

1. Andersson M., Hilbertson A., and Cenci M. A. (1999) Striatal fosB expression is causally linked with L-DOPA-induced abnormal involuntary movements and the associated upregulation of striatal prodynorphin mRNA in a rat model of Parkinson's disease. Neurobiol. Dis. 6, 461-474.
2. André V., Ferrandon A., Marescaux C., and Nehlig A. (2000) The lesional and epileptogenic consequences of lithium-pilocarpine-induced status epilepticus are affected by previous exposure to isolated seizures: effects of amygdala kindling and maximal electroshocks. Neuroscience 99, 469-481.
3. Andrew R. D., Adams J. R., and Polischuk T. M. (1996) Imaging kainate and NMDA-induced intrinsic optical signals from the hippocampal slice. J. Neurophysiol. 76, 2707-2717.
4. Avoli M., D'Antuono M., Louvel J., et al. (2002) Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system. Prog. Neurobiol. 68, 167-207.
5. Barbarosie M. and Avoli M. (1997) CA3-driven hippocampal-entorhinal loop controls rather than sustains in vitro limbic seizures. J. Neurosci. 17, 9308-9314.
6. Barbarosie M., Louvel J., Kurcewicz I., and Avoli M. (2000) CA3-released entorhinal seizures disclose dentate gyrus epileptogenicity and unmask a temporoammonic pathway. J. Neurophysiol. 83, 1115-1124.
7. Barbarosie M., Louvel J., D'Antuono M., Kurcewicz I., and Avoli M. (2002) Masking synchronous GABA-mediated potentials controls limbic seizures. Epilepsia 43, 1469-1479.
8. Bartolomei F., Wendling F., Bellanger J. J., Regis J., and Chauvel P. (2001) Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin. Neurophysiol. 112, 1746-1760.
9. Biagini G., Pich E. M., Carani C., et al. (1993) Indole-pyruvic acid, a tryptophan ketoanalogue, antagonizes the endocrine but not the behavioral effects of repeated stress in a model of depression. Biol. Psychiatry 33, 712-719.
10. Biagini G., Babinski K., Avoli M., Marcinkiewicz M., and Sequela P. (2001) Regional and subunit-specific downregulation of acid-sensing ion channels in the pilocarpine model of epilepsy. Neurobiol. Dis. 8, 45-58.
11. o. Brain Res. 590, 128-135.
12. Chase T. D., Carrey N., Brown R. E., and Wilkinson M. (2005) Methylphenidate differentially regulates c-fos and fosB expression in the developing rat striatum. Dev. Brain Res. 157, 181-191.
13. Chen J., Kelz M. B., Hope B. T., Nakabeppu Y., and Nestler E. J. (1997) Chronic Fos-related antigens: stable variants of ΔFosB induced in brain by chronic treatments. J. Neurosci. 17, 4933-4941.
14. D'Antuono M., Benini R., Biagini G., et al. (2002) Limbic network interactions leading to hyperexcitability in a model of temporal lobe epilepsy. J. Neurophysiol. 87, 634-639.
15. D'Arcangelo G., Tancredi V., and Avoli M. (2001) Intrinsic optical signals and electrographic seizures in the rat limbic system. Neurobiol. Dis. 8, 993-1005.
16. D'Arcangelo G., Panuccio G., Tancredi V., and Avoli M. (2005) Repetitive low-frequency stimulation reduces epileptiform synchronization in limbic neuronal networks. Neurobiol. Dis. 19, 119-128.
17. Dalby N. O. and Mody I. (2001) The process of epileptogenesis: a pathophysiological approach. Cur. Op. Neurol. 14, 187-192.
18. de Curtis M. and Avanzini G. (2001) Interictal spikes in focal epileptogenesis. Prog. Neurobiol. 63, 541-567.
19. Du F., Eid T., Lothman E. W., Köhler C., and Schwarcz R. (1995) Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J. Neurosci. 15, 6301-6313.
20. Esclapez M., Hirsch J. C., Ben-Ari Y., and Bernard C. (1999) Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporallobe epilepsy. J. Comp. Neurol. 408, 449-460.
21. Fabene P. F., Marzola P., Sbarbati A., and Bentivoglio M. (2003) Magnetic resonance imaging of changes elicited by status epilepticus in the rat brain: diffusion-weighted and T2-weighted images, regional blood volume maps, and direct correlation with tissue and cell damage. Neuroimage 18, 375-389.
22. Gloor P. (1997) The Temporal Lobe and Limbic System. Oxford University Press, New York.
23. Goussakov I. V., Fink K., Elger C. E., and Beck H. (2000) Metaplasticity of mossy fiber synaptic transmission involves altered release probability. J. Neurosci. 20, 3434-3441.
24. Gutierrez R. (2003) The GABAergic phenotype of the " glutamatergic" granule cells of the dentate gyrus. Prog. Neurobiol. 71, 337-358.
25. Hauser W. A. and Kurland L. T. (1975) The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia 16, 1-66.
26. Jarvis C. R., Lilge L., Vipond G. J., and Andrew R. D. (1999) Interpretation of intrinsic optical signals and calcein fluorescence during acute excitotoxic insult in the hippocampal slice. Neuroimage 10, 357-372.
27. Jefferys J. G. (1999) Hippocampal sclerosis and temporal lobe epilepsy : cause or consequence? [Editorial]. Brain 122, 1007-1008.
28. Ji L. L., Fleming T., Penny M. L., Toney G. M., and Cunningham J. T. (2005) Effects of water deprivation and rehydration on c-Fos and FosB staining in the rat supraoptic nucleus and lamina terminalis region. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R311-R321.
29. Kohler C. (1988) Intrinsic connections of the retrohippocampal region in the rat brain. III. The lateral entorhinal cortex. J. Comp. Neurol. 271, 208-228.
30. Köhling R., Lucke A., Nagao T., Speckmann E. J., and Avoli M. (1995) Extracellular potassium elevations in the hippocampus of rats with long-term pilocarpine seizures. Neurosci. Lett. 201, 87-91.
31. Liu Z., Nagao T., Desjardins G. C., Gloor P., and Avoli M. (1994) Quantitative evaluation of neuronal loss in the dorsal hippocampus in rats with long-term pilocarpine seizures. Epilepsy Res. 17, 237-247.
32. MacVicar B. and Hochman D. (1991) Imaging of synaptically evoked intrinsic optical signals in hippocampal slices. J. Neurosci. 11, 1458-1469.
33. Mathern G. W., Babb T. L., and Armstrong D. L. (1997) Hippocampal sclerosis. In: Engel J, Pedley T. A., eds. Epilepsy: A Comprehensive Textbook. Philadelphia (PA): Lippincott-Raven; 1997, pp. 133-155.
34. McClung C. A., Ulery P. G., Perrotti L. I., Zachariou V., Berton O., and Nestler E. J. (2004) DeltaFosB: a molecular switch for long-term adaptation in the brain. Mol. Brain Res. 132, 146-154.
35. McCormick D. A. and Contreras D. (2001) On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 63, 815-846.
36. McNamara J. O. (1994) Cellular and molecular basis of epilepsy. J. Neurosci. 14, 3413-3425.
37. Mikkonen M., Soininen H., Kalvianen R., et al. (1998) Remodeling of neuronal circuitries in human temporal lobe epilepsy: increased expression of highly polysialylated neural cell adhesion molecule in the hippocampus and the entorhinal cortex. Ann. Neurol. 44, 923-934.
38. Mohapel P., Zhang X., Gillespie G. W., et al. (2001) Kindling of claustrum and insular cortex: comparison to perirhinal cortex in the rat. Eur. J. Neurosci. 13, 1501-1519.
39. Morris T. A., Jafari N., and DeLorenzo R. J. (2000) Chronic DeltaFosB expression and increased AP-1 transcription factor binding are associated with the long term plasticity changes in epilepsy. Mol. Brain. Res. 79, 138-149.
40. Naber P. A., Lopes da Silva F. H., and Witter M. P. (2001) Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 and the subiculum. Hippocampus 11, 99-104.
41. Nagao T., Avoli M., and Gloor P. (1994) Interictal discharges in the hippocampus of rats with long-term pilocarpine seizures. Neurosci. Lett. 174, 160-164.
42. Nagao T., Alonso A., and Avoli M. (1996) Epileptiform activity induced by pilocarpine in the rat hippocampal-entorhinal slice preparation. Neuroscience 72, 399-408.
43. Paxinos G. and Watson C. (1998) The Rat Brain in Stereotaxic Coordinates. Fourth ed. Academic, San Diego.
44. Racine R. J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294.
45. Rutecki P. A., Grossman R. G., Armstrong D., and Irish-Loewen S. (1989) Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J. Neurosurg. 70, 667-675.
46. Schmued L. C., Albertson C., and Slikker W. Jr. (1997) Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 751, 37-46.
47. Spencer S. S. and Spencer D. D. (1994) Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 35, 721-727.
48. Swartzwelder H. S., Lewis D. V., Anderson W. W., and Wilson W. A. (1987) Seizure-like events in brain slices: suppression by interictal activity. Brain Res. 410, 362-366.
49. Traynelis S. F. and Dingledine R. (1988) Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J. Neurophysiol. 59, 259-276.
50. Turski W. A., Cavalheiro E. A., Schwarz M., Czuczwar S. J., Kleinrok Z., and Turski L. (1983) Limbic seizures produced by pilocarpine in rats: behavioral, electroencephalographic and neuropathological study. Behav. Brain Res. 9, 315-335.
51. Weissinger F., Buchheim K., Siegmund H., and Meierkord H. (2005) Seizure spread through the life cycle: optical imaging in combined brain slices from immature, adult, and senile rats in vitro. Neurobiol. Dis. 19, 84-95.
52. Werme M., Messer C., Olson L., et al. (2002) ΔFosB regulates wheel running. J. Neurosci. 22, 8133-8138.
53. Wiebe S., Blume W. T., Girvin J. P., and Eliasziw M. (2001) A randomized, controlled trial of surgery for temporal lobe epilepsy. N. Engl. J. Med. 345, 311-318.
54. Wilson W. A., Swartzwelder H. S., Anderson W. W., and Lewis D. V. (1988) Seizure activity in vitro: a dual focus model. Epilepsy Res. 2, 289-293.
55. Witter M. P., Griffioen A. W., Jorritsma-Byham B., and Krijnen J. L. (1988) Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci. Lett. 85, 193-198.
56. Witter M. P., Groenewegen H. J., Lopes da Silva F. H., and Lohman A. H. M. (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33, 161-253.
57. Wozny C., Gabriel S., Jandova K., Schulze K., Heinemann U., and Behr J. (2005) Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol. Dis. 19, 451-460.
58. Wu K. and Leung L. S. (2001) Enhanced but fragile inhibition in the dentate gyrus in vivo in the kainic acid model of temporal lobe epilepsy: a study using current source density analysis. Neuroscience 104, 379-396.
59. Wu K. and Leung L. S. (2003) Increased dendritic excitability in hippocampal CA1 in vivo in the kainic acid model of temporal lobe epilepsy: a study using current source density analysis. Neuroscience 116, 599-616.