Cell domain-dependent changes in the glutamatergic and GABAergic drives during epileptogenesis in the rat CA1 region

Journal of Physiology

Volumn 578, Issue 1, 2007, Pages 193-211

  El hassar, Lynda ^a   Milh, Mathieu ^a   Wendling, Fabrice ^b   Ferrand, Nadine ^a   Esclapez, Monique ^a   Bernard, Christophe ^a,c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; PILOCARPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DISEASE; CONTROLLED STUDY; DENDRITE; DISEASE ACTIVITY; DISEASE COURSE; EPILEPTOGENESIS; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IN VIVO STUDY; LATENT PERIOD; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; ADULT; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUTAMATERGIC SYNAPSE; HIPPOCAMPAL CA1 REGION; MALE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY;

ALGORITHMS; ANIMALS; DENDRITES; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; EPILEPSY; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; HIPPOCAMPUS; MALE; MUSCARINIC AGONISTS; NEURONS; PILOCARPINE; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33845773857     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.119297     Document Type: Article

References (60)

1. Avoli M, D'Antuono M, Louvel J, Kohling R, Biagini G, Pumain R, D'Arcangelo G & Tancredi V (2002). Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 68, 167-207.
2. Bartolomei F, Wendling F, Bellanger JJ, Regis J & Chauvel P (2001). Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112, 1746-1760.
3. Bausch SB (2005). Axonal sprouting of GABAergic interneurons in temporal lobe epilepsy. Epilepsy Behav 7, 390-400.
4. Bernard C (2005). Dogma and dreams: Experimental lessons for epilepsy mechanism chasers. Cell Mol Life Sci 62, 1177-1181.
5. Bernard C, Anderson A, Becker A, Poolos NP, Beck H & Johnston D (2004). Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532-535.
6. Bernard C & Wheal H (1994). A model of the connectivity patterns in the CA3 and CA1 areas of the hippocampus. Hippocampus 4, 497-529.
7. Bourien J, Bartolomei F, Bellanger JJ, Gavaret M, Chauvel P & Wendling F (2005). A method to identify reproducible subsets of co-activated structures during interictal spikes. Application to intracerebral EEG in temporal lobe epilepsy. Clin Neurophysiol 116, 443-455.
8. Brooks-Kayal AR, Shumate MD, Jin H, Rikhter TY & Coulter DA (1998). Selective changes in single cell GABA A receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4, 1166-1172.
9. Buzsaki G (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340.
10. Cavazzuti GB, Cappella L & Nalin A (1980). Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 21, 43-55.
11. Christian E & Dudek F (1988). Electrophysiological evidence from glutamate microapplications for local excitatory circuits in the CA1 area of rat hippocampal slices. J Neurophysiol 59, 110-123.
12. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC & Rubenstein JL (2005). Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8, 1059-1068.
13. Cohen I, Navarro V, Clemenceau S, Baulac M & Miles R (2002). On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418-1421.
14. Cossart R, Hirsch JC, Cannon RC, Dinoncourt C, Wheal HV, Ben-Ari Y, Esclapez M & Bernard C (2000). Distribution of spontaneous currents along the somato-dendritic axis of rat hippocampal CA1 pyramidal neurons. Neuroscience 99, 593-603.
15. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M & Bernard C (2001). Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4, 52-62.
16. Cossart R, Bernard C & Ben-Ari Y (2005). Multiple facets of GABAergic neurons and synapses: Multiple fates of GABA signalling in epilepsies. Trends Neurosci 28, 108-115.
17. Dinocourt C, Petanjek Z, Freund TF, Ben Ari Y & Esclapez M (2003). Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459, 407-425.
18. Doherty J & Dingledine R (2001). Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus. J Neurosci 21, 2048-2057.
19. Engel J Jr (1996). Introduction to temporal lobe epilepsy. Epilepsy Res 26, 141-150.
20. Esclapez M, Hirsch JC, Ben Ari Y & Bernard C (1999). Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408, 449-460.
21. Esclapez M, Hirsch JC, Khazipov R, Ben-Ari Y & Bernard C (1997). Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc Natl Acad Sci U S A 94, 12151-12156.
22. Freund TF & Buzsáki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
23. Goodkin HP, Yeh JL & Kapur J (2005). Status epilepticus increases the intracellular accumulation of GABA A receptors. J Neurosci 25, 5511-5520.
24. Gorter JA, van Vliet EA, Aronica E & Lopes da Silva FH (2002). Long-lasting increased excitability differs in dentate gyrus vs. CA1 in freely moving chronic epileptic rats after electrically induced status epilepticus. Hippocampus 12, 311-324.
25. Hellier JL, Patrylo PR, Dou P, Nett M, Rose GM, Dudek FE (1999). Assessment of inhibition and epileptiform activity in the septal dentate gyrus of freely behaving rats during the first week after kainate treatment. J Neurosci 19, 10053-10064.
26. Herman ST (2002). Epilepsy after brain insult: Targeting epileptogenesis. Neurology 59, S21-S26.
27. Hirsch JC, Agassandian C, Merchan-Perez A, Ben-Ari Y, DeFelipe J, Esclapez M & Bernard C (1999). Deficit of quantal release of GABA in experimental models of temporal lobe epilepsy. Nat Neurosci 2, 499-500.
28. Ishizuka N, Weber J & Amaral D (1990). Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295, 580-623.
29. Kobayashi M & Buckmaster PS (2003). Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23, 2440-2452.
30. Kobayashi M, Wen X & Buckmaster PS (2003). Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 23, 8471-8479.
31. Leung LW, Lopes da Silva FH & Wadman WJ (1982). Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol 54, 203-219.
32. Liu G (2004). Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7, 373-379.
33. Lopes da Silva F (2002). Electrical potentials. In Encyclopedia of the Human Brain, vol. 2, ed. Ramachandran VS, pp. 147-167. Elsevier, New York.
34. Magee JC & Cook EP (2000). Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3, 895-903.
35. Magee J, Hoffman D, Colbert C & Johnston D (1998). Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60, 327-346.
36. Mangan PS & Bertram EH III (1998). Ontogeny of altered synaptic function in a rat model of chronic temporal lobe epilepsy. Brain Res 799, 183-196.
37. Megias M, Emri Z, Freund TF & Gulyas AI (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527-540.
38. Miles R, Toth K, Gulyás AI, Hajos N & Freund TF (1996). Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815-823.
39. Miles R & Wong R (1987). Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388, 611-629.
40. Obenaus A, Esclapez M & Houser CR (1993). Loss of glutamate decarboxylase mRNA-conatining neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 13, 4470-4485.
41. Perez Y, Morin F, Beaulieu C & Lacaille J-C (1996). Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur J Neurosci 8, 736-748.
42. Sanabria ER, Su H & Yaari Y (2001). Initiation of network bursts by CaINSERM U751 Facultéde Médecine Timone 27 Bd Jean Moulin 13385 Marseille Cedex 05; -dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J Physiol 532, 205-216.
43. 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.
44. Shao LR & Dudek FE (2005). Changes in mIPSCs and sIPSCs after kainate treatment: Evidence for loss of inhibitory input to dentate granule cells and possible compensatory responses. J Neurophysiol 94, 952-960.
45. Siddiqui AH & Joseph SA (2005). CA3 axonal sprouting in kainate-induced chronic epilepsy. Brain Res 1066, 129-146.
46. Smith BN & Dudek FE (2001). Short- and long-term changes in CA1 network excitability after kainate treatment in rats. J Neurophysiol 85, 1-9.
47. Soltesz I, Smetters DK & Mody I (1995). Tonic inhibition originates from synapses close to the soma. Neuron 14, 1273-1283.
48. Staley K, Hellier JL & Dudek FE (2005). Do interictal spikes drive epileptogenesis? Neuroscientist 11, 272-276.
49. Su H, Sochivko D, Becker A, Chen J, Jiang Y, Yaari Y & Beck H (2002). Upregulation of a T-type CaINSERM U751 Facultéde Médecine Timone 27 Bd Jean Moulin 13385 Marseille Cedex 05; channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J Neurosci 22, 3645-3655.
50. Szabadics J, Varga C, Molnar G, Olah S, Barzo P & Tamas G (2006). Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311, 233-235.
51. Thomson A & Radpour S (1991). Excitatory connections between CA1 pyramidal cells revealed by spike triggered averaging in slices of rat hippocampus are partially NMDA receptor mediated. Eur J Neurosci 3, 587-601.
52. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Wang X, Zielke HR, Kang J & Nedergaard M (2005). An astrocytic basis of epilepsy. Nat Med 11, 973-981.
53. Traub RD, Contreras D, Cunningham MO, Murray H, LeBeau FE, Roopun A, Bibbig A, Wilent WB, Higley MJ & Whittington MA (2005). Single-column thalamocortical network model exhibiting γ oscillations, sleep spindles, and epileptogenic bursts. J Neurophysiol 93, 2194-2232.
54. Traub R & Miles R (1991). Neuronal Network of the Hippocampus. Cambridge University Press, New York.
55. Wendling F, Bartolomei F, Bellanger JJ & Chauvel P (2002). Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition. Eur J Neurosci 15, 1499-1508.
56. Whittington MA, Stanford IM, Colling SB, Jefferys JG & Traub RD (1997). Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol 502, 591-607.
57. Whittington MA, Traub RD & Jefferys JG (1995). Erosion of inhibition contributes to the progression of low magnesium bursts in rat hippocampal slices. J Physiol 486, 723-734.
58. Witter MP, Wouterlood FG, Naber PA & van Haeften T (2000). Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci 911, 1-24.
59. Wozny C, Gabriel S, Jandova K, Schulze K, Heinemann U & Behr J (2005). Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol Dis 19, 451-460.
60. Yang J, Woodhall GL & Jones RS (2006). Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J Neurosci 26, 406-410.