Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro

Annals of Neurology

Volumn 64, Issue 6, 2008, Pages 674-686

  Gnatkovsky, Vadym ^a   Librizzi, Laura ^a   Trombin, Federica ^a   De Curtis, Marco ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BICUCULLINE; POTASSIUM ION;

ACTION POTENTIAL; ANIMAL TISSUE; ARTERY PERFUSION; ARTICLE; BRAIN NERVE CELL; CELL SYNCHRONIZATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; EPILEPTIC DISCHARGE; GUINEA PIG; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; ION MONITORING; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SEIZURE;

ACTION POTENTIALS; ANIMALS; ENTORHINAL CORTEX; GUINEA PIGS; INHIBITORY POSTSYNAPTIC POTENTIALS; NERVE NET; NEURAL INHIBITION; SEIZURES;

EID: 58149268009     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.21519     Document Type: Article

References (67)

1. Lieb JP, Walsh GO, Babb TL. A comparison of EEG seizure patterns recorded with surface and depth electrodes in patients with temporal lobe epilepsy. Epilepsia 1976;17:137-160.
2. Quesney LF, Gloor P. Localization of epileptic foci. Electroencephalogr Clin Neurophysiol Suppl 1985;37:165-200.
3. Engel JJ, Rausch R, Lieb JP, et al. Correlation of criteria used for localizing epileptic foci in patients considered for surgical therapy of epilepsy. Ann Neurol 1981;9:215-224.
4. Bancaud J, Angelergues R, Bernouilli C, et al. Functional stereotaxic exploration (stereo-electroencephalography) in epilepsies. Rev Neurol (Paris) 1969;120:448.
5. Fisher RS, Webber WR, Lesser RP, et al. High-frequency EEG activity at the start of seizures. J Clin Neurophysiol 1992;9:441-448.
6. Gotman J, Levtova V, Olivier A. Frequency of the electroencephalographic discharge in seizures of focal and widespread onset in intracerebral recordings. Epilepsia 1995;36:697-703.
7. Cendes F, Dubeau F, Andermann F, et al. Significance of mesial temporal atrophy in relation to intracranial ictal and interictal stereo EEG abnormalities. Brain 1996;119:1317-1326.
8. Pacia SV, Ebersole JS. Intracranial EEG in temporal lobe epilepsy. J Clin Neurophysiol 1999;16:399-407.
9. Spencer SS, Spencer DD. Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 1994;35:721-727.
10. Bartolomei F, Khalil M, Wendling F, et al. Entorhinal cortex involvement in human mesial temporal lobe epilepsy: an electrophysiologic and volumetric study. Epilepsia 2005;46:677-687.
11. Bartolomei F, Wendling F, Vignal JP, et al. Seizures of temporal lobe epilepsy: identification of subtypes by coherence analysis using stereo-electro-encephalography. Clin Neurophysiol 1999;110:1741-1754.
12. Kahane P, Chabardes S, Minotti L, et al. The role of the temporal pole in the genesis of temporal lobe seizures. Epileptic Disord 2002;4(suppl 1):S51-S58.
13. Mintzer S, Cendes F, Soss J, et al. Unilateral hippocampal sclerosis with contralateral temporal scalp ictal onset. Epilepsia 2004;45:792-802.
14. Spencer SS, Kim J, Spencer DD. Ictal spikes: a marker of specific hippocampal cell loss. Electroencephalogr Clin Neurophysiol 1992;83:104-111.
15. Wendling F, Bartolomei F, Bellanger JJ, Chauvel P. Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition. Eur J Neurosci 2002;15:1499-1508.
16. Avoli M, D'Antuono M, Louvel J, et al. Network pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Progr Neurobiol 2002;68:167-207.
17. Muhlethaler M, de Curtis M, Walton K, Llinas R. The isolated and perfused brain of the guinea-pig in vitro. Eur J Neurosci 1993;5:915-926.
18. de Curtis M, Biella G, Buccellati C, Folco G. Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res Protoc 1998;3:221-228.
19. Uva L, Librizzi L, Wendling F, de Curtis M. Propagation dynamics of epileptiform activity acutely induced by bicuculline in the hippocampal- parahippocampal region of the isolated Guinea pig brain. Epilepsia 2005;46:1914-1925.
20. Librizzi L, de Curtis M. Epileptiform ictal discharges are prevented by periodic interictal spiking in the olfactory cortex. Ann Neurol 2003;53:382-389.
21. Avoli M, D'Antuono M, Louvel J, et al. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 2002;68:167-207.
22. Bragin A, Csicsvari J, Penttonen M, Buzsaki G. Epileptic after-discharge in the hippocampal-entorhinal system: current source density and unit studies. Neuroscience 1997;76:1187-1203.
23. Pare D, de Curtis M, Llinas R. Role of the hippocampalentorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro. J Neurosci 1992;12:1867-1881.
24. Wozny C, Gabriel S, Jandova K, et al. Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol Dis 2005;19:451-460.
25. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 1989;33:161-253.
26. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AH. Anatomic organization and physiology of the limbic cortex. Physiol Rev 1990;70:453-511.
27. Witter MP, Wouterlood F. The parahippocampal region. Organization and role in cognitive functions. Oxford: Oxford University Press, 2002.
28. Bartesaghi R, Gessi T, Sperti L. Electrophysiological analysis of the hippocampal projections to the entorhinal area. Neuroscience 1989;30:51-62.
29. Deadwyler SA, West JR, Cotman CW, Lynch G. Physiological studies of the reciprocal connections between the hippocampus and entorhinal cortex. Exp Neurol 1975;49:35-57.
30. Jones RSG, Heinemann V. Synaptic and intrinsic responses of medial entorhinal cortical cells in normal and magnesium-free medium in vitro. J Neurophysiol 1988;59:1476-1496.
31. Finch DM, Tan AM, Isokawa-Akesson M. Feedforward inhibition of the rat entorhinal cortex and subicular complex. J Neurosci 1988;8:2213-2226.
32. Kloosterman F, Van Haeften T, Witter MP, Lopes Da Silva FH. Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system. Eur J Neurosci 2003;18:3037-3052.
33. van Haeften T, Baks-te-Bulte L, Goede PH, et al. Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 2003;13:943-952.
34. Gnatkovsky V, de Curtis M. Hippocampus-mediated activation of superficial and deep layer neurons in the medial entorhinal cortex of the isolated guinea pig brain. J Neurosci 2006;26:873-881.
35. Kobayashi M, Wen X, Buckmaster PS. Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 2003;23:8471-8479.
36. De Guzman P, Inaba Y, Baldelli E, et al. Network hyperexcitability within the deep layers of the pilocarpine-treated rat entorhinal cortex J Physiol 2008;586:1867-1883.
37. Forti M, Biella G, Caccia S, de Curtis M. Persistent excitability changes in the piriform cortex of the isolated guinea-pig brain after transient exposure to bicuculline. Eur J Neurosci 1997;9:435-451.
38. de Curtis M, Manfridi A, Biella G. Activity-dependent pH shifts and periodic recurrence of spontaneous interictal spikes in a model of focal epileptogenesis. J Neurosci 1998;18:7543-7551.
39. Biella G, Panzica F, de Curtis M. Interactions between associative synaptic potentials in the piriform cortex of the in vitro isolated guinea pig brain. Eur J Neurosci 1996;8:1350-1357.
40. Librizzi L, Janigro D, De Biasi S, de Curtis M. Blood-brain barrier preservation in the in vitro isolated guinea pig brain preparation. J Neurosci Res 2001;66:289-297.
41. Gnatkovsky V, Wendling F, de Curtis M. Cellular correlates of spontaneous periodic events in the medial entorhinal cortex of the in vitro isolated guinea pig brain. Eur J Neurosci 2007;26:302-311.
42. Dunwiddie TV, Worth TS, Olsen RW. Facilitation of recurrent inhibition in rat hippocampus by barbiturate and related nonbarbiturate depressant drugs. J Pharmacol Exp Ther 1986;238:564-575.
43. Wendling F, Hernandez A, Bellanger JJ, et al. Interictal to ictal transition in human temporal lobe epilepsy: insights from a computational model of intracerebral EEG. J Clin Neurophysiol 2005;22:343-356.
44. Labyt E, Uva L, de Curtis M, Wendling F. Realistic modeling of entorhinal cortex field potentials and interpretation of epileptic activity in the guinea pig isolated brain preparation. J Neurophysiol 2006;96:363-377.
45. Biella G, de Curtis M. Olfactory inputs activate the medial entorhinal cortex via the hippocampus. J Neurophysiol 2000;83:1924-1931.
46. Perrault P, Avoli M. 4-Aminopyridine-induced activity in hilar neurons in the guinea pig hippocampal slice. J Neurosci 1992;12:104-115.
47. Avoli M, Barbarosie M, Lücke A, et al. Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J Neurosci 1996;16:3912-3924.
48. Lopantsev V, Avoli M. Laminar organization of epileptiform discharges in the rat entorhinal cortex in vitro. J Physiol 1998;509:785-796.
49. Lopantsev V, Avoli M. Participation of GABAA-mediated inhibition in ictallike discharges in the rat entorhinal cortex. J Neurophysiol 1998;79:352-360.
50. Chrobak JJ, Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 1998;18:388-398.
51. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003;37:311-322.
52. Traub RD, Whittington MA, Buhl EH, et al. On the mechanism of the gamma 3 beta frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation. J Neurosci 1999;19:1088-1105.
53. Bracci E, Vreugdenhil M, Hack SP, Jefferys JGR. On the synchronizing mechanisms of tetanically induced hippocampal oscillations. J Neurosci 1999;19:8104-8113.
54. Traub RD, Jefferys JGR, Whittington MA. Fast oscillations in cortical circuits. Cambridge, MA: MIT Press, 1999.
55. Fisahn A, Pike FG, Buhl EH, Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 1998;394:186-189.
56. Williams JH, Kauer JA. Properties of carcachol-induced oscillatory activity in the rat hippocampus. J Neurophysiol 1997;78:2631-2640.
57. van der Linden S, de Curtis M, Panzica F. Carbachol induces fast oscillations in the medial but not in the later entorhinal cortex of the isolated guinea pig brain. J Neurophysiol 1999;82:2441-2450.
58. Dickson CT, Biella G, de Curtis M. Evidence for spatial modules mediated by temporal synchronisation of carbachol induced gamma rhythm in medial entorhinal cortex. J Neurosci 2000;20:7846-7854.
59. A receptor-mediated oscillations. J Neurosci 2000;20:6820-6829.
60. Velazquez JLP, Carlen PL. Synchronization of GABAergic interneuronal networks during seizure-like actvity in the rat horizontal hippocampal slice. Eur J Neurosci 1999;11:4110-4118.
61. Tolner EA, Kloosterman F, Kalitzin SN, et al. Physiological changes in chronic epileptic rats are prominent in superficial layers of the medial entorhinal area. Epilepsia 2005;46(suppl 5):72-81.
62. Fujiwara-Tsukamoto Y, Isomura Y, Kaneda K, Takada M. Synaptic interactions between pyramidal cells and interneurone subtypes during seizure-like activity in the rat hippocampus. J Physiol 2004;557:961-979.
63. Bragin A, Wilson CL, Staba RJ, et al. Interictal high-frequency oscillations (80-500 Hz) in the human epileptic brain: entorhinal cortex. Ann Neurol 2002;52:407-415.
64. Staba RJ, Wilson CL, Bragin A, et al. Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 2002;88:1743-1752.
65. Bragin A, Engel J, Wison CL. Hippocampal and entorhinal cortex high-frequency oscillations in human epileptic brain and kainic acid treated rats. Epilepsia 1999;40:127-137.
66. Farrant M, Kaila K. The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 2007;160:59-87.
67. Thompson SM, Gahwiler BH. Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. J Neurophysiol 1989;61:512-523.