Seizure-like discharges induced by 4-aminopyridine in the olfactory system of the in vitro isolated guinea pig brain

Epilepsia

Volumn 54, Issue 4, 2013, Pages 605-615

  Uva, Laura ^a   Trombin, Federica ^a   Carriero, Giovanni ^a   Avoli, Massimo ^b   De Curtis, Marco ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Epileptic network; Piriform cortex; System epilepsy

Indexed keywords

4 AMINOPYRIDINE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY PERFUSION; ARTICLE; BRAIN; CELL MEMBRANE DEPOLARIZATION; CELL STRUCTURE; ELECTRODE; ENTORHINAL CORTEX; GUINEA PIG; HEMISPHERE; IN VITRO STUDY; LIMBIC CORTEX; NERVE CELL; NERVE POTENTIAL; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; PYRIFORM CORTEX; SEIZURE;

4-AMINOPYRIDINE; ANIMALS; EXTRACELLULAR SPACE; GUINEA PIGS; LIMBIC SYSTEM; MEMBRANE POTENTIALS; MICROELECTRODES; NERVE NET; NEURONS; OLFACTORY PATHWAYS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; SEIZURES;

EID: 84875858379     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/epi.12133     Document Type: Article

References (64)

1. Avanzini G, Manganotti P, Meletti S, Moshe SL, Panzica F, Wolf P, Capovilla G,. (2012) The system epilepsies: a pathophysiological hypothesis. Epilepsia 53: 771-778.
2. Avoli M, Perreault P,. (1987) A GABAergic depolarizing potential in the hippocampus disclosed by the convulsant 4-aminopyridine. Brain Res 400: 191-195.
3. 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.
4. Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, van Emde Boas W, Engel J, French J, Glauser TA, Mathern GW, Moshe SL, Nordli D, Plouin P, Scheffer IE,. (2010) Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 51: 676-685.
5. Bezanilla F, Armstrong CM,. (1974) Gating currents of the sodium channels: three ways to block them. Science 183: 753-754.
6. Biella G, de Curtis M,. (2000) Olfactory inputs activate the medial entorhinal cortex via the hippocampus. J Neurophysiol 83: 1924-1931.
7. Biella GR, Gnatkovsky V, Takashima I, Kajiwara R, Iijima T, de Curtis M,. (2003) Olfactory input to the parahippocampal region of the isolated guinea pig brain reveals weak entorhinal-to-perirhinal interactions. Eur J Neurosci 18: 95-101.
8. Boeijinga PH, Van Groen T,. (1984) Inputs from the olfactory bulb and olfactory cortex to the entorhinal cortex in the cat. Exp Brain Res 57: 40-48.
9. Canning KJ, Leung LS,. (1997) Lateral entorhinal, perirhinal and amygdala-entorhinal transition projections to hippocampal CA1 or dentate gyrus in the rat: a current source density study. Hippocampus 7: 643-655.
10. Carriero G, Uva L, Gnatkovsky V, de Curtis M,. (2009) Distribution of the olfactory fiber input into the olfactory tubercle of the in vitro isolated guinea pig brain. J Neurophysiol 101: 1613-1619.
11. Carriero G, Uva L, Gnatkovsky V, Avoli M, de Curtis M,. (2010) Independent epileptiform discharge patterns in the olfactory and limbic areas of the in vitro isolated Guinea pig brain during 4-aminopyridine treatment. J Neurophysiol 103: 2728-2736.
12. Chapman AC, Racine RJ,. (1997) Converging inputs to the entorhinal cortex from the piriform cortex and medial septum: facilitation and current source density analysis. J Neurophysiol 78: 2602-2615.
13. Danober L, Deransart C, Depaulis A, Vergnes M, Marescaux C,. (1998) Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55: 27-57.
14. de Curtis M, Gnatkovsky V,. (2009) Reevaluating the mechanisms of focal ictogenesis: the role of low-voltage fast activity. Epilepsia 50: 2514-2525.
15. de Curtis M, Biella G, Forti M, Panzica F,. (1994) Multifocal spontaneous epileptic activity induced by restricted bicuculline ejection in the piriform cortex of the isolated guinea pig brain. J Neurophysiol 71: 2463-2475.
16. de Curtis M, Biella G, Buccellati C, Folco G,. (1998) Simultaneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res Protoc 3: 221-228.
17. Deadwyler SA, West JR, Cotman CW, Lynch G,. (1975) Physiological studies of the reciprocal connections between the hippocampus and entorhinal cortex. Exp Neurol 49: 35-57.
18. Demir R, Haberly LB, Jackson MB,. (1999) Sustained and accelerating activity at two discrete sites generate epileptiform discharges in slices of piriform cortex. J Neurosci 19: 1294-1306.
19. Demir R, Haberly LB, Jackson MB,. (2001) Epileptiform discharges with in-vivo-like features in slices of rat piriform cortex with longitudinal association fibers. J Neurophysiol 86: 2445-2460.
20. Derchansky M, Jahromi SS, Mamani M, Shin DS, Sik A, Carlen PL,. (2008) Transition to seizures in the isolated immature mouse hippocampus: a switch from dominant phasic inhibition to dominant phasic excitation. J Physiol 586: 477-494.
21. Dickson CT, Biella G, de Curtis M,. (2000) Evidence for spatial modules mediated by temporal synchronisation of carbachol induced gamma rhythm in medial entorhinal cortex. J Neurosci 20: 7846-7854.
22. Fujiwara-Tsukamoto Y, Isomura Y, Imanishi M, Fukai T, Takada M,. (2007) Distinct types of ionic modulation of GABA actions in pyramidal cells and interneurons during electrical induction of hippocampal seizure-like network activity. Eur J Neurosci 25: 2713-2725.
23. Galvan M, Grafe P, ten Bruggencate G,. (1982) Convulsant actions of 4-aminopyridine on the guinea-pig olfactory cortex slice. Brain Res 241: 75-86.
24. Gloor P, Fariello RG,. (1988) Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci 11: 63-68.
25. Gnatkovsky V, de Curtis M,. (2006) Hippocampus-mediated activation of superficial and deep layer neurons in the medial entorhinal cortex of the isolated guinea pig brain. J Neurosci 26: 873-881.
26. Gnatkovsky V, Uva L, de Curtis M,. (2004) Topographic distribution of direct and hippocampus- mediated entorhinal cortex activity evoked by olfactory tract stimulation. Eur J Neurosci 20: 1897-1905.
27. Gnatkovsky V, Librizzi L, Trombin F, de Curtis M,. (2008) Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann Neurol 64: 674-686.
28. Hjorth-Simonsen A, Jeune B,. (1972) Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 174: 591-606.
29. Hoffman WH, Haberly LB,. (1993) Role of synaptic excitation in the generation of bursting-induced epileptiform potentials in the endopiriform nucleus and piriform cortex. J Neurophysiol 70: 2550-2561.
30. Hoffman WH, Haberly LB,. (1996) Kindling-induced epileptiform potentials in piriform cortex slices originate in the underlying endopiriform nucleus. J Neurophysiol 76: 1430-1438.
31. Jankowska E, Lundberg A, Rudomin P, Sykova E,. (1977) Effects of 4-aminopyridine on transmission in excitatory and inhibitory synapses in the spinal cord. Brain Res 136: 387-392.
32. Khalilov I, Holmes GL, Ben-Ari Y,. (2003) In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 6: 1079-1085.
33. Kosel KC, Van Hoesen GW, West JR,. (1981) Olfactory bulb projection to the parahippocampal area of the rat. J Comp Neurol 198: 467-482.
34. Krettek JE, Price JL,. (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178: 225-254.
35. Leresche N, Lambert RC, Errington AC, Crunelli V,. (2012) From sleep spindles of natural sleep to spike and wave discharges of typical absence seizures: is the hypothesis still valid? Pflugers Arch 463: 201-212.
36. Leung LS, Roth L, Canning KJ,. (1995) Entorhinal inputs to the hippocampal CA1 and dentate gyrus in the rat: a current source density analysis. J Neurophysiol 73: 2392-2403.
37. Librizzi L, de Curtis M,. (2003) Epileptiform ictal discharges are prevented by periodic interictal spiking in the olfactory cortex. Ann Neurol 53: 382-389.
38. Liu P, Bilkey DK,. (1997) Parallel involvement of perirhinal and lateral entorhinal cortex in the polysynaptic activation of hippocampus by olfactory inputs. Hippocampus 7: 296-306.
39. Llinas R, Walton K, Bohr V,. (1976) Synaptic transmission in squid giant synapse after potassium conductance blockage with external 3- and 4-aminopyridine. Biophys J 16: 83-86.
40. Luhmann HJ, Dzhala VI, Ben-Ari Y,. (2000) Generation and propagation of 4-AP-induced epileptiform activity in neonatal intact limbic structures in vitro. Eur J Neurosci 12: 2757-2768.
41. Luskin MB, Price JL,. (1983) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216: 292-302.
42. McIntyre DC, Gilby KL,. (2008) Mapping seizure pathways in the temporal lobe. Epilepsia 49 (Suppl. 3): 23-30.
43. Mouly AM, Litaudon P, Chabaud P, Ravel N, Gervais R,. (1998) Spatiotemporal distributiono f a late synchronized activity in olfactory pathways following stimulation of the olfactory bulb in rats. Eur J Neurosci 10: 1128-1135.
44. Muhlethaler M, de Curtis M, Walton K, Llinas R,. (1993) The isolated and perfused brain of the guinea-pig in vitro. Eur J Neurosci 5: 915-926.
45. Neville KR, Haberly L,. (2004) Olfactory cortex. In, Shepherd GM, (Ed.) The synaptic organization of the brain. Oxford University Press, New York, pp. 415-454.
46. Panuccio G, Sanchez G, Levesque M, Salami P, de Curtis M, Avoli M,. (2012) On the ictogenic properties of the piriform cortex in vitro. Epilepsia 53: 459-468.
47. Perreault P, Avoli M,. (1991) Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J Neurophysiol 65: 771-785.
48. Piredda S, Gale K,. (1985) A crucial epileptogenic site in the deep prepiriform cortex. Nature 317: 623-625.
49. Room P, Groenewegen HJ, Lohman AH,. (1984) Inputs from the olfactory bulb and olfactory cortex to the entorhinal cortex in the cat. I. Anatomical observations. Exp Brain Res 56: 488-496.
50. Satou M, Mori K, Tazawa Y, Takagi SF,. (1983) Monosynaptic and disynaptic activation of pyriform cortex neurons by synchronous lateral olfactory tract volleys in the rabbit. Exp Neurol 81: 571-585.
51. Schwerdtfeger WK, Buhl EH, Germroth P,. (1990) Disynaptic olfactory input to the hippocampus mediated by stellate cells in the entorhinal cortex. J Comp Neurol 292: 163-177.
52. Sewards TV, Sewards MA,. (2003) Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions? Brain Res Brain Res Rev 42: 243-251.
53. Storm JF,. (1987) Action potential repolarization and a fast-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385: 733-759.
54. Thesleff S,. (1980) Aminopyridines and synaptic transmission. Neuroscience 5: 1413-1419.
55. Trombin F, Gnatkovsky V, de Curtis M,. (2011) Changes in action potential features during focal seizure discharges in the entorhinal cortex of the in vitro isolated guinea pig brain. J Neurophysiol 106: 1411-1423.
56. Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Anderson WS, Brown EN, Halgren E, Cash SS,. (2011) Single-neuron dynamics in human focal epilepsy. Nat Neurosci 14: 635-641.
57. Uva L, de Curtis M,. (2005) Polysynaptic olfactory pathway to the ipsi- and contralateral entorhinal cortex mediated via the hippocampus. Neuroscience 130: 249-258.
58. Uva L, Librizzi L, Wendling F, de Curtis M,. (2005) Propagation dynamics of epileptiform activity acutely induced by bicuculline in the hippocampal-parahippocampal region of the isolated Guinea pig brain. Epilepsia 46: 1914-1925.
59. van der Linden S, de Curtis M, Panzica F,. (1999) Carbachol induces fast oscillations in the medial but not in the later entorhinal cortex of the isolated guinea pig brain. J Neurophysiol 82: 2441-2450.
60. Van Groen T, Lopes da Silva FH, Wadman WJ,. (1987) Synaptic organization of olfactory inputs and local circuits in the entorhinal cortex, a current-source density analysis in the cat. Exp Brain Res 67: 502-509.
61. van Luijtelaar G, Sitnikova E,. (2006) Global and focal aspects of absence epilepsy: the contribution of genetic models. Neurosci Biobehav Rev 30: 983-1003.
62. Weiser M, Vega-Saenz de Miera E, Kentros C, Moreno H, Franzen L, Hillman D, Baker H, Rudy B,. (1994) Differential expression of Shaw-related K+ channels in the rat central nervous system. J Neurosci 14: 949-972.
63. Wilson RC, Steward O,. (1978) Polysynaptic activation of the dentate gyrus of the hippocampal formation: an olfactory input via the lateral entorhinal cortex. Exp Brain Res 33: 523-534.
64. Ziburkus J, Cressman JR, Barreto E, Schiff SJ,. (2006) Interneuron and pyramidal cell interplay during in vitro seizure-like events. J Neurophysiol 95: 3948-3954.