Imaging the induction and spread of seizure activity in the isolated brain of the guinea pig: The roles of GABA and glutamate receptors

Journal of Neurophysiology

Volumn 76, Issue 5, 1996, Pages 3471-3492

  Federico, Paolo ^a   MacVicar, Brian A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; BICUCULLINE METHIODIDE; DIZOCILPINE; GLUTAMATE RECEPTOR; TRANEXAMIC ACID;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENCEPHALE ISOLE; ENTORHINAL CORTEX; EVOKED RESPONSE; GUINEA PIG; NONHUMAN; OLFACTORY CORTEX; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; SEIZURE;

EID: 0029861175     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.5.3471     Document Type: Article

References (82)

1. ALHEID, G. F., DE OLMOS, J. S., AND BELTRAMINO, C. A. Amygdala and extended amygdala. In: The Rat Nervous System (2nd ed.), edited by G. Paxinos. Toronto: Academic Press, p. 495-578, 1995.
2. AMARAL, D. G. AND WITTER, M. P. Hippocampal formation. In: The Rat Nervous System (2nd ed.), edited by G. Paxinos. Toronto: Academic Press, p. 443-494, 1995.
3. ARVANOV, V. L., HOLMES, K. H., KEELE, N. B., AND SHINNICK-GALLAGHER, P. The functional role of metabotropic glutamate receptors in epileptiform activity induced by 4-aminopyridine in the rat amygdala slice. Brain Res. 669: 140-144, 1995.
4. AVOLI, M. Penicillin induced hyperexcitability in the in vitro hippocampal slice can be unrelated to impairment of somatic inhibition. Brain Res. 323: 154-158, 1984.
5. BASKYS, A. AND MALENKA, R. C. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rut hippocampus. J. Physiol. Lond. 444: 687-701, 1991.
6. BLISS, T. V. AND COLLINGRIDGE, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature Lond. 361: 31-39, 1993.
7. BURKE, J. P. AND HABLITZ, J. J. Modulation of epileptiform activity by metabotropic glutamate receptors in immature rat neocortex. J. Neurophysiol. 73: 205-217, 1995.
8. CAIN, D. P. Long-term potentiation and kindling: how similar are the mechanisms? Trends Neurosci. 12: 6-10, 1989.
9. CHAGNAC-AMITAI, Y. AND CONNORS, B. W. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61: 747-758, 1989.
10. CHARPAK, S., GÄHWILER, B. H., DO, K. Q., AND KNOPFEL, T. Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature Lond. 347: 765-767, 1990.
11. CHAVIS, P., NOONEY, J. M., BOCKAERT, J., FAGNI, L., FELTZ, A., AND BOSSU, J. L. Facilitatory coupling between a glutamate metabotropic receptor and dihydropyridine-sensitive calcium channels in cultured cerebellar granule cells. J. Neurosci. 15: 135-143, 1995.
12. CHAVIS, P., SHINOZAKI, H., BOCKAERT, J., AND FAGNI, L. The metabotropic glutamate receptor types 2/3 inhibit L-type calcium channels via a pertussis toxin-sensitive G-protein in cultured cerebellar granule cells. J. Neurosci. 14: 7067-7076, 1994.
13. 2+ channels involves multiple receptor subtypes in cortical neurons. J. Neurosci. 16: 36-45, 1995.
14. DEACON, T. W., EICHENBAUM, H., ROSENBERG, P., AND ECKMANN, K. W. Afferent connections of the perirhinal cortex in the rat. J. Comp. Neurol. 220: 68-190, 1983.
15. DE CURTIS, M., BIELLA, G., FORTI, M. AND PANZICA, F. Multifocal spontaneous epileptic activity induced by restricted bicuculline ejection in the piriform cortex of the isolated guinea pig brain. J. Neurophysiol 71: 2463-2476, 1994.
16. DE CURTIS, M. AND LLINAS, R. R. Entorhinal cortex long-term potentiation evoked by theta-patterned stimulation of associative fibers in the isolated in vitro guinea pig brain. Brain Res. 600: 327-330, 1993.
17. DE CURTIS, M., PARÉ, D., AND LLINÁS, R. R. The electrophysiology of the olfactory-hippocampal circuit in the isolated and perfused adult mammalian brain in vitro. Hippocampus 1: 341-354, 1991.
18. DESAI, M. A. AND CONN, J. P. Excitatory effects of ACPD receptor activation in the hippocampus are mediated by direct effects on pyramidal cells and blockade of synaptic inhibition. J. Neurophysiol. 66, 40-52, 1991.
19. DINGLEDINE, R., MCBAIN, C. J., AND MCNAMARA, J. O. Excitatory amino acid receptors in epilepsy. Trends Pharmacol. Sci. 11: 334-338, 1990.
20. FEDERICO, P., BORG, S. G., ŠALKAUSKUS, A. G., AND MACVICAR, B. A. Imaging of seizure spread across cortex of the perfused guinea-pig brain. Soc. Neurosci. Abstr. 18: 909, 1992.
21. FEDERICO, P., BORG, S. G., ŠALKAUSKUS, A. G., AND MACVICAR, B. A. Mapping patterns of neuronal activity and seizure propagation by imaging intrinsic optical signals in the isolated whole brain of the guinea-pig. Neuroscience 58: 461-480, 1994.
22. FEDERICO, P. AND MACVICAR, B. A. The roles of glutamate receptor subtypes in the induction and propagation of seizure activity in the hippocampus and olfactory cortex of the guinea-pig isolated whole brain. Soc. Neurosci. Abstr. 19: 420.13, 1993.
23. GIARETTA, D., KOSTOPOULOS, G., GLOOR, P., AND AVOLI, M. Intracortical inhibitory mechanisms are preserved in feline generalized penicillin epilepsy. Neurosci. Lett. 59: 203-208, 1985.
24. GLAUM, S. R. AND MILLER, R. J. Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. J. Neurosci. 13: 1636-1641, 1993.
25. HABERLY, L. B. AND SUTULA, T. P. Neuronal processes that underlie expression of kindled epileptiform events in the piriform cortex in vivo. J. Neurosci. 12: 2211-2224, 1992.
26. HEINEMANN, U. AND JONES, R. S. G. Neurophysiology. In: Comprehensive Epileptology, edited by M. Dam and L. Gram. New York: Raven Press, p. 17-42, 1990.
27. HEINEMANN, U., ZHANG, C. L., AND EDER, C. Entorhinal cortex-hippocampal interactions in normal and epileptic temporal lobe. Hippocampus 3: 89-98, 1993.
28. HOLMES, K. H., BILKEY, D. K., AND LAVERTY, R. The infusion of an NMDA antagonist into perirhinal cortex suppresses amygdala-kindled seizures. Brain Res. 587: 285-290, 1992.
29. HÖNACK, D., WAHNSCHAFFER, U., AND LOSCHER, W. Kindling from stimulation of a highly sensitive locus in the posterior part of the piriform cortex. Comparison with amygdala kindling and effects of antiepileptic drugs. Brain Res. 538: 196-202, 1991.
30. B receptor activation in absence seizures of lethargic (lh/lh) mice. Science Wash. DC 257: 398-401, 1992.
31. HWA, G. G. AND AVOLI, M. The involvement of excitatory amino acids in neocortical epileptogenesis: NMDA and non-NMDA receptors. Exp. Brain Res. 86: 248-256, 1991.
32. INOUÉ, S. Video Microscopy. New York: Plenum Press, 1986.
33. JONES, R. S. G. AND LAMBERT, J. D. C. Involvement of excitatory amino acid receptors in epileptiform activity in the rat entorhinal cortex and dentate gyrus in vitro. Br. J. Pharmacol. 98 (Suppl.): 835P, 1989.
34. JONES, R. S. G. AND LAMBERT, J. D. C. The role of excitatory amino acid receptors in the propagation of epileptiform discharges from the entorhinal cortex to the dentate gyms in vitro. Exp. Br. Res. 80: 310-322, 1990a.
35. JONES, R. S. G. AND LAMBERT, J. D. C. Synchronous discharges in the rat entorhinal cortex in vitro: site of initiation and the role of excitatory amino acid receptors. Neuroscience 34: 657-670, 1990b.
36. B receptor blocker CGP 35348. Neuroscience 47: 63-68, 1992.
37. KELLY, M. E., ARMSTRONG, J. M., AND MCINTYRE, D. C. Kindling in the perirhinal cortex. I. Kindling rate and seizure characteristics. Soc. Neurosci. Abstr. 17: 201.15, 1991.
38. KÖHR, G., DE KONINCK, Y. D, AND MODY, I. Properties of NMDA receptor channels in neurons acutely isolated from epileptic (kindled) rats. J. Neurosci. 13: 3612-3627, 1993.
39. LAMBERT, J. D. C., JONES, R. S. G., ANDREASEN, M., JENSEN, M. S., AND HEINEMANN, U. The role of excitatory amino acids in synaptic transmission in the hippocampus. Comp. Biochem. Physiol. A Comp. Physiol. 93: 195-201, 1989.
40. LESTER, R. A. J. AND JAHR, C. E. Quisqualate receptor-mediated depression of calcium currents in hippocampal neurons. Neuron 4: 741-749, 1990.
41. LOTHMAN, E. W., BERTRAM, E. H., STRINGER, J. L. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37: 1-82, 1991.
42. LOVINGER, D. M., TYLER, E., FIDLER, S., AND MERRITT, A. Properties of a presynaptic metabotropic glutamate receptor in rat neostriatal slices. J. Neurophysiol. 69: 1236-1244, 1993.
43. MACVICAR, B. A. AND MÜHLETHALER, M. M. Synchronization of seizure activity in the hippocampus and entorhinal cortex of the perfused whole guinea-pig brain. Soc. Netirosci. Abstr. 16: 309, 1990.
44. MATSUMOTO, H. AND AJMONE MARSAN, C. Cortical cellular phenomena in experimental epilepsy: ictal manifestations. Exp. Neurol. 9: 305-326, 1964.
45. MCDONALD, J. W., FIX, A. S., TIZZANO, J. P., AND SCHOEPP, D. D. Seizures and brain injury in neonatal rats induced by 1S,3,R-ACPD, a metabotropic glutamate receptor agonist. J. Neurosci. 13: 4445-4455, 1993.
46. MCINTYRE, D. C. AND KELLY, M. E. Pyriform cortex involvement in limbic kindling. Soc. Neurosci. Abstr. 16: 452.13, 1990.
47. MCINTYRE, D. C., KELLY, M. E., AND ARMSTRONG, J. N. Kindling in the perirhinal cortex. Brain Res. 615: 1-6, 1993.
48. MCINTYRE, D. C. AND PLANT, J. R. Pyriform cortex involvement in kindling. Neurosci. Biobehav. Rev. 13: 277-280, 1989.
49. MCINTYRE, D. C. AND RACINE, R. J. Kindling mechanisms: current progress of an experimental epilepsy model. Prog. Neurobiol. 27: 1-12, 1986.
50. MCINTYRE, D. C. AND WONG, R. K. S. Cellular and synaptic properties of amygdala-kindled pyriform cortex in vitro. J. Neurophysiol. 55: 1295-1307, 1986.
51. MERLIN, L. R., TAYLOR, G. W., AND WONG, R. K. S. Role of metabotropic glutamate receptor subtypes in the patterning of epileptiform activities in vitro. J. Neurophysiol. 74: 896-900, 1995.
52. MILES, R., TRAUB, R. D., AND WONG, R. K. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J. Neurophysiol. 60: 1481-1496, 1988.
53. MILLER, L. D. P., PETROZZINO, J. J., AND CONNOR, J. A. Metabotropic glutamate receptor responses in pyramidal neurons induced by synaptic activation of different pathways in hippocampal slice cultures. Soc. Neurosci. Abstr. 19: 117.3, 1993.
54. MONAGHAN, D. T., BRIDGES, R. J., AND COTMAN, C. W. The excitatory amino acid receptors: their classes, pharmacology and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29: 365-402, 1989.
55. MÜHLETHALER, M. M., CAND, P., HENAUER, R., AND SERAFIN, M. Design of a microprocessor-controlled thermoregulated chamber for perfusing in vitro mammalian brain preparations. J. Neurosci. Methods 31: 215-223, 1990.
56. MÜHLETHALER, M. M., DE CURTIS, M., WALTON K., AND LLINÁS, R. R. The isolated and perfused brain of the guinea-pig in vitro. Eur. J. Neurosci. 5: 915-926, 1993.
57. NAKANISHI, S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13: 1031-1037, 1994.
58. NAMBA, T., MORIMOTO, K., SATO, K., YAMADA, N., AND KURODA, S. Antiepileptogenic and anticonvulsant effects of NBQX, a selective AMPA receptor antagonist, in the rat kindling model of epilepsy. Brain Res. 638: 36-44, 1994.
59. PARÉ, D., DE CURTIS, M., AND LLINÁS, R. R. Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro. J. Neurosci. 12: 1867-1881, 1992.
60. PRICE, J. L., RUSSCHEN, F. T., AND AMARAL, D. G. The limbic region. II. The amygdaloid complex. In: Handbook of Chemical Neuroanatomy, edited by A. Bjorklund, T. Hokfelt, and L. W. Swanson. New York: Elsevier, vol. 5, p. 279-388, 1987.
61. RAINNIE, D. G. AND SHINNICK-GALLAGHER, P. Trans-ACPD and L-APB presynaptically inhibit excitatory glutamatergic transmission in the basolateral amygdala. Neurosci. Lett. 139: 87-91, 1992.
62. SACAAN, A. I. AND SCHOEPP, D. D. Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139: 77-82, 1992.
63. SAHARA, Y. AND WESTBRROK, G. L. Modulation of calcium currents by a metabotropic glutamate receptor involves fast and slow kinetic components in cultured hippocampal neurons. J. Neurosci. 13: 3041-3050, 1993.
64. SHEARDOWN, M. J. Metabotropic glutamate receptor agonists reduce epileptiform activity in the rat cortex. Neuroreport 3: 916-918, 1992.
65. B-mediated mechanisms in experimental generalized absence seizures. Eur. J. Pharmacol. 213: 343-349, 1992.
66. SORENSON, K. E. AND CHRISTENSEN, H. B. T. The topographical and laminar organization of a commisural-associational entorhino-entorhinal projection in the guinea pig. Brain Res. 505: 75-82, 1989.
67. STASHEFF, S. F., ANDERSON, W. W., CLARK, S., AND WILSON, W. A. NMDA antagonists differentiate epileptogenesis from seizure expression in an in vitro model. Science Wash. DC 245: 684-651, 1989.
68. STRINGER, J. L. AND LOTHMAN, E. W. Reverberatory seizure discharges in hippocampal-parahippocampal circuits. Exp. Neurol. 116: 198-203, 1992.
69. STROWBRIDGE, B. W., MASUKAWA, L. M., SPENCER, D. D., AND SHEPHERD, G. M. Hyperexcitability associated with localizable lesions in epileptic patients. Brain Res. 587: 158-163, 1992.
70. SUZUKI, K., MORI, N., KITTAKA, H., IWATA, Y., YAMADA, Y., OSONOE, K., AND NIWA, S. Anticonvulsant action of metabotropic glutamate receptor agonists in kindled amygdala of rats. Neurosci. Lett. 204: 41-44, 1996.
71. SWANSON, L. W., KÖHLER, C., AND BJÖRKLUND, A. The limbic region. I. The septohippocampal system. In: Handbook of Chemical Neuroanatomy. Integrated Systems of the CNS. Hypothalamus, Hippocampus, Amygdala, Retina, edited by A. Björklund, T. Hokfelt, and L. W. Swanson. Amsterdam: Elsevier, vol. 5, part I, chapt. II, p. 125-277, 1987.
72. SWARTZWELDER, H. S., BRAGDON, A. C., SUTCH, C. P., AULT, B., AND WILSON, W. A. Baclofen suppresses hippocampal epileptiform activity at low concentrations without suppressing synaptic transmission. J. Pharmacol. Exp. Therap. 237: 881-887, 1986.
73. TANCREDI, V., AVOLI, M., AND HWA, G. G. C. Low magnesium epilepsy in rat hippocampal slices: inhibitory postsynaptic potentials in the CA1 subfield. Neurosci. Lett. 89: 293-298, 1988.
74. TASCHENBERGER, H., ROY, B. L., AND LOWE, D. A. Effects of a metabotropic glutamate agonist, trans-ACPD, on cortical epileptiform activity. Neuroreport 3: 629-632, 1992.
75. TESKEY, G. C., VALENTINE, P. A., SAINSBURY, R. S., AND TREPEL, C. Evolution of afterdischarge and seizure characteristics during electrical kindling of the guinea-pig. Brain Res. 672: 137-147, 1995.
76. TROMBLEY, P. Q. AND WESTBROOK, G. L. L-AP4 inhibits calcium currents and synaptic transmission via a G-protein-coupled glutamate receptor. J. Neurosci. 12: 2043-2050, 1992.
77. VAN GROEN, T. AND WYSS, J. M. The connections of presubiculum and parasubiculum in the rat. Brain Res. 518: 227-243, 1990.
78. WADA, J. A. Transhemispheric horizontal channels for transmission of epileptic information. Jpn. J. Psychiat. 45: 235-241, 1991.
79. WITTER, M. P., GROENEWEGEN, H. J., LOPES DA SILVA, F. H., AND LOHMAN, A. H. M. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33: 161-253, 1989.
80. WONG, B. Y. AND PRINCE, D. A. The lateral spread of ictal discharges in neocortical brain slices. Epilepsy Res. 1: 29-39, 1990.
81. ZHANG, C. L., GLOVELI, T., AND HEINEMANN, U. Effects of NMDA- and AMPA-receptor antagonists on different forms of epileptiform activity in rat temporal cortex slices. Epilepsia 35: S68-S73, 1994.
82. ZHENG, F. AND GALLAGHER, J. P. Pharmacologically distinct, pertussis toxin-resistant inward currents evoked by metabotropic glutamate receptor (mGluR) agonists in dorsolateral septal nucleus (DLSN) neurons. J. Neurosci. 15: 504-510, 1995.