Mechanisms and functional significance of a slow inhibitory potential in neurons of the lateral amygdala

European Journal of Neuroscience

Volumn 10, Issue 3, 1998, Pages 853-867

  Danober, Laurence ^a   Pape, Hans Christian ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Burst discharges; Ca2+ activated K+ conductance; Gamma aminobutyric acid; N methyl D aspartate; Temporal lobe epilepsy

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; CALCIUM ION; CHLORIDE CHANNEL; CHLORIDE ION; DOPAMINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLUTAMATE RECEPTOR; LIDOCAINE ETHOBROMIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM ION;

AFTERDISCHARGE; AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE POTENTIAL; CHLORIDE TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; EPILEPTIC DISCHARGE; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NONHUMAN; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE;

AMYGDALA; ANIMALS; CALCIUM; CHLORIDE CHANNELS; EPILEPSY; EXCITATORY AMINO ACIDS; FEMALE; GUINEA PIGS; MALE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 0031903209     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1998.00092.x     Document Type: Article

References (66)

1. Aggleton, J.P. (1992) The functional effects of amygdala lesions in humans: a comparison with findings from monkeys. In Aggleton, J.P. (ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 485-504.
2. Alger, B.E. & Nicoll, R.A. (1980) Epileptiform burst afterhyperpolarization: Calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. Science, 210, 1122-1124.
3. Alger, B.E. & Williamson, A. (1988) A transient calcium-dependent potassium component of the epileptiform burst after-hyperpolarization in rat hippocampus. J. Physiol. Lond., 399, 191-205.
4. A-mediated inhibition and in vitro epileptogenesis in the human neocortex. J. Neurophysiol., 73, 468-484.
5. Ben-Ari, Y., Le Gal La Salle, G. & Champagnat, J.C. (1974) Lateral amygdala unit activity: I. Relationship between spontaneous and evoked activity. Electroenceph. Clin. Neurophysiol., 37, 449-461.
6. Callahan, P.M., Paris, J.M., Cunningham, K.A. & Shinnick-Gallagher, P. (1991) Decrease of GABA-immunoreactive neurones in the amygdala after electrical kindling in rat. Brain Res., 555, 335-339.
7. Danober, L. & Pape, H.-C. (1998) Strychnine-sensitive glycine responses in neurons of the lateral amygdala: an electrophysiological and immunocytochemical characterization. Neuroscience, in press.
8. Danober, L. & Pape, H.-C. (1996) Contribution of a slow membrane hyperpolarization to the prevention of epileptic activity in the lateral amygdala. Soc. Neurosci. Abstr., 22, 2098.
9. Dichter, M.A. & Ayala, G.F. (1987) Cellular mechanisms of epilepsy: a status report. Science, 237, 157-164.
10. Dichter, M. & Spencer, W.A. (1969) Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction. J. Neurophysiol., 32, 663-687.
11. Dingledine, R., Hynes, M.A. & King, G.L. (1986) Involvement of N-methyl-D-aspartate receptor in epileptiform bursting in the rat hippocampal slice. J. Physiol. Lond., 380, 175-189.
12. Dixon, W.J. & Massey, F.J. (1969) Introduction to Statistical Analysis, 3rd edn, McGraw Hill, New York.
13. Domann, R., Dorn, T. & Witte, O.W. (1989) Calcium-dependent potassium current following penicillin-induced epileptiform discharges in the hippocampal slice. Exp. Brain Res., 78, 646-648.
14. Farb, C.R., Aoki, C. & Ledoux, J.E. (1995) Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: a light and electron microscopic study. J. Comp. Neurol., 362, 86-108.
15. A-receptor heterogeneity in adult rat brain: differential regional and cellular distribution of seven major subunits. J. Comp. Neurol., 359, 154-194.
16. 2+ currents through somatic and dendritic glutamate receptor channels of rat hippocampal CA1 pyramidal neurones. J. Physiol. Lond., 491, 757-172.
17. Gaudreau, H. & Paré, D. (1996) Projection neurons of the lateral amygdaloid nucleus are virtually silent throughout the sleep-waking cycle. J. Neurophysiol., 75, 1301-1305.
18. Gean, P.W. (1990) The epileptiform activity induced by 4-aminopyridine in rat amygdala slices: antagonism by non-N-methyl-D-aspartate receptor antagonists. Brain Res., 530, 251-256.
19. Gean, P.W. & Chang, F.C. (1991) Bursting discharges in disinhibited amygdala slices: the role of excitatory amino acid receptors. Neuropharmacol., 30, 797-802.
20. Gean, P.W. & Chang, F.C. (1992) Pharmacological characterization of excitatory synaptic potentials in rat basolateral amygdaloid neurons. Synapse, 11, 1-9.
21. Gean, P.W. & Shinnick-Gallagher, P. (1987) Picrotoxin induced epileptiform activity in amygdaloid neurons. Neurosci. Lett., 73, 149-154.
22. Gloor, P. (1992) Role of the amygdala in temporal lobe epilepsy. In Aggleton, J.P. (ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 505-538.
23. Hablitz, J.J. (1981) Effects of intracellular injections of chloride and EGTA on postepileptiform-burst hyperpolarizations in hippocampal neurons. Neurosci. Lett., 22, 159-163.
24. Hablitz, J.J. (1984) Picrotoxin-induced epileptiform activity in hippocampus: role of endogenous vs. synaptic factors. J. Neurophysiol., 51, 1011-1027.
25. Horikawa, K. & Armstrong, W.E. (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Meth., 25, 1-11.
26. Huang, C.C., Hsu, K.S. & Gean, P.W. (1996) Isoproterenol. potentiates transmission primarily by enhancing presynaptic calcium influx via P- and/ or Q-type calcium channels in the rat amygdala. J. Neurosci., 16, 1026-1033.
27. + currents. Neurosci. Lett., 231, 13-16.
28. Lang, E.J. & Paré, D. (1997a) Similar inhibitory processes dominate the responses of cat lateral amygdaloid projection neurons to their various afferents. J. Neurophysiol., 77, 341-352.
29. Lang, E.J. & Paré, D. (1997b) Synaptic and synaptically activated intrinsic conductances underlie inhibitory potentials in cat lateral amygdaloid projection neurons in vivo. J. Neurophysiol., 77, 353-363.
30. Le Gal La Salle, G. (1976) Unitary responses in the amygdaloid complex following stimulation of various diencephalic structures. Brain Res., 118, 475-478.
31. Le Doux, J.E. (1995) Emotion: clues from the brain. Annu. Rev. Psychol., 46, 209-235.
32. Lee, W.L. & Hablitz, J.J. (1991) Initiation of epileptiform activity by excitatory amino acid receptors in the disinhibited rat neocortex. J. Neurophysiol., 65, 87-95.
33. Löscher, W. & Schwark, W.S. (1987) Further evidence for abnormal GABAergic circuits in amygdala-kindled rats. Brain Res., 420, 385-390.
34. Mangan, P.S., Rempe, D.A. & Lothman, E.W. (1995) Changes in inhibitory neurotransmission in the CAl region and dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol., 74, 829-840.
35. McDonald, A.J. (1996) Glutamate and aspartate immunoreactive neurons of the rat basolateral amygdala: colocalization of excitatory amino acids and projections to the limbic circuit. J. Comp. Neurol., 365, 367-379.
36. McIntyre, D.C. & Racine, R.J. (1986) Kindling mechanisms: current progress on an experimental epilepsy model. Prog. Neurobiol., 27, 1-12.
37. + current in acutely isolated pyramidal-like neurons from the rat basolateral amygdaloid complex. J. Neurophysiol., in press. Author, details please?
38. 2+ in rat central neurones. J. Physiol. (Lond.), 494, 479-492.
39. Nose, I., Higashi, H., Inokuchi, H. & Nishi, S. (1991) Synaptic responses of guinea-pig and rat central amygdala neurons in vitro. J. Neurophysiol., 65, 1227-1241.
40. Ottersen, O.P. (1982) Connections of the amygdala of the rat. IV: corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol., 205, 30-48.
41. Pape, H.-C. & Driesang, R.B. (1997) Ionic mechanisms of intrinsic oscillations in neurons of the basolateral amygdaloid complex. J. Neurophysiol., in press.
42. Pape, H.-C., Paré, D. & Driesang, R.B. (1997) Two types of intrinsic oscillations in neurons of the lateral and basolateral nuclei of the amygdala. J. Neurophysiol., in press.
43. Paré, D., Pape, H.-C. & Dong, J. (1995) Bursting and oscillating neurons of the cat basolateral amygdaloid complex in vivo: electrophysiological properties and morphological features. J. Neurophysiol., 74, 1-13.
44. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron., 11, 1023-1035.
45. AHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J. Neurophysiol., 74, 2749-2753.
46. Pitkänen, A., Stefanacci, L., Farb, C.R., Go, G.G., Ledoux, J.E. & Amaral, D.G. (1995) Intrinsic connections of the rat amygdaloid complex: projections originating in the lateral nucleus. J. Comp. Neurol., 356, 288-310.
47. Prince, D.A. (1968) Inhibition in 'epileptic' neurons. Exp. Neurol., 21, 307-321.
48. Rainnie, D.O., Asprodini, E.K. & Shinnick-Gallagher, P. (1991a) Excitatory transmission in the basolateral amygdala. J. Neurophysiol., 66, 986-998.
49. Rainnie, D.G., Asprodini, E.K. & Shinnick-Gallagher, P. (1991b) Inhibitory transmission in the basolateral amygdala. J. Neurophysiol., 66, 999-1009.
50. + currents in neurones: types, physiological roles and modulation. Trends Neurosci., 19, 150-154.
51. B receptors in partially disinhibited rat hippocampal slice cultures. J. Physiol. Lond., 444, 375-396.
52. Schneggenburger, R., Zhou, Z., Konnerth, A. & Neher, E. (1993) Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron., 11, 133-143.
53. Schwartzkroin, P.A. & Stafstrom, C.E. (1980) Effects of EGTA on the calcium-activated afterhyperpolarization in hippocampal CA3 pyramidal cells. Science, 210, 1125-1126.
54. Smith, B.N. & Dubek, F.E. (1996) Amino acid-mediated regulation of spontaneous synaptic activity patterns in the rat basolateral amygdala. J. Neurophysiol., 76, 1958-1967.
55. Smith, Y. & Paré, D. (1994) Intra-amygdaloid projections of the lateral nucleus in the cat: PHA-L anterograde labeling combined with postembedding GABA and glutamate immunocytochemistry. J. Comp. Neurol., 342, 232-248.
56. Starr, S.M. (1996) The role of dopamine in epilepsy. Synapse, 22, 159-194.
57. Sugita, S., Tanaka, E. & North, R.A. (1993) Membrane properties and synaptic potentials of three types of neurone in rat lateral amygdala. J. Physiol. Lond., 460, 705-718.
58. Teskey, G.C., Valentine, P.A., Sainsbury, R.S. & Trepel, C. (1995) Evolution of afterdischarges and seizure characteristics during electrical kindling of the guinea-pig. Brain Res., 672, 137-147.
59. Thompson, S.M., Deisz, R.A. & Prince, D.A. (1988) Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J. Neurophysiol., 60, 105-124.
60. Traub, R.D., Miles, R. & Jefferys, J.G. (1993) Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J. Physiol. Lond., 461, 525-547.
61. Traub, R.D., Wong, R.K., Miles, R. & Michelson, H. (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J. Neurophysiol., 66, 635-650.
62. Turski, W.A., Cavalheiro, E.A., Calderazzo-Filho, L.S., Kleinrok, Z., Czuczwar, S.J. & Turski, L. (1985) Injections of picrotoxin and bicuculline into the amygdaloid complex of the rat: an electroencephalographic, behavioural and morphological analysis. Neuroscience, 14, 37-53.
63. Washburn, M.S. & Moises, H.C. (1992a) Inhibitory responses of rat basolateral amygdaloid neurons recorded in vitro. Neuroscience, 50, 811-830.
64. Washburn, M.S. & Moises, H.C. (1992b) Muscarinic responses of rat basolateral amygdaloid neurons recorded in vitro. J. Physiol. (Lond.), 449, 121-154.
65. Westerhoff, C.H.A., Domann, R. & Witte, O.W. (1995) Inhibitory mechanisms in epileptiform activity by low magnesium. Pflügers Arch., 430, 238-245.
66. Womble, M.D. & Moises, H.C. (1993) Muscarinic modulation of conductances underlying the afterhyperpolarization in neurons of the rat basolateral amygdala. Brain Res., 621, 87-96.