Cell-specific alterations in synaptic properties of hippocampal CA1 interneurons after kainate treatment

Journal of Neurophysiology

Volumn 80, Issue 6, 1998, Pages 2836-2847

  Morin, F ^a   Beaulieu, C ^a   Lacaille, J C ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; KAINIC ACID;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE CONDUCTANCE; CELL SPECIFICITY; CONTROLLED STUDY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MALE; MONOSYNAPTIC PATHWAY; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY;

EID: 0032444946     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.80.6.2836     Document Type: Article

References (62)

1. ASHWOOD, T. J., LANCASTER, B., AND WHEAL, H. V. Intracellular electrophysiology of CA1 pyramidal neurons in slices of kainic acid-lesioned hippocampus of the rat. Exp. Brain Res. 62: 189-198, 1986.
2. BEKENSTEIN, J. W. AND LOTHMAN, E. W. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 259: 97-100, 1993.
3. BEN-ARI Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14: 375-403, 1985.
4. BEST, N., MITCHELL, J., BAIMBRIDGE, K. G., AND WHEAL, H. V. Changes in parvalbumin-immunoreactive neurons in the rat hippocampus following a kainic acid lesion. Neurosci. Lett. 155: 1-6, 1993.
5. BEST, N., MITCHELL, J., AND WHEAL, H. V. Ultrastructure of parvalbumin-immunoreactive neurons in the CA1 area of the rat hippocampus following a kainic acid injection. Acta Neuropathol. 87: 187-195, 1994.
6. BLASCO-IBANEZ, J. M. AND FREUND, T. F. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur. J. Neurosci. 7: 2170-2180, 1995.
7. BUHL, E. H., HAN, Z.-S., LORINCZI, Z., STEZHKA, V. V., KARNUP, S. V., AND SOMOGYI, P. Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J. Neurophysiol. 71: 1289-1307, 1994.
8. BUHL, E. H., OTIS, T. S., AND MODY, I. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271: 369-373, 1996.
9. DAVENPORT, C. J., BROWN, W. J., AND BABB, T. L. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp. Neurol. 109: 180-190, 1990.
10. EDWARDS, F. A., KONNERTH, A., SAKMANN, B., AND TAKAHASHI, T. A thin slice preparation for patch clamp recordings from neurones of the mammalian nervous system. Pflügers Arch. 414: 600-612, 1989.
11. ESCLAPEZ, M., HIRSCH, J. C., KHAZIPOV, R., BEN-ARI, Y., AND BERNARD, C. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc. Natl. Acacl. Sci. USA 94: 12151-12156, 1997.
12. FRANCK, J. E., KUNKEL, D. D., BASKIN, D. G., AND SCHWARTZKROIN, P. A. Inhibition in kainate-lesioned hyperexcitable hippocampi: physiologic, autoradiographic and immunocytochemical observations. J. Neurosci. 8: 1991-2002, 1988.
13. FRANCK, J. E. AND SCHWARTZKROIN, P. A. Do kainate-lesioned hippocampi become epileptogenic? Brain Res. 389: 309-313, 1985.
14. FREUND, T. F. AND BUZSÁKI, G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996.
15. GIBBS, J. W., SHUMATE, M. D., AND COULTER, D. A. Differential epilepsy-associated alterations in postsynaptic GABAA receptor function in dentate granule cells and CA1 neurons. J. Neurophysiol. 77: 1924-1938, 1997.
16. HAMILL, O. P., MARTY, A., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch clamp techniques for high resolution current recording from cells and cell free membrane patches. Pflügers Arch. 391: 85-100, 1981.
17. HOUSER, C. R. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem. Res. 16: 295-308, 1991.
18. HOUSER, C. R. AND ESCLAPEZ, M. Vulnerability and plasticity of the GABA system in the pilocarpine model of spontaneous recurrent seizures. Epilepsy Res. 26: 207-218, 1996.
19. ISOKAWA, M. Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J. Neurophysiol. 75: 1901-1908, 1996.
20. KAWAGUCHI, Y. AND HAMA, K. Physiological heterogeneity of nonpyramidal cells in rat hippocampal CA1 region. Exp. Brain Res. 72: 494-502, 1988.
21. KAPUR, J. AND COULTER, D. A. Experimental status epilepticus alters γ-aminobutyric acid type A receptor function in CA1 pyramidal neurons. Ann. Neurol. 38: 893-900, 1995.
22. A receptors. J. Neurosci. 17: 7532-7540, 1997.
23. KUNKEL, D. D., LACAILLE, J.-C., AND SCHWARTZKROIN, P. A. Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse 2: 382-394, 1988.
24. LACAILLE, J.-C., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Electrophysiological and morphological characterization of hippocampal interneurons. In: The Hippocampus-New Vistas, edited by V. Chan-Palay and C. Kohler. New York: Liss, 1989, p. 287-305.
25. LACAILLE, J.-C., MUELLER, A. L., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Local circuit interactions between oriens-alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 7: 1979-1993, 1987.
26. LACAILLE, J.-C. AND SCHWARTZKROIN, P. A. Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J. Neurosci. 8: 1400-1410, 1988a.
27. LACAILLE, J.-C. AND SCHWARTZKROIN, P. A. Stratum lacunosum-moleculare interneurons of hippocampal CA1 region: II. Intrasomatic and intradendritic recording of local circuit synaptic interactions. J. Neurosci. 8: 1411-1424, 1988b.
28. LACAILLE, J.-C. AND WILLIAMS, S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36: 349-359, 1990.
29. LLEWELLYN-SMITH, I. J., PILOWSKY, P., AND MINSON, J. B. The tungstate-stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons, J. Neurosci. Methods 46: 27-40, 1993.
30. LOTHMAN, E. W., BERTRAM, E. H., III, AND STRINGER, J. L. Functional anatomy of hippocampal seizures. Prog. Neurobiol. 37: 1-82, 1991.
31. LOTHMAN, E. W., REMPE, D. A., AND MANGAN, P. S. Changes in excitatory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 74: 841-848, 1995.
32. MACCAFERRI, G. AND MCBAIN, C. J. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15: 137-145, 1995.
33. MACCAFERRI, G. AND MCBAIN, C. J. Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J. Neurosci. 16: 5334-5343, 1996.
34. B receptor-mediated processes in region CA1 in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 76: 1282-1296, 1996.
35. MANGAN, P. S., REMPE, D. A., AND LOTHMAN, E. W. Changes in inhibitory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 74: 829-840, 1995.
36. MCBAIN, C. J., DICHIARA, T. J., AND KAUER, J. A. Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J. Neurosci. 14: 4433-4445, 1994.
37. MEIER, C. L. AND DUDEK, F. E. Spontaneous and stimulation-induced synchronized burst afterdischarges in the isolated CA1 of kainate-treated rats. J. Neurophysiol. 76: 2231-2239, 1996.
38. MODY, I., STANTON, P. K., AND HEINEMANN, U. Activation of N-methyl-D-aspartate receptors parallels changes in cellular and synaptic properties of dentate gyrus granule cells after kindling. J. Neurophysiol. 50: 1033-1054, 1988.
39. MORIN, F., BEAULIEU, C., AND LACAILLE, J.-C. Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J. Neurophysiol. 76: 1-16, 1996.
40. MORIN, F., BEAULIEU, C., AND LACAILLE, J.-C. Selective loss of GABA neurons in area CA1 of the rat hippocampus after intraventricular kainate. Epilepsy Res. 32: 363-369, 1998.
41. NADLER, J. V., PERRY, B. W., AND COTMAN, C. W. Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res. 182: 1-9, 1980a.
42. NADLER, J. V., PERRY, B. W., GENTRY, C., AND COTMAN, C. W. Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res. 191: 387-403, 1980b.
43. NADLER, J. V. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 29: 2031-2012, 1981.
44. NAKAJIMA, S., FRANCK, J. E., BILKEY, D., AND SCHWARTZKROIN, P. A. Local circuit synaptic interactions between CA1 pyramidal cells and interneurons in the kainate-lesioned hyperexcitable hippocampus. Hippocampus 1: 67-78, 1991.
45. NATHAN, T., JENSEN, M. S., AND LAMBERT, J.D.C. The slow inhibitory postsynaptic potential in rat hippocampal CA1 neurones in blocked by intracellular injection of QX314. Neurosci. Lett. 110: 309-313, 1990.
46. OLIVIER, M. W. AND MILLER, J. J. Inhibitory processes of hippocampal CA1 pyramidal neurons following kindling-induced epilepsy in the rat. Can. J. Physiol. Pharmacol. 63: 872-878, 1985.
47. PEREZ, Y. AND LACAILLE, J.-C. Spontaneous excitatory postsynaptic currents in hippocampal CA1 interneurons in the kainate model of epilepsy. Soc. Neurosci. Abstr. 23: 2153, 1997.
48. PEREZ, Y., MORIN, F., BEAULIEU, C., AND LACAILLE, J.-C. Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur. J. Neurosci. 8: 736-748, 1996.
49. PETERSON, G. M., RIBAK, C. E., AND OERTEL, W. H. A regional increase in the number of hippocampal GABAergic neurons and terminals in the seizure-sensitive gerbil. Brain Res. 340: 384-389, 1985.
50. PYAPALI, G. K. AND TURNER, D. A. Denervation-induced dendritic alterations in CA1 pyramidal cells following kainic acid hippocampal lesions in rats. Brain Res. 652: 279-290, 1994.
51. REMPE, D. A., MANGAN, P. S., AND LOTHMAN, E. W. Regional heterogeneity of pathophysiological alterations in CA1 and dentate gyrus in a chronic model of temporal lobe epilepsy. J. Neurophysiol. 74: 816-828, 1995.
52. REMPE, D. A., BERTRAM, E. H., WILLIAMSON, J. M., AND LOTHMAN, E. W. Interneurons in area CA1 stratum radiatum and stratum oriens remain functionally connected to excitatory synaptic input in chronically epileptic animals. J. Neurophysiol. 78: 1504-1515, 1997.
53. RICE, A., RAFIQ, A., SHAPIRO, S. M., JAKOI, E. R., COULTER, D. A., AND DELORENZO, R. J. Long-lasting reduction of inhibitory function and γ-aminobutyric acid type A receptor subunit mRNA expression in a model of temporal lobe epilepsy. Proc. Natl. Acad. Sci. USA 93: 9665-9669, 1996.
54. SAH, P., HESTRIN, S., AND NICOLL, R. A. Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurons. J. Physiol. (Lond.) 430: 605-616, 1990.
55. SIK, A., PENTTONEN, M., YLINEN, A., AND BUZSÁKI, G. Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci. 15: 6651-6665, 1995.
56. SLOVITER, R. S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235: 73-76, 1987.
57. SLOVITER, R. S. Permanently altered structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1: 41-66, 1991.
58. SLOVITER, R. S. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol. 35: 640-654, 1994.
59. TURNER, D. A. AND WHEAL, H. V. Excitatory synaptic potentials in kainic acid-denervated rat CA1 pyramidal neurons. J. Neurosci. 11: 2786-2794, 1991.
60. 2 mRNA levels are decreased following induction of spontaneous epileptiform discharges in hippocampal-entorhinal cortical slices. Brain Res. 721: 111-119, 1996.
61. WILLIAMS, S., SAMULACK, D. D., BEAULIEU, C., AND LACAILLE, J.-C. Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J. Neurophysiol. 71: 2217-2235, 1994.
62. WILLIAMS, S., VACHON, P., AND LACAILLE, J.-C. Monosynaptic GABA-mediated inhibitory postsynaptic potentials in CA1 pyramidal cells of hyperexcitable hippocampal slices from kainic acid-treated rats. Neuroscience 52: 541-554, 1993.