Alterations of perisomatic GABA synapses on hippocampal CA1 inhibitory interneurons and pyramidal cells in the kainate model of epilepsy

Neuroscience

Volumn 93, Issue 2, 1999, Pages 457-467

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

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Electron microscopy; Epilepsy; GABA; Hippocampus; Immunocytochemistry; Interneurons

Indexed keywords

KAINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EPILEPSY; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HISTOGRAM; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD STAINING; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; ELECTROPHYSIOLOGY; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; KAINIC ACID; MALE; MICROSCOPY, ELECTRON; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 0032776815     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00199-2     Document Type: Article

References (56)

1. Acsady L., Arabadzisz D., Freund T.F. Correlated morphological and neurochemical features identify different subsets of vasoactive intestinal polypeptide-immunoreactive interneurons in rat hippocampus. Neuroscience. 73:1996;299-315.
2. Acsady L., Arabadzisz D., Freund T.F. Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience. 73:1996;317-334.
3. Babb T.L., Pretorius J.K., Kupfer W.R., Brown W.J. Distribution of glutamate-decarboxylase-immunoreactive neurons and synapses in the rat and monkey hippocampus: light and electron microscopy. J. comp. Neurol. 278:1988;121-138.
4. Babb T.L., Pretorius J.K., Kupfer W.R., Crandall R.H. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci. 9:1989;2563-2574.
5. Beaulieu C., Campistron G., Crevier C. Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat. J. comp. Neurol. 339:1994;559-572.
6. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience. 14:1985;375-403.
7. Best N., Mitchell J., Baimbridge K.G., Wheal H.V. Changes in parvalbumin-immunoreactive neurons in the rat hippocampus following a kainic acid lesion. Neurosci. Lett. 155:1993;1-6.
8. Best N., Mitchell J., Wheal H.V. Ultrastructure of parvalbumin-immunoreactive neurons in the CA1 area of the rat hippocampus following a kainic acid injection. Acta neuropath. 87:1994;187-195.
9. Blasco-Ibanez J.M., 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. 7:1995;2170-2180.
10. Buhl E.H., Cobb S.R., Halasy K., Somogyi P. Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur. J. Neurosci. 7:1995;1989-2004.
11. Bundman M.C., Pico R.M., Gall C.M. Ultrastructural plasticity of the dentate gyrus granule cells following recurrent limbic seizures: I. Increase in somatic spines. Hippocampus. 4:1994;601-610.
12. Bundman M.C., Gall C.M. Ultrastructural plasticity of the dentate gyrus granule cells following recurrent limbic seizures: II. Alterations in somatic synapses. Hippocampus. 4:1994;611-622.
13. Cobb S.R., Halasy K., Vida I., Nyiri G., Tamas G., Buhl E.H., Somogyi P. Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience. 79:1997;629-648.
14. Davenport C.J., Brown W.J., Babb T.L. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Expl Neurol. 109:1990;180-190.
15. Davies S.N., Collingridge G.L. Role of excitatory amino acid receptors in synaptic transmission in area CA1 of rat hippocampus. Proc. R. Soc. Lond. B. 236:1989;373-384.
16. Esclapez M., Hirsch J.C., Khazipov R., Ben-Ari Y., Bernard C. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc. natn. Acad. Sci. U.S.A. 94:1997;12,151-12,156.
17. Farias P.A., Low S.Q., Peterson G.M., Ribak C.E. Morphological evidence for altered synaptic organization and structure in the hippocampal formation of seizure-sensitive gerbils. Hippocampus. 2:1992;229-245.
18. Franck J.E., Kunkel D.D., Baskin D.G., Schwartzkroin P.A. Inhibition in kainate-lesioned hyperexcitable hippocampi: physiologic, autoradiographic and immunocytochemical observations. J. Neurosci. 8:1988;1991-2002.
19. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature. 336:1988;170-173.
20. Freund T.F. GABAergic septal and serotonergic median raphe afferents preferentially innervate inhibitory interneurons in the hippocampus and dentate gyrus. Epilepsy Res., Suppl. 7:1992;79-91.
21. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470.
22. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15:1995;193-204.
23. Gulyas A.I., Toth K., Danos P., Freund T.F. Subpopulations of GABAergic neurons containing parvalbumin, calbindin D-28k, and cholecystokinin in the rat hippocampus. J. comp. Neurol. 312:1991;371-378.
24. Gulyas A.I., Toth K., McBain C.J., Freund T.F. Stratum radiatum giant cells: a type of principal cell in rat hippocampus. Eur. J. Neurosci. 10:1998;3813-3822.
25. Houser C.R., Harris A.B., Vaughn J.E. Time course of the reduction of GABA terminals in a model of focal epilepsy: a glutamic acid decarboxylase immunocytochemical study. Brain Res. 383:1986;129-145.
26. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419:1987;119-130.
27. Kunkel D.D., Lacaille J.-C., Schwartzkroin P.A. Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse. 2:1988;382-394.
28. Lacaille J.-C., Mueller A.L., Kunkel D.D., Schwartzkroin P.A. Local circuit interactions between oriens-alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 7:1987;1979-1993.
29. Lacaille J.-C., Schwartzkroin P.A. Stratum lacunosum-moleculare interneurons of hippocampal CA1 region: I. Intracellular response characteristics, synaptic responses, and morphology. J. Neurosci. 8:1988;1400-1410.
30. Lacaille J.-C., Schwartzkroin P.A. Stratum lacunosum-moleculare interneurons of hippocampal CA1 region: II. Intrasomatic and intradendritic recording of local circuit synaptic interactions. J. Neurosci. 8:1988;1411-1424.
31. Lacaille J.-C., Williams S. Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience. 36:1990;349-359.
32. Lorente de No R. Studies on the structure of the cerebral cortex: II. Continuation of the study of the ammonic system. J. Psychol. Neurol., Lpz. 46:1934;113-177.
33. Marco P., Sola R.G., Ramon y Cajal S., DeFelipe J. Loss of inhibitory synapses on the soma and axon initial segment of pyramidal cells in human epileptic peritumoural neocortex: implications for epilepsy. Brain Res. Bull. 44:1997;47-66.
34. Micheva K.D., Beaulieu C. An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex. Proc. natn. Acad. Sci. U.S.A. 92:1995;11,834-11,838.
35. Micheva K.D., Beaulieu C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J. comp. Neurol. 373:1996;340-354.
36. Miles R., Toth K., Gulyas A.I., Hajos N., Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron. 16:1996;815-823.
37. Morin F., Beaulieu C., Lacaille J.-C. Selective loss of GABA neurons in area CA1 of the rat hippocampus after intraventricular kainate. Epilepsy Res. 32:1998;363-369.
38. Morin F., Beaulieu C., Lacaille J.C. Cell-specific alterations in synaptic properties of hippocampal CA1 interneurons after kainate treatment. J. Neurophysiol. 80:1998;2836-2847.
39. Nadler J.V., Perry B.W., Gentry C., Cotman C.W. Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res. 191:1980;387-403.
40. Nadler J.V. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci. 29:1981;2031-2042.
41. Perez Y., Morin F., Beaulieu C., Lacaille J.-C. Axonal sprouting of CA1 pyramidal cells in hyperexcitable hippocampal slices of kainate-treated rats. Eur. J. Neurosci. 8:1996;736-748.
42. Peterson G.M., Ribak C.E., Oertel W.H. A regional increase in the number of hippocampal GABAergic neurons and terminals in the seizure-sensitive gerbil. Brain Res. 340:1985;384-389.
43. Ramon y Cajal S. (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. Maloine, Paris.
44. Ribak C.E., Harris A.B., Vaughn J.E., Roberts E. Inhibitory, GABAergic nerve terminals decrease at sites of focal epilepsy. Science. 205:1979;211-214.
45. Ribak C.E., Bradburne R.M., Harris A.B. A preferential loss of GABAergic, symmetric synapses in epileptic foci: a quantitative ultrastrutural analysis of monkey neocortex. J. Neurosci. 2:1982;1725-1735.
46. Sah P., Hestrin S., Nicoll R.A. Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurons. J. Physiol., Lond. 430:1990;605-616.
47. Schwartzkroin P.A., Mathers L.H. Physiological and morphological identification of a nonpyramidal hippocampal cell type. Brain Res. 157:1978;1-10.
48. Schwartzkroin P.A., Kunkel D.D. Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J. comp. Neurol. 232:1985;205-218.
49. Scotti A.L., Kalt G., Bollag O., Nitsch C. Parvalbumin disappears from GABAergic CA1 neurons of the gerbil hippocampus with seizure onset while its presence persists in the perforant path. Brain Res. 760:1997;109-117.
50. Seress L., Ribak C.E. Ultrastructural features of primate granule cell bodies show important differences from those of rats - axosomatic synapses, somatic spines and infolded nuclei. Brain Res. 569:1992;353-357.
51. Sik A., Penttonen M., Ylinen A., Buzsaki G. Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J. Neurosci. 15:1995;6651-6665.
52. Sloviter R.S., Dichter M.A., Rachinsky T.L., Dean E., Goodman J.H., Sollas A.L., Martin D.L. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J. comp. Neurol. 373:1996;593-618.
53. Somogyi P., Hodgson A.J. Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J. Histochem. Cytochem. 33:1985;249-257.
54. Turner D.A., Wheal H.V. Excitatory synaptic potentials in kainic acid-denervated rat CA1 pyramidal neurons. J. Neurosci. 11:1991;2786-2794.
55. Umbriaco D., Garcia S., Beaulieu C., Descarries L. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus. 5:1995;605-620.
56. Williams S., Vachon P., Lacaille J.-C. Monosynaptic GABA-mediated inhibitory postsynaptic potentials in CA1 pyramidal cells of hyperexcitable hippocampal slices from kainic acid-treated rats. Neuroscience. 52:1993;541-554.