Interneuron-specific Ca2+ responses linked to metabotropic and ionotropic glutamate receptors in rat hippocampal slices

European Journal of Neuroscience

Volumn 9, Issue 8, 1997, Pages 1625-1635

  Carmant, Lionel ^a   Woodhall, Gavin ^a   Ouardouz, Mohamed ^a   Robitaille, Richard ^a   Lacaille, Jean Claude ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Ca2+ oscillations; fluo 3 AM; Hippocampus; Inhibitory cells; Intracellular Ca2+

Indexed keywords

AMINO ACID RECEPTOR BLOCKING AGENT; CALCIUM; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; 2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; CALCIUM ION; GLUTAMIC ACID; IONOTROPIC RECEPTOR;

ANIMAL; ARTICLE; CEREBROSPINAL FLUID; CYTOLOGY; DRUG ANTAGONISM; HIPPOCAMPUS; IN VITRO STUDY; INTERNEURON; MALE; PERFUSION; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; ANIMAL TISSUE; CALCIUM CELL LEVEL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CULTURE MEDIUM; DENDRITE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; SECOND MESSENGER; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CEREBROSPINAL FLUID; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; INTERNEURONS; MALE; PERFUSION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUTAMATE; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0030611364     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.1997.tb01520.x     Document Type: Article

References (60)

1. 2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors. J. Physiol. (Lond.), 469, 693-716.
2. Baude, A., Nusser, Z., Roberts, J. D. B., Mulvihill, E., McIlhinney, R. A. J. and Somogyi, P. (1993) The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron, 11, 771-787.
3. Berridge, M. J. (1991) Cytoplasmic calcium oscillations: a two pool model. Cell Calcium, 12, 63-72.
4. Best, N., Mitchell, J., Baimbridge, K. G. and Wheal, H. V. (1993) Changes in parvalbumin-immunoreactive neurons in the rat hippocampus following a kainic acid lesion. Neurosci. Lett., 155, 1-6.
5. Best, N., Mitchell, J. and Wheal, H. V. (1994) Ultrastructure of parvalbumin-immunoreactive neurons in the CA1 area of the rat hippocampus following a kainic acid injection. Acta Neuropathol., 87, 187-195.
6. Buhl, E. H., Halasy, K. and Somogyi, P. (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature, 368, 823-828.
7. Buzsáki, G. and Chrobak, J. J. (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol., 5, 504-510.
8. Carmant, L., Liu, Z., Werner, S., Mikati, M. and Holmes, G. L. (1995a) Effect of kainic-acid induced status epilepticus on inositol-trisphosphate and seizure-induced brain damage. Dev. Brain Res., 89, 67-72.
9. 2+ responses elicited by glutamate in CA1 interneurons of rat hippocampal slices. Soc. Neurosci. Abstr., 21, 1437.
10. Chavis, P., Fagni, L., Lansman, J. B. and Bockaert, J. (1996) Functional coupling between ryanodine receptors and L-type calcium channels in neurons. Nature, 382, 719-722.
11. Choi, D. W. (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci., 7, 369-379.
12. Cornell-Bell, A. H., Villalba, R. and Selinfreund, R. (1994) Intact unrolled hippocampal preparation: an alternative to acute slice. Soc. Neurosci. Abstr., 20, 212.
13. de Lanerolle, N. C., Kim, J. H., Robbins, R. J. and Spencer, D. D. (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res., 495, 387-395.
14. 2+ release. Cell Calcium, 12, 73-85.
15. Edwards, F. A., Konnerth, A., Sakmann, B. and Takahashi, T. A. (1989) A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflueger's Arch., 414, 600-612.
16. Franck, J. E., Kunkel, D. D., Baskin, D. G. and Schwartzkroin, P. A. (1988) Inhibition in kainate-lesioned hyperexcitable hippocampi: physiologic, autoradiographic, and immunocytochemical observations. J. Neurosci., 8, 1991-2002.
17. Freund, T. F. and Buzsáki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347-470.
18. Gosh, A. and Greenberg, M. E. (1995) Calcium signalling in neurons: molecular mechanisms and cellular consequences. Science, 268, 239-247.
19. Gulyás, A. I., Tóth, K., Dános, P. and Freund, T. F. (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28K, and cholecystokinin in the rat hippocampus. J. Comp. Neurol., 312, 371-378.
20. 2+ in neurons. Neuroscience, 46, 251-273.
21. 2+-permeable AMPA receptors in rat hippocampal slices. J. Physiol. (Lond.), 491, 719-733.
22. Jaffe, D. B. and Brown, T. H. (1994) Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J. Neurophysiol., 72, 471-474.
23. 2+ entry into hippocampal neurons. Nature, 357, 244-246.
24. Jonas, P. and Burnashev, N. (1995) Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron, 15, 987-990.
25. Kawaguchi, Y. and Hama, K. (1987) Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection. Brain Res., 411, 190-195.
26. 2+-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J. Physiol. (Lond.), 485, 383-402.
27. Lacaille, J.-C. (1991) Postsynaptic potentials mediated by excitatory and inhibitory amino acids in interneurons of stratum pyramidale of the CA1 region of rat hippocampal slices in vitro. J. Neurophysiol., 66, 1441-1454.
28. Lacaille, J.-C. and Schwartzkroin, P. A. (1988a) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J. Neurosci., 8, 1400-1410.
29. Lacaille, J.-C. and Schwartzkroin, P. A. (1988b) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J. Neurosci., 9, 1411-1424.
30. Lacaille, J.-C. and Williams, S. (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience, 36, 349-359.
31. Lacaille, J.-C., Kunkel, D. D. and Schwartzkroin, P. A. (1989) Electrophysiological and morphological characterization of hippocampal interneurons. In Chan-Palay, V. and Kohler, C. (eds), The Hippocampus: New Vistas. Allan Liss, New York, pp. 287-305.
32. Lorente de Nó, R. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. Lpz., 46, 113-177.
33. Maccaferri, G. and McBain, C.J. (1995) Passive propagation of LTD to striatum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron, 15, 137-145.
34. Maccaferri, G. and McBain, C. J. (1996) Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J. Neurosci., 16, 5334-5343.
35. 2+ entry through the N-methyl-D-aspartate channel. Proc. Natl Acad. Sci. USA, 91, 8170-8174.
36. Markram, H., Helm, P. J. and Sakmann, B. (1995) Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J. Physiol. (Lond.), 485, 1-20.
37. Masu, M., Tanabe, Y., Tsuchida, K., Shigemoto, R. and Nakanishi, S. (1991) Sequence and expression of a metabotropic glutamate receptor. Nature, 349, 760-765.
38. McBain, C. J. and Dingledine, R. (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurons of rat hippocampus. J. Physiol. (Lond.), 462, 373-392.
39. McBain, C. J., DiChiara, T. J. and Kauer, J. A. (1994) Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J. Neurosci., 14, 4433-4445.
40. Miles, R. and Poncer, J.-C. (1993) Metabotropic glutamate receptors mediate a post-tetanic excitation of guinea-pig hippocampal inhibitory, neurones. J. Physiol. (Lond.), 463, 461-473.
41. Morin, F., Beaulieu, C. and Lacaille, J. -C. (1996) Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J. Neurophysiol., 76, 1-16.
42. 2+ homeostasis in hippocampal neurons in vitro. Mol. Pharmacol., 35, 671-680.
43. Nakanishi, S. (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron, 13, 1031-1037.
44. Olbrich, H. G. and Braak, H. (1985) Ratio of pyramidal cells versus nonpyramidal cells in sector CA1 of the human Ammon's horn. Anat. Embryol., 173, 105-110.
45. Ouardouz, M. and Lacaille, J.-C. (1995) Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J. Neurophysiol., 73, 810-819.
46. 2+ changes induced by tetanic stimulation of afferents in rat hippocampal interneurons. Soc. Neurosci. Abstr., 22, 430.
47. Ozawa, S., Jino, M. and Tsuzuki, K. (1991) Two types of kainate response in cultured rat hippocampal neurons. J. Neurophysiol., 66, 2-11.
48. Perouansky, M. and Yaari, Y. (1993) Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. J. Physiol. (Lond.), 465, 223-244.
49. 2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron, 14, 1223-1231.
50. Ramon y Cajal, S. (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. Maloine, Paris.
51. Ribak, C. E., Vaughn, J. E. and Saito, K. (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res., 140, 315-332.
52. Robitaille, R. and Charlton, M. P. (1992) Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels. J. Neurosci., 12, 297-305.
53. Sah, P., Hestrin, S. and Nicoll, R. A. (1990) Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurones. J. Physiol. (Lond.), 430, 605-616.
54. Schwartzkroin, P. A. and Prince, D. A. (1980) Changes in excitatory and inhibitory synaptic potentials leading to epileptogenic activity. Brain Res., 183, 61-76.
55. i rise in GABAergic than non-GABAergic hippocampal neurons. Neurosci. Lett., 140, 243-246.
56. 2+ stores: activation and function. Trends Neurosci., 18, 299-306.
57. Somogyi, P., Hodgson, A. J., Smith, A. D., Nunzi, M. G., Gorio, A. and Wu, J. J. (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin-immunoreactive material. J. Neurosci., 4, 2590-2603.
58. Williams, S., Samulack, D. D., Beaulieu, C. and Lacaille, J.-C. (1994) Membrane properties and synaptic reponses 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.
59. 2+ responses induced by activation of mGluRs in hippocampal interneurons using confocal microscopy and whole cell recording. Soc. Neurosci. Abstr., 22, 430.
60. Woodson, W., Nitecka, L. and Ben-Ari, Y. (1989) Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J. Comp. Neurol., 280, 254-271.