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

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

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Glutamate-mediated regulation of intracellular Ca2+ levels was examined in different populations of CA1 interneurons, using confocal microscopy and the Ca2+ indicator fluo 3-AM in rat hippocampal slices. Interneurons in basal [stratum oriens/alveus (OA)] and apical [strata radiatum and lacunosum-moleculare (R/LM)] dendritic layers responded heterogeneously to glutamate. In control medium, OA interneurons responded mostly with oscillatory Ca2+ responses, which consisted of a large Ca2+ transient and successive smaller elevations. R/LM interneurons responded mostly with biphasic responses, characterized by an initial large transient and a secondary prolonged elevation. Other interneurons in both R/LM and OA responded with transient elevations in Ca2+ levels. Ionotropic glutamate receptor antagonists (±)2-amino-5-phosphonopentanoic acid and 6-cyano-7-nitro-quinoxaline-2,3-dione reduced peak Ca2+ responses in OA and R/LM cells, and blocked biphasic responses in R/LM interneurons. The metabotropic glutamate receptor antagonist (RS)-α-methyl-4-carboxyphenylglycine reduced peak Ca2+ responses only in OA interneurons, and prevented oscillatory responses. In low Ca2+ medium, peak responses were reduced in R/LM but not in OA interneurons, and oscillatory responses were absent. Combination of ionotropic and metabotropic receptor antagonists blocked all glutamate-evoked Ca2+ responses. Activation of different types of glutamate receptors may thus produce heterogeneous Ca2+ signals in subpopulations of CA1 interneurons. Ionotropic receptors may generate biphasic responses in interneurons in apical dendritic layers, whereas combined activation of metabotropic and ionotropic receptors may trigger oscillatory responses in interneurons of basal dendritic layers. These heterogeneous Ca2+ responses indicate that glutamate-mediated Ca2+ processes and second messenger systems differ in subpopulations of hippocampal interneurons and suggest possible postsynaptic functional specialization of interneurons.

Original languageEnglish
Pages (from-to)1625-1635
Number of pages11
JournalEuropean Journal of Neuroscience
Volume9
Issue number8
DOIs
Publication statusPublished - 1 Aug 1997

Fingerprint

Ionotropic Glutamate Receptors
Metabotropic Glutamate Receptors
Interneurons
Glutamic Acid
Excitatory Amino Acid Antagonists
2-Amino-5-phosphonovalerate
Quinoxalines
Glutamate Receptors
Second Messenger Systems
Confocal Microscopy

Keywords

  • Ca oscillations
  • fluo 3-AM
  • Hippocampus
  • Inhibitory cells
  • Intracellular Ca

Cite this

Carmant, Lionel ; Woodhall, Gavin ; Ouardouz, Mohamed ; Robitaille, Richard ; Lacaille, Jean Claude. / Interneuron-specific Ca2+ responses linked to metabotropic and ionotropic glutamate receptors in rat hippocampal slices. In: European Journal of Neuroscience. 1997 ; Vol. 9, No. 8. pp. 1625-1635.
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Interneuron-specific Ca2+ responses linked to metabotropic and ionotropic glutamate receptors in rat hippocampal slices. / Carmant, Lionel; Woodhall, Gavin; Ouardouz, Mohamed; Robitaille, Richard; Lacaille, Jean Claude.

In: European Journal of Neuroscience, Vol. 9, No. 8, 01.08.1997, p. 1625-1635.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Interneuron-specific Ca2+ responses linked to metabotropic and ionotropic glutamate receptors in rat hippocampal slices

AU - Carmant, Lionel

AU - Woodhall, Gavin

AU - Ouardouz, Mohamed

AU - Robitaille, Richard

AU - Lacaille, Jean Claude

PY - 1997/8/1

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N2 - Glutamate-mediated regulation of intracellular Ca2+ levels was examined in different populations of CA1 interneurons, using confocal microscopy and the Ca2+ indicator fluo 3-AM in rat hippocampal slices. Interneurons in basal [stratum oriens/alveus (OA)] and apical [strata radiatum and lacunosum-moleculare (R/LM)] dendritic layers responded heterogeneously to glutamate. In control medium, OA interneurons responded mostly with oscillatory Ca2+ responses, which consisted of a large Ca2+ transient and successive smaller elevations. R/LM interneurons responded mostly with biphasic responses, characterized by an initial large transient and a secondary prolonged elevation. Other interneurons in both R/LM and OA responded with transient elevations in Ca2+ levels. Ionotropic glutamate receptor antagonists (±)2-amino-5-phosphonopentanoic acid and 6-cyano-7-nitro-quinoxaline-2,3-dione reduced peak Ca2+ responses in OA and R/LM cells, and blocked biphasic responses in R/LM interneurons. The metabotropic glutamate receptor antagonist (RS)-α-methyl-4-carboxyphenylglycine reduced peak Ca2+ responses only in OA interneurons, and prevented oscillatory responses. In low Ca2+ medium, peak responses were reduced in R/LM but not in OA interneurons, and oscillatory responses were absent. Combination of ionotropic and metabotropic receptor antagonists blocked all glutamate-evoked Ca2+ responses. Activation of different types of glutamate receptors may thus produce heterogeneous Ca2+ signals in subpopulations of CA1 interneurons. Ionotropic receptors may generate biphasic responses in interneurons in apical dendritic layers, whereas combined activation of metabotropic and ionotropic receptors may trigger oscillatory responses in interneurons of basal dendritic layers. These heterogeneous Ca2+ responses indicate that glutamate-mediated Ca2+ processes and second messenger systems differ in subpopulations of hippocampal interneurons and suggest possible postsynaptic functional specialization of interneurons.

AB - Glutamate-mediated regulation of intracellular Ca2+ levels was examined in different populations of CA1 interneurons, using confocal microscopy and the Ca2+ indicator fluo 3-AM in rat hippocampal slices. Interneurons in basal [stratum oriens/alveus (OA)] and apical [strata radiatum and lacunosum-moleculare (R/LM)] dendritic layers responded heterogeneously to glutamate. In control medium, OA interneurons responded mostly with oscillatory Ca2+ responses, which consisted of a large Ca2+ transient and successive smaller elevations. R/LM interneurons responded mostly with biphasic responses, characterized by an initial large transient and a secondary prolonged elevation. Other interneurons in both R/LM and OA responded with transient elevations in Ca2+ levels. Ionotropic glutamate receptor antagonists (±)2-amino-5-phosphonopentanoic acid and 6-cyano-7-nitro-quinoxaline-2,3-dione reduced peak Ca2+ responses in OA and R/LM cells, and blocked biphasic responses in R/LM interneurons. The metabotropic glutamate receptor antagonist (RS)-α-methyl-4-carboxyphenylglycine reduced peak Ca2+ responses only in OA interneurons, and prevented oscillatory responses. In low Ca2+ medium, peak responses were reduced in R/LM but not in OA interneurons, and oscillatory responses were absent. Combination of ionotropic and metabotropic receptor antagonists blocked all glutamate-evoked Ca2+ responses. Activation of different types of glutamate receptors may thus produce heterogeneous Ca2+ signals in subpopulations of CA1 interneurons. Ionotropic receptors may generate biphasic responses in interneurons in apical dendritic layers, whereas combined activation of metabotropic and ionotropic receptors may trigger oscillatory responses in interneurons of basal dendritic layers. These heterogeneous Ca2+ responses indicate that glutamate-mediated Ca2+ processes and second messenger systems differ in subpopulations of hippocampal interneurons and suggest possible postsynaptic functional specialization of interneurons.

KW - Ca oscillations

KW - fluo 3-AM

KW - Hippocampus

KW - Inhibitory cells

KW - Intracellular Ca

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