Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons

Gavin Woodhall, Christine E. Gee, Richard Robitaille, Jean Claude Lacaille*

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Metabotropic glutamate receptors (mGluRs) are expressed heterogeneously in hippocampal interneurons, and their signal transduction cascades remain largely unclear. We characterized an oscillatory response activated by the mGluR agonist 1S, 3R-1-aminocyclopentane-1,3-dicarboxylic acid (1S, 3R-ACPD) in hippocampal interneurons of stratum oriens-alveus (OA) with simultaneous whole cell current-clamp recordings and intracellular Ca2+ imaging with confocal microscopy. 1S, 3R-ACPD induced oscillatory membrane depolarizations and rises in intracellular Ca2+ that persisted in tetrodotoxin and were blocked by the antagonist of group I and II mGluRs (S)-α-methyl-4- carboxyphenylglycine. Membrane depolarizations and intracellular Ca2+ rises were blocked by extracellular Cd2+ and in Ca2+-free medium, mGluR responses therefore required Ca2+ influx via voltage-gated Ca2+ channels, 1S,3R-ACPD responses were also antagonized by depleting intracellular stores with thapsigargin and ryanodine, indicating that Ca2+ release from intracellular stores was also necessary. These data suggest that oscillatory responses generated by group I/II mGluRs involve a coupling of Ca2+ entry through voltage-gated Ca2+ channels and Ca2+ release from internal stores. In contrast, 1S, 3R-ACPD evoked only smaller depolarizations and intracellular Ca2+ rises, with no oscillations, in other hippocampal interneurons located in or near stratum lacunosum-moleculare. Thus mGluR- mediated oscillatory responses are specifically expressed in certain interneuron subtypes. This heterogeneous expression of glutamate and Ca2+ signaling pathways in specific interneurons may be relevant to their selective vulnerability to excitotoxicity.

Original languageEnglish
Pages (from-to)371-382
Number of pages12
JournalJournal of Neurophysiology
Volume81
Issue number1
DOIs
Publication statusPublished - 1 Jan 1999

Fingerprint

Metabotropic Glutamate Receptors
Interneurons
Membrane Potentials
Ryanodine
Intracellular Membranes
Thapsigargin
Tetrodotoxin
Confocal Microscopy
Glutamic Acid
Signal Transduction
Membranes
1-amino-1,3-dicarboxycyclopentane

Cite this

Woodhall, Gavin ; Gee, Christine E. ; Robitaille, Richard ; Lacaille, Jean Claude. / Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons. In: Journal of Neurophysiology. 1999 ; Vol. 81, No. 1. pp. 371-382.
@article{ec61426616e748d5a96c51e194db2a96,
title = "Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons",
abstract = "Metabotropic glutamate receptors (mGluRs) are expressed heterogeneously in hippocampal interneurons, and their signal transduction cascades remain largely unclear. We characterized an oscillatory response activated by the mGluR agonist 1S, 3R-1-aminocyclopentane-1,3-dicarboxylic acid (1S, 3R-ACPD) in hippocampal interneurons of stratum oriens-alveus (OA) with simultaneous whole cell current-clamp recordings and intracellular Ca2+ imaging with confocal microscopy. 1S, 3R-ACPD induced oscillatory membrane depolarizations and rises in intracellular Ca2+ that persisted in tetrodotoxin and were blocked by the antagonist of group I and II mGluRs (S)-α-methyl-4- carboxyphenylglycine. Membrane depolarizations and intracellular Ca2+ rises were blocked by extracellular Cd2+ and in Ca2+-free medium, mGluR responses therefore required Ca2+ influx via voltage-gated Ca2+ channels, 1S,3R-ACPD responses were also antagonized by depleting intracellular stores with thapsigargin and ryanodine, indicating that Ca2+ release from intracellular stores was also necessary. These data suggest that oscillatory responses generated by group I/II mGluRs involve a coupling of Ca2+ entry through voltage-gated Ca2+ channels and Ca2+ release from internal stores. In contrast, 1S, 3R-ACPD evoked only smaller depolarizations and intracellular Ca2+ rises, with no oscillations, in other hippocampal interneurons located in or near stratum lacunosum-moleculare. Thus mGluR- mediated oscillatory responses are specifically expressed in certain interneuron subtypes. This heterogeneous expression of glutamate and Ca2+ signaling pathways in specific interneurons may be relevant to their selective vulnerability to excitotoxicity.",
author = "Gavin Woodhall and Gee, {Christine E.} and Richard Robitaille and Lacaille, {Jean Claude}",
year = "1999",
month = "1",
day = "1",
doi = "10.1152/jn.1999.81.1.371",
language = "English",
volume = "81",
pages = "371--382",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "1",

}

Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons. / Woodhall, Gavin; Gee, Christine E.; Robitaille, Richard; Lacaille, Jean Claude.

In: Journal of Neurophysiology, Vol. 81, No. 1, 01.01.1999, p. 371-382.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Membrane potential and intracellular Ca2+ oscillations activated by mGluRs in hippocampal stratum oriens/alveus interneurons

AU - Woodhall, Gavin

AU - Gee, Christine E.

AU - Robitaille, Richard

AU - Lacaille, Jean Claude

PY - 1999/1/1

Y1 - 1999/1/1

N2 - Metabotropic glutamate receptors (mGluRs) are expressed heterogeneously in hippocampal interneurons, and their signal transduction cascades remain largely unclear. We characterized an oscillatory response activated by the mGluR agonist 1S, 3R-1-aminocyclopentane-1,3-dicarboxylic acid (1S, 3R-ACPD) in hippocampal interneurons of stratum oriens-alveus (OA) with simultaneous whole cell current-clamp recordings and intracellular Ca2+ imaging with confocal microscopy. 1S, 3R-ACPD induced oscillatory membrane depolarizations and rises in intracellular Ca2+ that persisted in tetrodotoxin and were blocked by the antagonist of group I and II mGluRs (S)-α-methyl-4- carboxyphenylglycine. Membrane depolarizations and intracellular Ca2+ rises were blocked by extracellular Cd2+ and in Ca2+-free medium, mGluR responses therefore required Ca2+ influx via voltage-gated Ca2+ channels, 1S,3R-ACPD responses were also antagonized by depleting intracellular stores with thapsigargin and ryanodine, indicating that Ca2+ release from intracellular stores was also necessary. These data suggest that oscillatory responses generated by group I/II mGluRs involve a coupling of Ca2+ entry through voltage-gated Ca2+ channels and Ca2+ release from internal stores. In contrast, 1S, 3R-ACPD evoked only smaller depolarizations and intracellular Ca2+ rises, with no oscillations, in other hippocampal interneurons located in or near stratum lacunosum-moleculare. Thus mGluR- mediated oscillatory responses are specifically expressed in certain interneuron subtypes. This heterogeneous expression of glutamate and Ca2+ signaling pathways in specific interneurons may be relevant to their selective vulnerability to excitotoxicity.

AB - Metabotropic glutamate receptors (mGluRs) are expressed heterogeneously in hippocampal interneurons, and their signal transduction cascades remain largely unclear. We characterized an oscillatory response activated by the mGluR agonist 1S, 3R-1-aminocyclopentane-1,3-dicarboxylic acid (1S, 3R-ACPD) in hippocampal interneurons of stratum oriens-alveus (OA) with simultaneous whole cell current-clamp recordings and intracellular Ca2+ imaging with confocal microscopy. 1S, 3R-ACPD induced oscillatory membrane depolarizations and rises in intracellular Ca2+ that persisted in tetrodotoxin and were blocked by the antagonist of group I and II mGluRs (S)-α-methyl-4- carboxyphenylglycine. Membrane depolarizations and intracellular Ca2+ rises were blocked by extracellular Cd2+ and in Ca2+-free medium, mGluR responses therefore required Ca2+ influx via voltage-gated Ca2+ channels, 1S,3R-ACPD responses were also antagonized by depleting intracellular stores with thapsigargin and ryanodine, indicating that Ca2+ release from intracellular stores was also necessary. These data suggest that oscillatory responses generated by group I/II mGluRs involve a coupling of Ca2+ entry through voltage-gated Ca2+ channels and Ca2+ release from internal stores. In contrast, 1S, 3R-ACPD evoked only smaller depolarizations and intracellular Ca2+ rises, with no oscillations, in other hippocampal interneurons located in or near stratum lacunosum-moleculare. Thus mGluR- mediated oscillatory responses are specifically expressed in certain interneuron subtypes. This heterogeneous expression of glutamate and Ca2+ signaling pathways in specific interneurons may be relevant to their selective vulnerability to excitotoxicity.

UR - http://www.scopus.com/inward/record.url?scp=0032988533&partnerID=8YFLogxK

UR - https://www.physiology.org/doi/full/10.1152/jn.1999.81.1.371

U2 - 10.1152/jn.1999.81.1.371

DO - 10.1152/jn.1999.81.1.371

M3 - Article

C2 - 9914296

AN - SCOPUS:0032988533

VL - 81

SP - 371

EP - 382

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 1

ER -