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GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission.
J Physiol. 2003 Nov 15; 553(Pt 1):155-67.JP

Abstract

Repetitive stimulation of Schaffer collaterals induces activity-dependent changes in the strength of polysynaptic inhibitory postsynaptic potentials (IPSPs) in hippocampal CA1 pyramidal neurons that are dependent on stimulation parameters. In the present study, we investigated the effects of two stimulation patterns, theta-burst stimulation (TBS) and 100 Hz tetani, on pharmacologically isolated monosynaptic GABAergic responses in adult CA1 pyramidal cells. Tetanization with 100 Hz trains transiently depressed both early and late IPSPs, whereas TBS induced long-term potentiation (LTP) of early IPSPs that lasted at least 30 min. Mechanisms mediating this TBS-induced potentiation were examined using whole-cell recordings. The paired-pulse ratio of monosynaptic inhibitory postsynaptic currents (IPSCs) was not affected during LTP, suggesting that presynaptic changes in GABA release are not involved in the potentiation. Bath application of the GABAB receptor antagonist CGP55845 or the group I/II metabotropic glutamate receptor antagonist E4-CPG inhibited IPSC potentiation. Preventing postsynaptic G-protein activation or Ca2+ rise by postsynaptic injection of GDP-beta-S or BAPTA, respectively, abolished LTP, indicating a G-protein- and Ca2+-dependent induction in this LTP. Finally during paired-recordings, activation of individual interneurons by intracellular TBS elicited solely short-term increases in average unitary IPSCs in pyramidal cells. These results indicate that a stimulation paradigm mimicking the endogenous theta rhythm activates cooperative postsynaptic mechanisms dependent on GABABR, mGluR, G-proteins and intracellular Ca2+, which lead to a sustained potentiation of GABAA synaptic transmission in pyramidal cells. GABAergic synapses may therefore contribute to functional synaptic plasticity in adult hippocampus.

Authors+Show Affiliations

Centre de Recherche en Sciences Neurologiques et Département de Physiologie, Université de Montréal, Montréal, Québec, Canada H3C 3J7.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

12963794

Citation

Patenaude, Christian, et al. "GABAB Receptor- and Metabotropic Glutamate Receptor-dependent Cooperative Long-term Potentiation of Rat Hippocampal GABAA Synaptic Transmission." The Journal of Physiology, vol. 553, no. Pt 1, 2003, pp. 155-67.
Patenaude C, Chapman CA, Bertrand S, et al. GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission. J Physiol. 2003;553(Pt 1):155-67.
Patenaude, C., Chapman, C. A., Bertrand, S., Congar, P., & Lacaille, J. C. (2003). GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission. The Journal of Physiology, 553(Pt 1), 155-67.
Patenaude C, et al. GABAB Receptor- and Metabotropic Glutamate Receptor-dependent Cooperative Long-term Potentiation of Rat Hippocampal GABAA Synaptic Transmission. J Physiol. 2003 Nov 15;553(Pt 1):155-67. PubMed PMID: 12963794.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission. AU - Patenaude,Christian, AU - Chapman,C Andrew, AU - Bertrand,Sandrine, AU - Congar,Patrice, AU - Lacaille,Jean-Claude, Y1 - 2003/09/08/ PY - 2003/9/10/pubmed PY - 2004/7/16/medline PY - 2003/9/10/entrez SP - 155 EP - 67 JF - The Journal of physiology JO - J Physiol VL - 553 IS - Pt 1 N2 - Repetitive stimulation of Schaffer collaterals induces activity-dependent changes in the strength of polysynaptic inhibitory postsynaptic potentials (IPSPs) in hippocampal CA1 pyramidal neurons that are dependent on stimulation parameters. In the present study, we investigated the effects of two stimulation patterns, theta-burst stimulation (TBS) and 100 Hz tetani, on pharmacologically isolated monosynaptic GABAergic responses in adult CA1 pyramidal cells. Tetanization with 100 Hz trains transiently depressed both early and late IPSPs, whereas TBS induced long-term potentiation (LTP) of early IPSPs that lasted at least 30 min. Mechanisms mediating this TBS-induced potentiation were examined using whole-cell recordings. The paired-pulse ratio of monosynaptic inhibitory postsynaptic currents (IPSCs) was not affected during LTP, suggesting that presynaptic changes in GABA release are not involved in the potentiation. Bath application of the GABAB receptor antagonist CGP55845 or the group I/II metabotropic glutamate receptor antagonist E4-CPG inhibited IPSC potentiation. Preventing postsynaptic G-protein activation or Ca2+ rise by postsynaptic injection of GDP-beta-S or BAPTA, respectively, abolished LTP, indicating a G-protein- and Ca2+-dependent induction in this LTP. Finally during paired-recordings, activation of individual interneurons by intracellular TBS elicited solely short-term increases in average unitary IPSCs in pyramidal cells. These results indicate that a stimulation paradigm mimicking the endogenous theta rhythm activates cooperative postsynaptic mechanisms dependent on GABABR, mGluR, G-proteins and intracellular Ca2+, which lead to a sustained potentiation of GABAA synaptic transmission in pyramidal cells. GABAergic synapses may therefore contribute to functional synaptic plasticity in adult hippocampus. SN - 0022-3751 UR - https://www.unboundmedicine.com/medline/citation/12963794/GABAB_receptor__and_metabotropic_glutamate_receptor_dependent_cooperative_long_term_potentiation_of_rat_hippocampal_GABAA_synaptic_transmission_ L2 - https://doi.org/10.1113/jphysiol.2003.049015 DB - PRIME DP - Unbound Medicine ER -