Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells

Hippocampal interneurons release the inhibitory transmitter GABA to regulate excitation, rhythm generation and synaptic plasticity. A subpopulation of GABAergic basket cells co-expresses the GABA/glycine vesicular transporters (VIAAT) and the atypical type III vesicular glutamate transporter (VGLUT3...

Full description

Bibliographic Details
Main Authors: Caroline Fasano, Jill Rocchetti, Katarzyna Pietrajtis, Johannes-Friedrich Zander, Frédéric Manseau, Diana Y. Sakae, Maya Marcus-Sells, Lauriane Ramet, Lydie J. Morel, Damien Carrel, Sylvie Dumas, Susanne Bolte, Véronique Bernard, Erika Vigneault, Romain Goutagny, Gudrun Ahnert-Hilger, Bruno Giros, Stéphanie Daumas, Sylvain Williams, Salah El Mestikawy
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-05-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncel.2017.00140/full
_version_ 1819137175808114688
author Caroline Fasano
Jill Rocchetti
Katarzyna Pietrajtis
Johannes-Friedrich Zander
Frédéric Manseau
Diana Y. Sakae
Maya Marcus-Sells
Lauriane Ramet
Lydie J. Morel
Damien Carrel
Sylvie Dumas
Susanne Bolte
Véronique Bernard
Erika Vigneault
Romain Goutagny
Gudrun Ahnert-Hilger
Bruno Giros
Bruno Giros
Stéphanie Daumas
Sylvain Williams
Salah El Mestikawy
Salah El Mestikawy
author_facet Caroline Fasano
Jill Rocchetti
Katarzyna Pietrajtis
Johannes-Friedrich Zander
Frédéric Manseau
Diana Y. Sakae
Maya Marcus-Sells
Lauriane Ramet
Lydie J. Morel
Damien Carrel
Sylvie Dumas
Susanne Bolte
Véronique Bernard
Erika Vigneault
Romain Goutagny
Gudrun Ahnert-Hilger
Bruno Giros
Bruno Giros
Stéphanie Daumas
Sylvain Williams
Salah El Mestikawy
Salah El Mestikawy
author_sort Caroline Fasano
collection DOAJ
description Hippocampal interneurons release the inhibitory transmitter GABA to regulate excitation, rhythm generation and synaptic plasticity. A subpopulation of GABAergic basket cells co-expresses the GABA/glycine vesicular transporters (VIAAT) and the atypical type III vesicular glutamate transporter (VGLUT3); therefore, these cells have the ability to signal with both GABA and glutamate. GABAergic transmission by basket cells has been extensively characterized but nothing is known about the functional implications of VGLUT3-dependent glutamate released by these cells. Here, using VGLUT3-null mice we observed that the loss of VGLUT3 results in a metaplastic shift in synaptic plasticity at Shaeffer’s collaterals – CA1 synapses and an altered theta oscillation. These changes were paralleled by the loss of a VGLUT3-dependent inhibition of GABAergic current in CA1 pyramidal layer. Therefore presynaptic type III metabotropic could be activated by glutamate released from VGLUT3-positive interneurons. This putative presynaptic heterologous feedback mechanism inhibits local GABAergic tone and regulates the hippocampal neuronal network.
first_indexed 2024-12-22T10:46:42Z
format Article
id doaj.art-129d07f0b5a44664b56ac9b5dcd7bb5d
institution Directory Open Access Journal
issn 1662-5102
language English
last_indexed 2024-12-22T10:46:42Z
publishDate 2017-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular Neuroscience
spelling doaj.art-129d07f0b5a44664b56ac9b5dcd7bb5d2022-12-21T18:28:54ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022017-05-011110.3389/fncel.2017.00140258170Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket CellsCaroline Fasano0Jill Rocchetti1Katarzyna Pietrajtis2Johannes-Friedrich Zander3Frédéric Manseau4Diana Y. Sakae5Maya Marcus-Sells6Lauriane Ramet7Lydie J. Morel8Damien Carrel9Sylvie Dumas10Susanne Bolte11Véronique Bernard12Erika Vigneault13Romain Goutagny14Gudrun Ahnert-Hilger15Bruno Giros16Bruno Giros17Stéphanie Daumas18Sylvain Williams19Salah El Mestikawy20Salah El Mestikawy21Douglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaInstitut für Integrative Neuroanatomie Research CenterBerlin, GermanyDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceUniversité Paris Descartes, Sorbonne Paris Cité, Centre National de la Recherche Scientifique, UMR 8250Paris, FranceOramacellParis, FranceSorbonne Universités, UPMC Univ Paris 06, CNRS, Core Facilities - Institut de Biologie Paris SeineParis, FranceSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaCNRS UMR 7364, Team NCD, Université de StrasbourgStrasbourg, FranceInstitut für Integrative Neuroanatomie Research CenterBerlin, GermanyDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaDouglas Mental Health University Institute, Department of Psychiatry, McGill University, MontrealQC, CanadaSorbonne Universités, UPMC Univ Paris 06, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Medicale, Institut de Biologie Paris Seine, Neuroscience Paris Seine (NPS)Paris, FranceHippocampal interneurons release the inhibitory transmitter GABA to regulate excitation, rhythm generation and synaptic plasticity. A subpopulation of GABAergic basket cells co-expresses the GABA/glycine vesicular transporters (VIAAT) and the atypical type III vesicular glutamate transporter (VGLUT3); therefore, these cells have the ability to signal with both GABA and glutamate. GABAergic transmission by basket cells has been extensively characterized but nothing is known about the functional implications of VGLUT3-dependent glutamate released by these cells. Here, using VGLUT3-null mice we observed that the loss of VGLUT3 results in a metaplastic shift in synaptic plasticity at Shaeffer’s collaterals – CA1 synapses and an altered theta oscillation. These changes were paralleled by the loss of a VGLUT3-dependent inhibition of GABAergic current in CA1 pyramidal layer. Therefore presynaptic type III metabotropic could be activated by glutamate released from VGLUT3-positive interneurons. This putative presynaptic heterologous feedback mechanism inhibits local GABAergic tone and regulates the hippocampal neuronal network.http://journal.frontiersin.org/article/10.3389/fncel.2017.00140/fullhippocampusbasket cellvesicular glutamate transporter type 3glutamate/GABA co-transmissiontype III mGluRs
spellingShingle Caroline Fasano
Jill Rocchetti
Katarzyna Pietrajtis
Johannes-Friedrich Zander
Frédéric Manseau
Diana Y. Sakae
Maya Marcus-Sells
Lauriane Ramet
Lydie J. Morel
Damien Carrel
Sylvie Dumas
Susanne Bolte
Véronique Bernard
Erika Vigneault
Romain Goutagny
Gudrun Ahnert-Hilger
Bruno Giros
Bruno Giros
Stéphanie Daumas
Sylvain Williams
Salah El Mestikawy
Salah El Mestikawy
Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
Frontiers in Cellular Neuroscience
hippocampus
basket cell
vesicular glutamate transporter type 3
glutamate/GABA co-transmission
type III mGluRs
title Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
title_full Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
title_fullStr Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
title_full_unstemmed Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
title_short Regulation of the Hippocampal Network by VGLUT3-Positive CCK- GABAergic Basket Cells
title_sort regulation of the hippocampal network by vglut3 positive cck gabaergic basket cells
topic hippocampus
basket cell
vesicular glutamate transporter type 3
glutamate/GABA co-transmission
type III mGluRs
url http://journal.frontiersin.org/article/10.3389/fncel.2017.00140/full
work_keys_str_mv AT carolinefasano regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT jillrocchetti regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT katarzynapietrajtis regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT johannesfriedrichzander regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT fredericmanseau regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT dianaysakae regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT mayamarcussells regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT laurianeramet regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT lydiejmorel regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT damiencarrel regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT sylviedumas regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT susannebolte regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT veroniquebernard regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT erikavigneault regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT romaingoutagny regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT gudrunahnerthilger regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT brunogiros regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT brunogiros regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT stephaniedaumas regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT sylvainwilliams regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT salahelmestikawy regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells
AT salahelmestikawy regulationofthehippocampalnetworkbyvglut3positivecckgabaergicbasketcells