Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons

GABAA receptors present in extrasynaptic areas mediate tonic inhibition in hippocampal neurons regulating the performance of neural networks. In this study, we investigated the effect of NMDA-induced plasticity on tonic inhibition in somatostatin- and parvalbumin-containing interneurons. Using pharm...

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Main Authors: Marcin Wyroślak, Grzegorz Dobrzański, Jerzy W. Mozrzymas
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2023.1193383/full
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author Marcin Wyroślak
Grzegorz Dobrzański
Jerzy W. Mozrzymas
author_facet Marcin Wyroślak
Grzegorz Dobrzański
Jerzy W. Mozrzymas
author_sort Marcin Wyroślak
collection DOAJ
description GABAA receptors present in extrasynaptic areas mediate tonic inhibition in hippocampal neurons regulating the performance of neural networks. In this study, we investigated the effect of NMDA-induced plasticity on tonic inhibition in somatostatin- and parvalbumin-containing interneurons. Using pharmacological methods and transgenic mice (SST-Cre/PV-Cre x Ai14), we induced the plasticity of GABAergic transmission in somatostatin- and parvalbumin-containing interneurons by a brief (3 min) application of NMDA. In the whole-cell patch-clamp configuration, we measured tonic currents enhanced by specific agonists (etomidate or gaboxadol). Furthermore, in both the control and NMDA-treated groups, we examined to what extent these changes depend on the regulation of distinct subtypes of GABAA receptors. Tonic conductance in the somatostatin-containing (SST+) interneurons is enhanced after NMDA application, and the observed effect is associated with an increased content of α5-containing GABAARs. Both fast-spiking and non–fast-spiking parvalbumin-positive (PV+) cells showed a reduction of tonic inhibition after plasticity induction. This effect was accompanied in both PV+ interneuron types by a strongly reduced proportion of δ-subunit-containing GABAARs and a relatively small increase in currents mediated by α5-containing GABAARs. Both somatostatin- and parvalbumin-containing interneurons show cell type-dependent and opposite sign plasticity of tonic inhibition. The underlying mechanisms depend on the cell-specific balance of plastic changes in the contents of α5 and δ subunit-containing GABAARs.
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spelling doaj.art-ec883cc3ef3241acbc45c46405e4f8722023-06-28T08:49:38ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-06-011710.3389/fncel.2023.11933831193383Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneuronsMarcin Wyroślak0Grzegorz Dobrzański1Jerzy W. Mozrzymas2Department of Biophysics and Neuroscience, Wroclaw Medical University, Wrocław, PolandNencki Institute of Experimental Biology, Warsaw, PolandDepartment of Biophysics and Neuroscience, Wroclaw Medical University, Wrocław, PolandGABAA receptors present in extrasynaptic areas mediate tonic inhibition in hippocampal neurons regulating the performance of neural networks. In this study, we investigated the effect of NMDA-induced plasticity on tonic inhibition in somatostatin- and parvalbumin-containing interneurons. Using pharmacological methods and transgenic mice (SST-Cre/PV-Cre x Ai14), we induced the plasticity of GABAergic transmission in somatostatin- and parvalbumin-containing interneurons by a brief (3 min) application of NMDA. In the whole-cell patch-clamp configuration, we measured tonic currents enhanced by specific agonists (etomidate or gaboxadol). Furthermore, in both the control and NMDA-treated groups, we examined to what extent these changes depend on the regulation of distinct subtypes of GABAA receptors. Tonic conductance in the somatostatin-containing (SST+) interneurons is enhanced after NMDA application, and the observed effect is associated with an increased content of α5-containing GABAARs. Both fast-spiking and non–fast-spiking parvalbumin-positive (PV+) cells showed a reduction of tonic inhibition after plasticity induction. This effect was accompanied in both PV+ interneuron types by a strongly reduced proportion of δ-subunit-containing GABAARs and a relatively small increase in currents mediated by α5-containing GABAARs. Both somatostatin- and parvalbumin-containing interneurons show cell type-dependent and opposite sign plasticity of tonic inhibition. The underlying mechanisms depend on the cell-specific balance of plastic changes in the contents of α5 and δ subunit-containing GABAARs.https://www.frontiersin.org/articles/10.3389/fncel.2023.1193383/fullGABAtonic inhibitionhippocampusinterneuronsplasticityextrasynaptic receptors
spellingShingle Marcin Wyroślak
Grzegorz Dobrzański
Jerzy W. Mozrzymas
Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
Frontiers in Cellular Neuroscience
GABA
tonic inhibition
hippocampus
interneurons
plasticity
extrasynaptic receptors
title Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
title_full Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
title_fullStr Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
title_full_unstemmed Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
title_short Bidirectional plasticity of GABAergic tonic inhibition in hippocampal somatostatin- and parvalbumin-containing interneurons
title_sort bidirectional plasticity of gabaergic tonic inhibition in hippocampal somatostatin and parvalbumin containing interneurons
topic GABA
tonic inhibition
hippocampus
interneurons
plasticity
extrasynaptic receptors
url https://www.frontiersin.org/articles/10.3389/fncel.2023.1193383/full
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AT grzegorzdobrzanski bidirectionalplasticityofgabaergictonicinhibitioninhippocampalsomatostatinandparvalbumincontaininginterneurons
AT jerzywmozrzymas bidirectionalplasticityofgabaergictonicinhibitioninhippocampalsomatostatinandparvalbumincontaininginterneurons