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Region-specific and state-dependent action of striatal GABAergic interneurons

Striatum processes a wide range of functions including goal-directed behavior and habit formation, respectively encoded by the dorsomedial striatum (DMS) and dorsolateral striatum (DLS). GABAergic feedforward inhibition is known to control the integration of cortical information by striatal projecti...

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Autores principales: Fino, Elodie, Vandecasteele, Marie, Perez, Sylvie, Saudou, Frédéric, Venance, Laurent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6104028/
https://www.ncbi.nlm.nih.gov/pubmed/30131490
http://dx.doi.org/10.1038/s41467-018-05847-5
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author Fino, Elodie
Vandecasteele, Marie
Perez, Sylvie
Saudou, Frédéric
Venance, Laurent
author_facet Fino, Elodie
Vandecasteele, Marie
Perez, Sylvie
Saudou, Frédéric
Venance, Laurent
author_sort Fino, Elodie
collection PubMed
description Striatum processes a wide range of functions including goal-directed behavior and habit formation, respectively encoded by the dorsomedial striatum (DMS) and dorsolateral striatum (DLS). GABAergic feedforward inhibition is known to control the integration of cortical information by striatal projection neurons (SPNs). Here we questioned whether this control is specific between distinct striatal functional territories. Using opto-activation and opto-inhibition of identified GABAergic interneurons, we found that different circuits are engaged in DLS and DMS, both ex vivo and in vivo: while parvalbumin interneurons efficiently control SPNs in DLS, somatostatin interneurons control SPNs in DMS. Moreover, both parvalbumin and somatostatin interneurons use a dual hyperpolarizing/depolarizing effect to control cortical input integration depending on SPN activity state: GABAergic interneurons potently inhibit spiking SPNs while in resting SPNs, they favor cortical activity summation via a depolarizing effect. Our findings establish that striatal GABAergic interneurons exert efficient territory-specific and state-dependent control of SPN activity and functional output.
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spelling pubmed-61040282018-08-23 Region-specific and state-dependent action of striatal GABAergic interneurons Fino, Elodie Vandecasteele, Marie Perez, Sylvie Saudou, Frédéric Venance, Laurent Nat Commun Article Striatum processes a wide range of functions including goal-directed behavior and habit formation, respectively encoded by the dorsomedial striatum (DMS) and dorsolateral striatum (DLS). GABAergic feedforward inhibition is known to control the integration of cortical information by striatal projection neurons (SPNs). Here we questioned whether this control is specific between distinct striatal functional territories. Using opto-activation and opto-inhibition of identified GABAergic interneurons, we found that different circuits are engaged in DLS and DMS, both ex vivo and in vivo: while parvalbumin interneurons efficiently control SPNs in DLS, somatostatin interneurons control SPNs in DMS. Moreover, both parvalbumin and somatostatin interneurons use a dual hyperpolarizing/depolarizing effect to control cortical input integration depending on SPN activity state: GABAergic interneurons potently inhibit spiking SPNs while in resting SPNs, they favor cortical activity summation via a depolarizing effect. Our findings establish that striatal GABAergic interneurons exert efficient territory-specific and state-dependent control of SPN activity and functional output. Nature Publishing Group UK 2018-08-21 /pmc/articles/PMC6104028/ /pubmed/30131490 http://dx.doi.org/10.1038/s41467-018-05847-5 Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Fino, Elodie
Vandecasteele, Marie
Perez, Sylvie
Saudou, Frédéric
Venance, Laurent
Region-specific and state-dependent action of striatal GABAergic interneurons
title Region-specific and state-dependent action of striatal GABAergic interneurons
title_full Region-specific and state-dependent action of striatal GABAergic interneurons
title_fullStr Region-specific and state-dependent action of striatal GABAergic interneurons
title_full_unstemmed Region-specific and state-dependent action of striatal GABAergic interneurons
title_short Region-specific and state-dependent action of striatal GABAergic interneurons
title_sort region-specific and state-dependent action of striatal gabaergic interneurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6104028/
https://www.ncbi.nlm.nih.gov/pubmed/30131490
http://dx.doi.org/10.1038/s41467-018-05847-5
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