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Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex

Inhibitory interneurons play central roles in the modulation of spontaneous network activity and in processing of neuronal information. In sensory neocortical areas, parvalbumin-positive (PV+) GABAergic interneurons control the representation and processing of peripheral sensory inputs. We studied t...

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Autores principales: Yeganeh, Fahimeh, Knauer, Beate, Guimarães Backhaus, Roberta, Yang, Jenq-Wei, Stroh, Albrecht, Luhmann, Heiko J., Stüttgen, Maik C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9653449/
https://www.ncbi.nlm.nih.gov/pubmed/36371511
http://dx.doi.org/10.1038/s41598-022-24156-y
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author Yeganeh, Fahimeh
Knauer, Beate
Guimarães Backhaus, Roberta
Yang, Jenq-Wei
Stroh, Albrecht
Luhmann, Heiko J.
Stüttgen, Maik C.
author_facet Yeganeh, Fahimeh
Knauer, Beate
Guimarães Backhaus, Roberta
Yang, Jenq-Wei
Stroh, Albrecht
Luhmann, Heiko J.
Stüttgen, Maik C.
author_sort Yeganeh, Fahimeh
collection PubMed
description Inhibitory interneurons play central roles in the modulation of spontaneous network activity and in processing of neuronal information. In sensory neocortical areas, parvalbumin-positive (PV+) GABAergic interneurons control the representation and processing of peripheral sensory inputs. We studied the functional role of PV+ interneurons in the barrel cortex of anesthetized adult PVCre mice by combining extracellular multi-electrode recordings with optogenetic silencing of a small fraction of PV+ interneurons. In all cortical layers, optogenetic inhibition caused an increase in spontaneous network activity from theta to gamma frequencies. The spatio-temporal representation of sensory inputs was studied by stimulating one or two whiskers at different intervals and analyzing the resulting local field potential (LFP) and single unit (SU) response. Silencing PV+ interneurons caused an increase in LFP response to sensory stimulation and a decrease in temporal discrimination of consecutive whisker deflections. The combined effect of whisker deflection and optogenetic inhibition was highly similar to the linear sum of the individual effects of these two manipulations. SU recordings revealed that optogenetic silencing reduced stimulus detectability by increasing stimulus-evoked firing rate by a constant offset, suggesting that PV+ interneurons improve signal-to-noise ratio by reducing ongoing spiking activity, thereby sharpening the spatio-temporal representation of sensory stimuli.
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spelling pubmed-96534492022-11-15 Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex Yeganeh, Fahimeh Knauer, Beate Guimarães Backhaus, Roberta Yang, Jenq-Wei Stroh, Albrecht Luhmann, Heiko J. Stüttgen, Maik C. Sci Rep Article Inhibitory interneurons play central roles in the modulation of spontaneous network activity and in processing of neuronal information. In sensory neocortical areas, parvalbumin-positive (PV+) GABAergic interneurons control the representation and processing of peripheral sensory inputs. We studied the functional role of PV+ interneurons in the barrel cortex of anesthetized adult PVCre mice by combining extracellular multi-electrode recordings with optogenetic silencing of a small fraction of PV+ interneurons. In all cortical layers, optogenetic inhibition caused an increase in spontaneous network activity from theta to gamma frequencies. The spatio-temporal representation of sensory inputs was studied by stimulating one or two whiskers at different intervals and analyzing the resulting local field potential (LFP) and single unit (SU) response. Silencing PV+ interneurons caused an increase in LFP response to sensory stimulation and a decrease in temporal discrimination of consecutive whisker deflections. The combined effect of whisker deflection and optogenetic inhibition was highly similar to the linear sum of the individual effects of these two manipulations. SU recordings revealed that optogenetic silencing reduced stimulus detectability by increasing stimulus-evoked firing rate by a constant offset, suggesting that PV+ interneurons improve signal-to-noise ratio by reducing ongoing spiking activity, thereby sharpening the spatio-temporal representation of sensory stimuli. Nature Publishing Group UK 2022-11-12 /pmc/articles/PMC9653449/ /pubmed/36371511 http://dx.doi.org/10.1038/s41598-022-24156-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Yeganeh, Fahimeh
Knauer, Beate
Guimarães Backhaus, Roberta
Yang, Jenq-Wei
Stroh, Albrecht
Luhmann, Heiko J.
Stüttgen, Maik C.
Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title_full Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title_fullStr Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title_full_unstemmed Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title_short Effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
title_sort effects of optogenetic inhibition of a small fraction of parvalbumin-positive interneurons on the representation of sensory stimuli in mouse barrel cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9653449/
https://www.ncbi.nlm.nih.gov/pubmed/36371511
http://dx.doi.org/10.1038/s41598-022-24156-y
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