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Translaminar recurrence from layer 5 suppresses superficial cortical layers

Information flow in the sensory cortex has been described as a predominantly feedforward sequence with deep layers as the output structure. Although recurrent excitatory projections from layer 5 (L5) to superficial L2/3 have been identified by anatomical and physiological studies, their functional i...

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Autores principales: Onodera, Koun, Kato, Hiroyuki K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095870/
https://www.ncbi.nlm.nih.gov/pubmed/35546553
http://dx.doi.org/10.1038/s41467-022-30349-w
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author Onodera, Koun
Kato, Hiroyuki K.
author_facet Onodera, Koun
Kato, Hiroyuki K.
author_sort Onodera, Koun
collection PubMed
description Information flow in the sensory cortex has been described as a predominantly feedforward sequence with deep layers as the output structure. Although recurrent excitatory projections from layer 5 (L5) to superficial L2/3 have been identified by anatomical and physiological studies, their functional impact on sensory processing remains unclear. Here, we use layer-selective optogenetic manipulations in the primary auditory cortex to demonstrate that feedback inputs from L5 suppress the activity of superficial layers regardless of the arousal level, contrary to the prediction from their excitatory connectivity. This suppressive effect is predominantly mediated by translaminar circuitry through intratelencephalic neurons, with an additional contribution of subcortical projections by pyramidal tract neurons. Furthermore, L5 activation sharpened tone-evoked responses of superficial layers in both frequency and time domains, indicating its impact on cortical spectro-temporal integration. Together, our findings establish a translaminar inhibitory recurrence from deep layers that sharpens feature selectivity in superficial cortical layers.
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spelling pubmed-90958702022-05-13 Translaminar recurrence from layer 5 suppresses superficial cortical layers Onodera, Koun Kato, Hiroyuki K. Nat Commun Article Information flow in the sensory cortex has been described as a predominantly feedforward sequence with deep layers as the output structure. Although recurrent excitatory projections from layer 5 (L5) to superficial L2/3 have been identified by anatomical and physiological studies, their functional impact on sensory processing remains unclear. Here, we use layer-selective optogenetic manipulations in the primary auditory cortex to demonstrate that feedback inputs from L5 suppress the activity of superficial layers regardless of the arousal level, contrary to the prediction from their excitatory connectivity. This suppressive effect is predominantly mediated by translaminar circuitry through intratelencephalic neurons, with an additional contribution of subcortical projections by pyramidal tract neurons. Furthermore, L5 activation sharpened tone-evoked responses of superficial layers in both frequency and time domains, indicating its impact on cortical spectro-temporal integration. Together, our findings establish a translaminar inhibitory recurrence from deep layers that sharpens feature selectivity in superficial cortical layers. Nature Publishing Group UK 2022-05-11 /pmc/articles/PMC9095870/ /pubmed/35546553 http://dx.doi.org/10.1038/s41467-022-30349-w 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 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Onodera, Koun
Kato, Hiroyuki K.
Translaminar recurrence from layer 5 suppresses superficial cortical layers
title Translaminar recurrence from layer 5 suppresses superficial cortical layers
title_full Translaminar recurrence from layer 5 suppresses superficial cortical layers
title_fullStr Translaminar recurrence from layer 5 suppresses superficial cortical layers
title_full_unstemmed Translaminar recurrence from layer 5 suppresses superficial cortical layers
title_short Translaminar recurrence from layer 5 suppresses superficial cortical layers
title_sort translaminar recurrence from layer 5 suppresses superficial cortical layers
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9095870/
https://www.ncbi.nlm.nih.gov/pubmed/35546553
http://dx.doi.org/10.1038/s41467-022-30349-w
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