Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex

Abstract Excitatory spiny stellate neurons are prominently featured in the cortical circuits of sensory modalities that provide high salience and high acuity representations of the environment. These specialized neurons are considered developmentally linked to bottom-up inputs from the thalamus, how...

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Main Authors: Timothy R. Young, Mariko Yamamoto, Satomi S. Kikuchi, Aya C. Yoshida, Takaya Abe, Kenichi Inoue, Joshua P. Johansen, Andrea Benucci, Yumiko Yoshimura, Tomomi Shimogori
Format: Article
Language:English
Published: Nature Portfolio 2023-09-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-41749-x
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author Timothy R. Young
Mariko Yamamoto
Satomi S. Kikuchi
Aya C. Yoshida
Takaya Abe
Kenichi Inoue
Joshua P. Johansen
Andrea Benucci
Yumiko Yoshimura
Tomomi Shimogori
author_facet Timothy R. Young
Mariko Yamamoto
Satomi S. Kikuchi
Aya C. Yoshida
Takaya Abe
Kenichi Inoue
Joshua P. Johansen
Andrea Benucci
Yumiko Yoshimura
Tomomi Shimogori
author_sort Timothy R. Young
collection DOAJ
description Abstract Excitatory spiny stellate neurons are prominently featured in the cortical circuits of sensory modalities that provide high salience and high acuity representations of the environment. These specialized neurons are considered developmentally linked to bottom-up inputs from the thalamus, however, the molecular mechanisms underlying their diversification and function are unknown. Here, we investigated this in mouse somatosensory cortex, where spiny stellate neurons and pyramidal neurons have distinct roles in processing whisker-evoked signals. Utilizing spatial transcriptomics, we identified reciprocal patterns of gene expression which correlated with these cell-types and were linked to innervation by specific thalamic inputs during development. Genetic manipulation that prevents the acquisition of spiny stellate fate highlighted an important role for these neurons in processing distinct whisker signals within functional cortical columns, and as a key driver in the formation of specific whisker-related circuits in the cortex.
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spelling doaj.art-e954fb4d89854a3b8c603ad41e9f578d2023-11-20T10:03:38ZengNature PortfolioNature Communications2041-17232023-09-0114112010.1038/s41467-023-41749-xThalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortexTimothy R. Young0Mariko Yamamoto1Satomi S. Kikuchi2Aya C. Yoshida3Takaya Abe4Kenichi Inoue5Joshua P. Johansen6Andrea Benucci7Yumiko Yoshimura8Tomomi Shimogori9Laboratory for Molecular Mechanisms of Brain Development, RIKEN Center for Brain ScienceDivision of Visual Information Processing, National Institute for Physiological Sciences, National Institutes of Natural SciencesLaboratory for Molecular Mechanisms of Brain Development, RIKEN Center for Brain ScienceLaboratory for Molecular Mechanisms of Brain Development, RIKEN Center for Brain ScienceLaboratory for Animal Resources and Genetic Engineering, RIKEN Center for Biosystems Dynamics ResearchLaboratory for Animal Resources and Genetic Engineering, RIKEN Center for Biosystems Dynamics ResearchLaboratory for Neural Circuitry of Learning and Memory, RIKEN Center for Brain ScienceLaboratory for Neural Circuits and Behavior, RIKEN Center for Brain ScienceDivision of Visual Information Processing, National Institute for Physiological Sciences, National Institutes of Natural SciencesLaboratory for Molecular Mechanisms of Brain Development, RIKEN Center for Brain ScienceAbstract Excitatory spiny stellate neurons are prominently featured in the cortical circuits of sensory modalities that provide high salience and high acuity representations of the environment. These specialized neurons are considered developmentally linked to bottom-up inputs from the thalamus, however, the molecular mechanisms underlying their diversification and function are unknown. Here, we investigated this in mouse somatosensory cortex, where spiny stellate neurons and pyramidal neurons have distinct roles in processing whisker-evoked signals. Utilizing spatial transcriptomics, we identified reciprocal patterns of gene expression which correlated with these cell-types and were linked to innervation by specific thalamic inputs during development. Genetic manipulation that prevents the acquisition of spiny stellate fate highlighted an important role for these neurons in processing distinct whisker signals within functional cortical columns, and as a key driver in the formation of specific whisker-related circuits in the cortex.https://doi.org/10.1038/s41467-023-41749-x
spellingShingle Timothy R. Young
Mariko Yamamoto
Satomi S. Kikuchi
Aya C. Yoshida
Takaya Abe
Kenichi Inoue
Joshua P. Johansen
Andrea Benucci
Yumiko Yoshimura
Tomomi Shimogori
Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
Nature Communications
title Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
title_full Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
title_fullStr Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
title_full_unstemmed Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
title_short Thalamocortical control of cell-type specificity drives circuits for processing whisker-related information in mouse barrel cortex
title_sort thalamocortical control of cell type specificity drives circuits for processing whisker related information in mouse barrel cortex
url https://doi.org/10.1038/s41467-023-41749-x
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