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Layer 5 of cortex innervates the thalamic reticular nucleus in mice

Neurons in the thalamic reticular nucleus (TRN) are a primary source of inhibition to the dorsal thalamus and, as they are innervated in part by the cortex, are a means of corticothalamic regulation. Previously, cortical inputs to the TRN were thought to originate solely from layer 6 (L6), but we re...

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Autores principales: Carroll, Briana J., Sampathkumar, Vandana, Kasthuri, Narayanan, Sherman, S. Murray
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499584/
https://www.ncbi.nlm.nih.gov/pubmed/36095204
http://dx.doi.org/10.1073/pnas.2205209119
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author Carroll, Briana J.
Sampathkumar, Vandana
Kasthuri, Narayanan
Sherman, S. Murray
author_facet Carroll, Briana J.
Sampathkumar, Vandana
Kasthuri, Narayanan
Sherman, S. Murray
author_sort Carroll, Briana J.
collection PubMed
description Neurons in the thalamic reticular nucleus (TRN) are a primary source of inhibition to the dorsal thalamus and, as they are innervated in part by the cortex, are a means of corticothalamic regulation. Previously, cortical inputs to the TRN were thought to originate solely from layer 6 (L6), but we recently reported the presence of putative synaptic terminals from layer 5 (L5) neurons in multiple cortical areas in the TRN [J. A. Prasad, B. J. Carroll, S. M. Sherman, J. Neurosci. 40, 5785–5796 (2020)]. Here, we demonstrate with electron microscopy that L5 terminals from multiple cortical regions make bona fide synapses in the TRN. We further use light microscopy to localize these synapses relative to recently described TRN subdivisions and show that L5 terminals target the edges of the somatosensory TRN, where neurons reciprocally connect to higher-order thalamus, and that L5 terminals are scarce in the core of the TRN, where neurons reciprocally connect to first-order thalamus. In contrast, L6 terminals densely innervate both edge and core subregions and are smaller than those from L5. These data suggest that a sparse but potent input from L5 neurons of multiple cortical regions to the TRN may yield transreticular inhibition targeted to higher-order thalamus.
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spelling pubmed-94995842023-03-12 Layer 5 of cortex innervates the thalamic reticular nucleus in mice Carroll, Briana J. Sampathkumar, Vandana Kasthuri, Narayanan Sherman, S. Murray Proc Natl Acad Sci U S A Biological Sciences Neurons in the thalamic reticular nucleus (TRN) are a primary source of inhibition to the dorsal thalamus and, as they are innervated in part by the cortex, are a means of corticothalamic regulation. Previously, cortical inputs to the TRN were thought to originate solely from layer 6 (L6), but we recently reported the presence of putative synaptic terminals from layer 5 (L5) neurons in multiple cortical areas in the TRN [J. A. Prasad, B. J. Carroll, S. M. Sherman, J. Neurosci. 40, 5785–5796 (2020)]. Here, we demonstrate with electron microscopy that L5 terminals from multiple cortical regions make bona fide synapses in the TRN. We further use light microscopy to localize these synapses relative to recently described TRN subdivisions and show that L5 terminals target the edges of the somatosensory TRN, where neurons reciprocally connect to higher-order thalamus, and that L5 terminals are scarce in the core of the TRN, where neurons reciprocally connect to first-order thalamus. In contrast, L6 terminals densely innervate both edge and core subregions and are smaller than those from L5. These data suggest that a sparse but potent input from L5 neurons of multiple cortical regions to the TRN may yield transreticular inhibition targeted to higher-order thalamus. National Academy of Sciences 2022-09-12 2022-09-20 /pmc/articles/PMC9499584/ /pubmed/36095204 http://dx.doi.org/10.1073/pnas.2205209119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Carroll, Briana J.
Sampathkumar, Vandana
Kasthuri, Narayanan
Sherman, S. Murray
Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title_full Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title_fullStr Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title_full_unstemmed Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title_short Layer 5 of cortex innervates the thalamic reticular nucleus in mice
title_sort layer 5 of cortex innervates the thalamic reticular nucleus in mice
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499584/
https://www.ncbi.nlm.nih.gov/pubmed/36095204
http://dx.doi.org/10.1073/pnas.2205209119
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