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Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans

Abundant evidence supports the presence of at least three distinct types of thalamocortical (TC) neurons in the primate dorsal lateral geniculate nucleus (dLGN) of the thalamus, the brain region that conveys visual information from the retina to the primary visual cortex (V1). Different types of TC...

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Autores principales: Bakken, Trygve E, van Velthoven, Cindy TJ, Menon, Vilas, Hodge, Rebecca D, Yao, Zizhen, Nguyen, Thuc Nghi, Graybuck, Lucas T, Horwitz, Gregory D, Bertagnolli, Darren, Goldy, Jeff, Yanny, Anna Marie, Garren, Emma, Parry, Sheana, Casper, Tamara, Shehata, Soraya I, Barkan, Eliza R, Szafer, Aaron, Levi, Boaz P, Dee, Nick, Smith, Kimberly A, Sunkin, Susan M, Bernard, Amy, Phillips, John, Hawrylycz, Michael J, Koch, Christof, Murphy, Gabe J, Lein, Ed, Zeng, Hongkui, Tasic, Bosiljka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8412930/
https://www.ncbi.nlm.nih.gov/pubmed/34473054
http://dx.doi.org/10.7554/eLife.64875
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author Bakken, Trygve E
van Velthoven, Cindy TJ
Menon, Vilas
Hodge, Rebecca D
Yao, Zizhen
Nguyen, Thuc Nghi
Graybuck, Lucas T
Horwitz, Gregory D
Bertagnolli, Darren
Goldy, Jeff
Yanny, Anna Marie
Garren, Emma
Parry, Sheana
Casper, Tamara
Shehata, Soraya I
Barkan, Eliza R
Szafer, Aaron
Levi, Boaz P
Dee, Nick
Smith, Kimberly A
Sunkin, Susan M
Bernard, Amy
Phillips, John
Hawrylycz, Michael J
Koch, Christof
Murphy, Gabe J
Lein, Ed
Zeng, Hongkui
Tasic, Bosiljka
author_facet Bakken, Trygve E
van Velthoven, Cindy TJ
Menon, Vilas
Hodge, Rebecca D
Yao, Zizhen
Nguyen, Thuc Nghi
Graybuck, Lucas T
Horwitz, Gregory D
Bertagnolli, Darren
Goldy, Jeff
Yanny, Anna Marie
Garren, Emma
Parry, Sheana
Casper, Tamara
Shehata, Soraya I
Barkan, Eliza R
Szafer, Aaron
Levi, Boaz P
Dee, Nick
Smith, Kimberly A
Sunkin, Susan M
Bernard, Amy
Phillips, John
Hawrylycz, Michael J
Koch, Christof
Murphy, Gabe J
Lein, Ed
Zeng, Hongkui
Tasic, Bosiljka
author_sort Bakken, Trygve E
collection PubMed
description Abundant evidence supports the presence of at least three distinct types of thalamocortical (TC) neurons in the primate dorsal lateral geniculate nucleus (dLGN) of the thalamus, the brain region that conveys visual information from the retina to the primary visual cortex (V1). Different types of TC neurons in mice, humans, and macaques have distinct morphologies, distinct connectivity patterns, and convey different aspects of visual information to the cortex. To investigate the molecular underpinnings of these cell types, and how these relate to differences in dLGN between human, macaque, and mice, we profiled gene expression in single nuclei and cells using RNA-sequencing. These efforts identified four distinct types of TC neurons in the primate dLGN: magnocellular (M) neurons, parvocellular (P) neurons, and two types of koniocellular (K) neurons. Despite extensively documented morphological and physiological differences between M and P neurons, we identified few genes with significant differential expression between transcriptomic cell types corresponding to these two neuronal populations. Likewise, the dominant feature of TC neurons of the adult mouse dLGN is high transcriptomic similarity, with an axis of heterogeneity that aligns with core vs. shell portions of mouse dLGN. Together, these data show that transcriptomic differences between principal cell types in the mature mammalian dLGN are subtle relative to the observed differences in morphology and cortical projection targets. Finally, alignment of transcriptome profiles across species highlights expanded diversity of GABAergic neurons in primate versus mouse dLGN and homologous types of TC neurons in primates that are distinct from TC neurons in mouse.
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spelling pubmed-84129302021-09-03 Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans Bakken, Trygve E van Velthoven, Cindy TJ Menon, Vilas Hodge, Rebecca D Yao, Zizhen Nguyen, Thuc Nghi Graybuck, Lucas T Horwitz, Gregory D Bertagnolli, Darren Goldy, Jeff Yanny, Anna Marie Garren, Emma Parry, Sheana Casper, Tamara Shehata, Soraya I Barkan, Eliza R Szafer, Aaron Levi, Boaz P Dee, Nick Smith, Kimberly A Sunkin, Susan M Bernard, Amy Phillips, John Hawrylycz, Michael J Koch, Christof Murphy, Gabe J Lein, Ed Zeng, Hongkui Tasic, Bosiljka eLife Neuroscience Abundant evidence supports the presence of at least three distinct types of thalamocortical (TC) neurons in the primate dorsal lateral geniculate nucleus (dLGN) of the thalamus, the brain region that conveys visual information from the retina to the primary visual cortex (V1). Different types of TC neurons in mice, humans, and macaques have distinct morphologies, distinct connectivity patterns, and convey different aspects of visual information to the cortex. To investigate the molecular underpinnings of these cell types, and how these relate to differences in dLGN between human, macaque, and mice, we profiled gene expression in single nuclei and cells using RNA-sequencing. These efforts identified four distinct types of TC neurons in the primate dLGN: magnocellular (M) neurons, parvocellular (P) neurons, and two types of koniocellular (K) neurons. Despite extensively documented morphological and physiological differences between M and P neurons, we identified few genes with significant differential expression between transcriptomic cell types corresponding to these two neuronal populations. Likewise, the dominant feature of TC neurons of the adult mouse dLGN is high transcriptomic similarity, with an axis of heterogeneity that aligns with core vs. shell portions of mouse dLGN. Together, these data show that transcriptomic differences between principal cell types in the mature mammalian dLGN are subtle relative to the observed differences in morphology and cortical projection targets. Finally, alignment of transcriptome profiles across species highlights expanded diversity of GABAergic neurons in primate versus mouse dLGN and homologous types of TC neurons in primates that are distinct from TC neurons in mouse. eLife Sciences Publications, Ltd 2021-09-02 /pmc/articles/PMC8412930/ /pubmed/34473054 http://dx.doi.org/10.7554/eLife.64875 Text en © 2021, Bakken et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Bakken, Trygve E
van Velthoven, Cindy TJ
Menon, Vilas
Hodge, Rebecca D
Yao, Zizhen
Nguyen, Thuc Nghi
Graybuck, Lucas T
Horwitz, Gregory D
Bertagnolli, Darren
Goldy, Jeff
Yanny, Anna Marie
Garren, Emma
Parry, Sheana
Casper, Tamara
Shehata, Soraya I
Barkan, Eliza R
Szafer, Aaron
Levi, Boaz P
Dee, Nick
Smith, Kimberly A
Sunkin, Susan M
Bernard, Amy
Phillips, John
Hawrylycz, Michael J
Koch, Christof
Murphy, Gabe J
Lein, Ed
Zeng, Hongkui
Tasic, Bosiljka
Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title_full Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title_fullStr Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title_full_unstemmed Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title_short Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans
title_sort single-cell and single-nucleus rna-seq uncovers shared and distinct axes of variation in dorsal lgn neurons in mice, non-human primates, and humans
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8412930/
https://www.ncbi.nlm.nih.gov/pubmed/34473054
http://dx.doi.org/10.7554/eLife.64875
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