Transcriptomic cytoarchitecture reveals principles of human neocortex organization

Nikolas L. Jorstad; Jennie Close; Nelson Johansen; Anna Marie Yanny; Eliza R. Barkan; Kyle J. Travaglini; Darren Bertagnolli; Jazmin Campos; Tamara Casper; Kirsten Crichton; Nick Dee; Song Lin Ding; Emily Gelfand; Jeff Goldy; Daniel Hirschstein; Katelyn Kiick; Matthew Kroll; Michael Kunst; Kanan Lathia; Brian Long; Naomi Martin; Delissa McMillen; Trangthanh Pham; Christine Rimorin; Augustin Ruiz; Nadiya Shapovalova; Soraya Shehata; Kimberly Siletti; Saroja Somasundaram; Josef Sulc; Michael Tieu; Amy Torkelson; Herman Tung; Edward M. Callaway; Patrick R. Hof; C. Dirk Keene; Boaz P. Levi; Sten Linnarsson; Partha P. Mitra; Kimberly Smith; Rebecca D. Hodge; Trygve E. Bakken; Ed S. Lein

doi:10.1126/SCIENCE.ADF6812

Transcriptomic cytoarchitecture reveals principles of human neocortex organization

Nikolas L. Jorstad, Jennie Close, Nelson Johansen, Anna Marie Yanny, Eliza R. Barkan, Kyle J. Travaglini, Darren Bertagnolli, Jazmin Campos, Tamara Casper, Kirsten Crichton, Nick Dee, Song Lin Ding, Emily Gelfand, Jeff Goldy, Daniel Hirschstein, Katelyn Kiick, Matthew Kroll, Michael Kunst, Kanan Lathia, Brian LongNaomi Martin, Delissa McMillen, Trangthanh Pham, Christine Rimorin, Augustin Ruiz, Nadiya Shapovalova, Soraya Shehata, Kimberly Siletti, Saroja Somasundaram, Josef Sulc, Michael Tieu, Amy Torkelson, Herman Tung, Edward M. Callaway, Patrick R. Hof, C. Dirk Keene, Boaz P. Levi, Sten Linnarsson, Partha P. Mitra, Kimberly Smith, Rebecca D. Hodge, Trygve E. Bakken, Ed S. Lein

Research output: Contribution to journal › Article › peer-review

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Abstract

Variation in cytoarchitecture is the basis for the histological definition of cortical areas. We used single cell transcriptomics and performed cellular characterization of the human cortex to better understand cortical areal specialization. Single-nucleus RNA-sequencing of 8 areas spanning cortical structural variation showed a highly consistent cellular makeup for 24 cell subclasses. However, proportions of excitatory neuron subclasses varied substantially, likely reflecting differences in connectivity across primary sensorimotor and association cortices. Laminar organization of astrocytes and oligodendrocytes also differed across areas. Primary visual cortex showed characteristic organization with major changes in the excitatory to inhibitory neuron ratio, expansion of layer 4 excitatory neurons, and specialized inhibitory neurons. These results lay the groundwork for a refined cellular and molecular characterization of human cortical cytoarchitecture and areal specialization.

Original language	English
Article number	eadf6812
Journal	Science
Volume	382
Issue number	6667
DOIs	https://doi.org/10.1126/SCIENCE.ADF6812
State	Published - 13 Oct 2023

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Jorstad, N. L., Close, J., Johansen, N., Yanny, A. M., Barkan, E. R., Travaglini, K. J., Bertagnolli, D., Campos, J., Casper, T., Crichton, K., Dee, N., Ding, S. L., Gelfand, E., Goldy, J., Hirschstein, D., Kiick, K., Kroll, M., Kunst, M., Lathia, K., ... Lein, E. S. (2023). Transcriptomic cytoarchitecture reveals principles of human neocortex organization. Science, 382(6667), Article eadf6812. https://doi.org/10.1126/SCIENCE.ADF6812

@article{fc938a6aa1a24447bd728e06f77b1d12,

title = "Transcriptomic cytoarchitecture reveals principles of human neocortex organization",

abstract = "Variation in cytoarchitecture is the basis for the histological definition of cortical areas. We used single cell transcriptomics and performed cellular characterization of the human cortex to better understand cortical areal specialization. Single-nucleus RNA-sequencing of 8 areas spanning cortical structural variation showed a highly consistent cellular makeup for 24 cell subclasses. However, proportions of excitatory neuron subclasses varied substantially, likely reflecting differences in connectivity across primary sensorimotor and association cortices. Laminar organization of astrocytes and oligodendrocytes also differed across areas. Primary visual cortex showed characteristic organization with major changes in the excitatory to inhibitory neuron ratio, expansion of layer 4 excitatory neurons, and specialized inhibitory neurons. These results lay the groundwork for a refined cellular and molecular characterization of human cortical cytoarchitecture and areal specialization.",

author = "Jorstad, {Nikolas L.} and Jennie Close and Nelson Johansen and Yanny, {Anna Marie} and Barkan, {Eliza R.} and Travaglini, {Kyle J.} and Darren Bertagnolli and Jazmin Campos and Tamara Casper and Kirsten Crichton and Nick Dee and Ding, {Song Lin} and Emily Gelfand and Jeff Goldy and Daniel Hirschstein and Katelyn Kiick and Matthew Kroll and Michael Kunst and Kanan Lathia and Brian Long and Naomi Martin and Delissa McMillen and Trangthanh Pham and Christine Rimorin and Augustin Ruiz and Nadiya Shapovalova and Soraya Shehata and Kimberly Siletti and Saroja Somasundaram and Josef Sulc and Michael Tieu and Amy Torkelson and Herman Tung and Callaway, {Edward M.} and Hof, {Patrick R.} and Keene, {C. Dirk} and Levi, {Boaz P.} and Sten Linnarsson and Mitra, {Partha P.} and Kimberly Smith and Hodge, {Rebecca D.} and Bakken, {Trygve E.} and Lein, {Ed S.}",

year = "2023",

month = oct,

day = "13",

doi = "10.1126/SCIENCE.ADF6812",

language = "English",

volume = "382",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

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Jorstad, NL, Close, J, Johansen, N, Yanny, AM, Barkan, ER, Travaglini, KJ, Bertagnolli, D, Campos, J, Casper, T, Crichton, K, Dee, N, Ding, SL, Gelfand, E, Goldy, J, Hirschstein, D, Kiick, K, Kroll, M, Kunst, M, Lathia, K, Long, B, Martin, N, McMillen, D, Pham, T, Rimorin, C, Ruiz, A, Shapovalova, N, Shehata, S, Siletti, K, Somasundaram, S, Sulc, J, Tieu, M, Torkelson, A, Tung, H, Callaway, EM, Hof, PR, Keene, CD, Levi, BP, Linnarsson, S, Mitra, PP, Smith, K, Hodge, RD, Bakken, TE & Lein, ES 2023, 'Transcriptomic cytoarchitecture reveals principles of human neocortex organization', Science, vol. 382, no. 6667, eadf6812. https://doi.org/10.1126/SCIENCE.ADF6812

TY - JOUR

T1 - Transcriptomic cytoarchitecture reveals principles of human neocortex organization

AU - Jorstad, Nikolas L.

AU - Close, Jennie

AU - Johansen, Nelson

AU - Yanny, Anna Marie

AU - Barkan, Eliza R.

AU - Travaglini, Kyle J.

AU - Bertagnolli, Darren

AU - Campos, Jazmin

AU - Casper, Tamara

AU - Crichton, Kirsten

AU - Dee, Nick

AU - Ding, Song Lin

AU - Gelfand, Emily

AU - Goldy, Jeff

AU - Hirschstein, Daniel

AU - Kiick, Katelyn

AU - Kroll, Matthew

AU - Kunst, Michael

AU - Lathia, Kanan

AU - Long, Brian

AU - Martin, Naomi

AU - McMillen, Delissa

AU - Pham, Trangthanh

AU - Rimorin, Christine

AU - Ruiz, Augustin

AU - Shapovalova, Nadiya

AU - Shehata, Soraya

AU - Siletti, Kimberly

AU - Somasundaram, Saroja

AU - Sulc, Josef

AU - Tieu, Michael

AU - Torkelson, Amy

AU - Tung, Herman

AU - Callaway, Edward M.

AU - Hof, Patrick R.

AU - Keene, C. Dirk

AU - Levi, Boaz P.

AU - Linnarsson, Sten

AU - Mitra, Partha P.

AU - Smith, Kimberly

AU - Hodge, Rebecca D.

AU - Bakken, Trygve E.

AU - Lein, Ed S.

PY - 2023/10/13

Y1 - 2023/10/13

N2 - Variation in cytoarchitecture is the basis for the histological definition of cortical areas. We used single cell transcriptomics and performed cellular characterization of the human cortex to better understand cortical areal specialization. Single-nucleus RNA-sequencing of 8 areas spanning cortical structural variation showed a highly consistent cellular makeup for 24 cell subclasses. However, proportions of excitatory neuron subclasses varied substantially, likely reflecting differences in connectivity across primary sensorimotor and association cortices. Laminar organization of astrocytes and oligodendrocytes also differed across areas. Primary visual cortex showed characteristic organization with major changes in the excitatory to inhibitory neuron ratio, expansion of layer 4 excitatory neurons, and specialized inhibitory neurons. These results lay the groundwork for a refined cellular and molecular characterization of human cortical cytoarchitecture and areal specialization.

AB - Variation in cytoarchitecture is the basis for the histological definition of cortical areas. We used single cell transcriptomics and performed cellular characterization of the human cortex to better understand cortical areal specialization. Single-nucleus RNA-sequencing of 8 areas spanning cortical structural variation showed a highly consistent cellular makeup for 24 cell subclasses. However, proportions of excitatory neuron subclasses varied substantially, likely reflecting differences in connectivity across primary sensorimotor and association cortices. Laminar organization of astrocytes and oligodendrocytes also differed across areas. Primary visual cortex showed characteristic organization with major changes in the excitatory to inhibitory neuron ratio, expansion of layer 4 excitatory neurons, and specialized inhibitory neurons. These results lay the groundwork for a refined cellular and molecular characterization of human cortical cytoarchitecture and areal specialization.

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U2 - 10.1126/SCIENCE.ADF6812

DO - 10.1126/SCIENCE.ADF6812

M3 - Article

C2 - 37824655

AN - SCOPUS:85175584886

SN - 0036-8075

VL - 382

JO - Science

JF - Science

IS - 6667

M1 - eadf6812

ER -

Transcriptomic cytoarchitecture reveals principles of human neocortex organization

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