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Comparative transcriptomics reveals human-specific cortical features

View ORCID ProfileNikolas L. Jorstad, View ORCID ProfileJanet H.T. Song, View ORCID ProfileDavid Exposito-Alonso, View ORCID ProfileHamsini Suresh, Nathan Castro, View ORCID ProfileFenna M. Krienen, View ORCID ProfileAnna Marie Yanny, View ORCID ProfileJennie Close, Emily Gelfand, View ORCID ProfileKyle J. Travaglini, View ORCID ProfileSoumyadeep Basu, View ORCID ProfileMarc Beaudin, View ORCID ProfileDarren Bertagnolli, View ORCID ProfileMegan Crow, View ORCID ProfileSong-Lin Ding, View ORCID ProfileJeroen Eggermont, View ORCID ProfileAlexandra Glandon, View ORCID ProfileJeff Goldy, View ORCID ProfileThomas Kroes, View ORCID ProfileBrian Long, View ORCID ProfileDelissa McMillen, View ORCID ProfileTrangthanh Pham, View ORCID ProfileChristine Rimorin, View ORCID ProfileKimberly Siletti, View ORCID ProfileSaroja Somasundaram, View ORCID ProfileMichael Tieu, View ORCID ProfileAmy Torkelson, View ORCID ProfileKatelyn Ward, View ORCID ProfileGuoping Feng, View ORCID ProfileWilliam D. Hopkins, View ORCID ProfileThomas Höllt, View ORCID ProfileC. Dirk Keene, View ORCID ProfileSten Linnarsson, View ORCID ProfileSteven A. McCarroll, View ORCID ProfileBoudewijn P. Lelieveldt, View ORCID ProfileChet C. Sherwood, View ORCID ProfileKimberly Smith, View ORCID ProfileChristopher A. Walsh, View ORCID ProfileAlexander Dobin, View ORCID ProfileJesse Gillis, View ORCID ProfileEd S. Lein, View ORCID ProfileRebecca D. Hodge, View ORCID ProfileTrygve E. Bakken
doi: https://doi.org/10.1101/2022.09.19.508480
Nikolas L. Jorstad
1Allen Institute for Brain Science; Seattle, WA, 98109
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Janet H.T. Song
2Division of Genetics and Genomics and HHMI, Boston Children’s Hospital, Harvard Medical School; Boston, MA
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David Exposito-Alonso
2Division of Genetics and Genomics and HHMI, Boston Children’s Hospital, Harvard Medical School; Boston, MA
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Hamsini Suresh
3Cold Spring Harbor Laboratory; Cold Spring Harbor, NY
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Nathan Castro
3Cold Spring Harbor Laboratory; Cold Spring Harbor, NY
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Fenna M. Krienen
4Department of Genetics, Harvard Medical School; 77 Avenue Louis Pasteur Boston MA 02115
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Anna Marie Yanny
1Allen Institute for Brain Science; Seattle, WA, 98109
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Jennie Close
1Allen Institute for Brain Science; Seattle, WA, 98109
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Emily Gelfand
1Allen Institute for Brain Science; Seattle, WA, 98109
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Kyle J. Travaglini
1Allen Institute for Brain Science; Seattle, WA, 98109
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Soumyadeep Basu
5LKEB, Dept of Radiology, Leiden University Medical Center; Leiden, The Netherlands
6Computer Graphics and Visualization Group, Delft University of Technology; Delft, The Netherlands
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Marc Beaudin
2Division of Genetics and Genomics and HHMI, Boston Children’s Hospital, Harvard Medical School; Boston, MA
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Darren Bertagnolli
1Allen Institute for Brain Science; Seattle, WA, 98109
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Megan Crow
3Cold Spring Harbor Laboratory; Cold Spring Harbor, NY
7Stanley Institute for Cognitive Genomics, Cold Spring Harbor Laboratory; Cold Spring Harbor, NY
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Song-Lin Ding
1Allen Institute for Brain Science; Seattle, WA, 98109
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Jeroen Eggermont
5LKEB, Dept of Radiology, Leiden University Medical Center; Leiden, The Netherlands
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Alexandra Glandon
1Allen Institute for Brain Science; Seattle, WA, 98109
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Jeff Goldy
1Allen Institute for Brain Science; Seattle, WA, 98109
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Thomas Kroes
5LKEB, Dept of Radiology, Leiden University Medical Center; Leiden, The Netherlands
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Brian Long
1Allen Institute for Brain Science; Seattle, WA, 98109
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Delissa McMillen
1Allen Institute for Brain Science; Seattle, WA, 98109
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Trangthanh Pham
1Allen Institute for Brain Science; Seattle, WA, 98109
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Christine Rimorin
1Allen Institute for Brain Science; Seattle, WA, 98109
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  • ORCID record for Christine Rimorin
Kimberly Siletti
8Department of Medical Biochemistry and Biophysics, Karolinska Institutet; Stockholm, Sweden
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Saroja Somasundaram
1Allen Institute for Brain Science; Seattle, WA, 98109
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Michael Tieu
1Allen Institute for Brain Science; Seattle, WA, 98109
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Amy Torkelson
1Allen Institute for Brain Science; Seattle, WA, 98109
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Katelyn Ward
1Allen Institute for Brain Science; Seattle, WA, 98109
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Guoping Feng
9McGovern Institute for Brain Research, Massachusetts Institute of Technology; Cambridge, Massachusetts 02139
10Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology; Cambridge, Massachusetts 02139
11Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard; Cambridge, Massachusetts 02142
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William D. Hopkins
12Keeling Center for Comparative Medicine and Research, University of Texas, MD Anderson Cancer Center; Houston, TX
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Thomas Höllt
6Computer Graphics and Visualization Group, Delft University of Technology; Delft, The Netherlands
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C. Dirk Keene
13Department of Laboratory Medicine and Pathology, University of Washington; Seattle, WA, USA
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Sten Linnarsson
8Department of Medical Biochemistry and Biophysics, Karolinska Institutet; Stockholm, Sweden
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Steven A. McCarroll
4Department of Genetics, Harvard Medical School; 77 Avenue Louis Pasteur Boston MA 02115
14Broad Institute of MIT and Harvard; Cambridge, MA 02142
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Boudewijn P. Lelieveldt
5LKEB, Dept of Radiology, Leiden University Medical Center; Leiden, The Netherlands
15Pattern Recognition and Bioinformatics group, Delft University of Technology; Delft, The Netherlands
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Chet C. Sherwood
16Department of Anthropology, The George Washington University; Washington, DC
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Kimberly Smith
1Allen Institute for Brain Science; Seattle, WA, 98109
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Christopher A. Walsh
2Division of Genetics and Genomics and HHMI, Boston Children’s Hospital, Harvard Medical School; Boston, MA
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Alexander Dobin
3Cold Spring Harbor Laboratory; Cold Spring Harbor, NY
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Jesse Gillis
17Department of Physiology, University of Toronto; Toronto, Canada
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Ed S. Lein
1Allen Institute for Brain Science; Seattle, WA, 98109
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Rebecca D. Hodge
1Allen Institute for Brain Science; Seattle, WA, 98109
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  • For correspondence: trygveb@alleninstitute.org rebeccah@alleninstitute.org
Trygve E. Bakken
1Allen Institute for Brain Science; Seattle, WA, 98109
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  • For correspondence: trygveb@alleninstitute.org rebeccah@alleninstitute.org
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Abstract

Humans have unique cognitive abilities among primates, including language, but their molecular, cellular, and circuit substrates are poorly understood. We used comparative single nucleus transcriptomics in adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets from the middle temporal gyrus (MTG) to understand human-specific features of cellular and molecular organization. Human, chimpanzee, and gorilla MTG showed highly similar cell type composition and laminar organization, and a large shift in proportions of deep layer intratelencephalic-projecting neurons compared to macaque and marmoset. Species differences in gene expression generally mirrored evolutionary distance and were seen in all cell types, although chimpanzees were more similar to gorillas than humans, consistent with faster divergence along the human lineage. Microglia, astrocytes, and oligodendrocytes showed accelerated gene expression changes compared to neurons or oligodendrocyte precursor cells, indicating either relaxed evolutionary constraints or positive selection in these cell types. Only a few hundred genes showed human-specific patterning in all or specific cell types, and were significantly enriched near human accelerated regions (HARs) and conserved deletions (hCONDELS) and in cell adhesion and intercellular signaling pathways. These results suggest that relatively few cellular and molecular changes uniquely define adult human cortical structure, particularly by affecting circuit connectivity and glial cell function.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Comparative transcriptomics reveals human-specific cortical features
Nikolas L. Jorstad, Janet H.T. Song, David Exposito-Alonso, Hamsini Suresh, Nathan Castro, Fenna M. Krienen, Anna Marie Yanny, Jennie Close, Emily Gelfand, Kyle J. Travaglini, Soumyadeep Basu, Marc Beaudin, Darren Bertagnolli, Megan Crow, Song-Lin Ding, Jeroen Eggermont, Alexandra Glandon, Jeff Goldy, Thomas Kroes, Brian Long, Delissa McMillen, Trangthanh Pham, Christine Rimorin, Kimberly Siletti, Saroja Somasundaram, Michael Tieu, Amy Torkelson, Katelyn Ward, Guoping Feng, William D. Hopkins, Thomas Höllt, C. Dirk Keene, Sten Linnarsson, Steven A. McCarroll, Boudewijn P. Lelieveldt, Chet C. Sherwood, Kimberly Smith, Christopher A. Walsh, Alexander Dobin, Jesse Gillis, Ed S. Lein, Rebecca D. Hodge, Trygve E. Bakken
bioRxiv 2022.09.19.508480; doi: https://doi.org/10.1101/2022.09.19.508480
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Comparative transcriptomics reveals human-specific cortical features
Nikolas L. Jorstad, Janet H.T. Song, David Exposito-Alonso, Hamsini Suresh, Nathan Castro, Fenna M. Krienen, Anna Marie Yanny, Jennie Close, Emily Gelfand, Kyle J. Travaglini, Soumyadeep Basu, Marc Beaudin, Darren Bertagnolli, Megan Crow, Song-Lin Ding, Jeroen Eggermont, Alexandra Glandon, Jeff Goldy, Thomas Kroes, Brian Long, Delissa McMillen, Trangthanh Pham, Christine Rimorin, Kimberly Siletti, Saroja Somasundaram, Michael Tieu, Amy Torkelson, Katelyn Ward, Guoping Feng, William D. Hopkins, Thomas Höllt, C. Dirk Keene, Sten Linnarsson, Steven A. McCarroll, Boudewijn P. Lelieveldt, Chet C. Sherwood, Kimberly Smith, Christopher A. Walsh, Alexander Dobin, Jesse Gillis, Ed S. Lein, Rebecca D. Hodge, Trygve E. Bakken
bioRxiv 2022.09.19.508480; doi: https://doi.org/10.1101/2022.09.19.508480

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