Comparative transcriptomics reveals human-specific cortical features

Nikolas L Jorstad; Janet H T Song; David Exposito-Alonso; Hamsini Suresh; Nathan Castro-Pacheco; Fenna M Krienen; Anna Marie Yanny; Jennie Close; Emily Gelfand; Brian Long; Stephanie C Seeman; Kyle J Travaglini; Soumyadeep Basu; Marc Beaudin; Darren Bertagnolli; Megan Crow; Song-Lin Ding; Jeroen Eggermont; Alexandra Glandon; Jeff Goldy; Katelyn Kiick; Thomas Kroes; Delissa McMillen; Trangthanh Pham; Christine Rimorin; Kimberly Siletti; Saroja Somasundaram; Michael Tieu; Amy Torkelson; 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

doi:10.1126/science.ade9516

Comparative transcriptomics reveals human-specific cortical features

Nikolas L Jorstad
, Janet H T Song
, David Exposito-Alonso
, Hamsini Suresh
, Nathan Castro-Pacheco
, Fenna M Krienen
, Anna Marie Yanny
, Jennie Close
, Emily Gelfand
, Brian Long
, Stephanie C Seeman
, Kyle J Travaglini
, Soumyadeep Basu
, Marc Beaudin
, Darren Bertagnolli
, Megan Crow
, Song-Lin Ding
, Jeroen Eggermont
, Alexandra Glandon
, Jeff Goldy

Katelyn Kiick, Thomas Kroes, Delissa McMillen, Trangthanh Pham, Christine Rimorin, Kimberly Siletti, Saroja Somasundaram, Michael Tieu, Amy Torkelson, 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

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

Abstract

The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.

Original language	English
Article number	eade9516
Journal	Science (New York, N.Y.)
Volume	382
Issue number	6667
DOIs	https://doi.org/10.1126/science.ade9516
Publication status	Published - 13 Oct 2023
Externally published	Yes

Keywords

Animals
Cognition
Gene Expression Profiling
Gorilla gorilla/genetics
Hominidae/genetics
Humans
Macaca mulatta/genetics
Neocortex/physiology
Pan troglodytes/genetics
Phylogeny
Species Specificity
Temporal Lobe/physiology
Transcriptome

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10.1126/science.ade9516

Cite this

Jorstad, N. L., Song, J. H. T., Exposito-Alonso, D., Suresh, H., Castro-Pacheco, N., Krienen, F. M., Yanny, A. M., Close, J., Gelfand, E., Long, B., Seeman, S. C., Travaglini, K. J., Basu, S., Beaudin, M., Bertagnolli, D., Crow, M., Ding, S.-L., Eggermont, J., Glandon, A., ... Bakken, T. E. (2023). Comparative transcriptomics reveals human-specific cortical features. Science (New York, N.Y.), 382(6667), Article eade9516. https://doi.org/10.1126/science.ade9516

@article{aa034df079aa4f91b3968cd7d2b42fba,

title = "Comparative transcriptomics reveals human-specific cortical features",

abstract = "The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.",

keywords = "Animals, Cognition, Gene Expression Profiling, Gorilla gorilla/genetics, Hominidae/genetics, Humans, Macaca mulatta/genetics, Neocortex/physiology, Pan troglodytes/genetics, Phylogeny, Species Specificity, Temporal Lobe/physiology, Transcriptome",

author = "Jorstad, \{Nikolas L\} and Song, \{Janet H T\} and David Exposito-Alonso and Hamsini Suresh and Nathan Castro-Pacheco and Krienen, \{Fenna M\} and Yanny, \{Anna Marie\} and Jennie Close and Emily Gelfand and Brian Long and Seeman, \{Stephanie C\} and Travaglini, \{Kyle J\} and Soumyadeep Basu and Marc Beaudin and Darren Bertagnolli and Megan Crow and Song-Lin Ding and Jeroen Eggermont and Alexandra Glandon and Jeff Goldy and Katelyn Kiick and Thomas Kroes and Delissa McMillen and Trangthanh Pham and Christine Rimorin and Kimberly Siletti and Saroja Somasundaram and Michael Tieu and Amy Torkelson and Guoping Feng and Hopkins, \{William D\} and Thomas H{\"o}llt and Keene, \{C Dirk\} and Sten Linnarsson and McCarroll, \{Steven A\} and Lelieveldt, \{Boudewijn P\} and Sherwood, \{Chet C\} and Kimberly Smith and Walsh, \{Christopher A\} and Alexander Dobin and Jesse Gillis and Lein, \{Ed S\} and Hodge, \{Rebecca D\} and Bakken, \{Trygve E\}",

year = "2023",

month = oct,

day = "13",

doi = "10.1126/science.ade9516",

language = "English",

volume = "382",

journal = "Science (New York, N.Y.)",

issn = "0036-8075",

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

number = "6667",

}

Jorstad, NL, Song, JHT, Exposito-Alonso, D, Suresh, H, Castro-Pacheco, N, Krienen, FM, Yanny, AM, Close, J, Gelfand, E, Long, B, Seeman, SC, Travaglini, KJ, Basu, S, Beaudin, M, Bertagnolli, D, Crow, M, Ding, S-L, Eggermont, J, Glandon, A, Goldy, J, Kiick, K, Kroes, T, McMillen, D, Pham, T, Rimorin, C, Siletti, K, Somasundaram, S, Tieu, M, Torkelson, A, Feng, G, Hopkins, WD, Höllt, T, Keene, CD, Linnarsson, S, McCarroll, SA, Lelieveldt, BP, Sherwood, CC, Smith, K, Walsh, CA, Dobin, A, Gillis, J, Lein, ES, Hodge, RD & Bakken, TE 2023, 'Comparative transcriptomics reveals human-specific cortical features', Science (New York, N.Y.), vol. 382, no. 6667, eade9516. https://doi.org/10.1126/science.ade9516

TY - JOUR

T1 - Comparative transcriptomics reveals human-specific cortical features

AU - Jorstad, Nikolas L

AU - Song, Janet H T

AU - Exposito-Alonso, David

AU - Suresh, Hamsini

AU - Castro-Pacheco, Nathan

AU - Krienen, Fenna M

AU - Yanny, Anna Marie

AU - Close, Jennie

AU - Gelfand, Emily

AU - Long, Brian

AU - Seeman, Stephanie C

AU - Travaglini, Kyle J

AU - Basu, Soumyadeep

AU - Beaudin, Marc

AU - Bertagnolli, Darren

AU - Crow, Megan

AU - Ding, Song-Lin

AU - Eggermont, Jeroen

AU - Glandon, Alexandra

AU - Goldy, Jeff

AU - Kiick, Katelyn

AU - Kroes, Thomas

AU - McMillen, Delissa

AU - Pham, Trangthanh

AU - Rimorin, Christine

AU - Siletti, Kimberly

AU - Somasundaram, Saroja

AU - Tieu, Michael

AU - Torkelson, Amy

AU - Feng, Guoping

AU - Hopkins, William D

AU - Höllt, Thomas

AU - Keene, C Dirk

AU - Linnarsson, Sten

AU - McCarroll, Steven A

AU - Lelieveldt, Boudewijn P

AU - Sherwood, Chet C

AU - Smith, Kimberly

AU - Walsh, Christopher A

AU - Dobin, Alexander

AU - Gillis, Jesse

AU - Lein, Ed S

AU - Hodge, Rebecca D

AU - Bakken, Trygve E

PY - 2023/10/13

Y1 - 2023/10/13

N2 - The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.

AB - The cognitive abilities of humans are distinctive among primates, but their molecular and cellular substrates are poorly understood. We used comparative single-nucleus transcriptomics to analyze samples of the middle temporal gyrus (MTG) from adult humans, chimpanzees, gorillas, rhesus macaques, and common marmosets to understand human-specific features of the neocortex. Human, chimpanzee, and gorilla MTG showed highly similar cell-type composition and laminar organization as well as a large shift in proportions of deep-layer intratelencephalic-projecting neurons compared with macaque and marmoset MTG. Microglia, astrocytes, and oligodendrocytes had more-divergent expression across species compared with neurons or oligodendrocyte precursor cells, and neuronal expression diverged more rapidly on the human lineage. Only a few hundred genes showed human-specific patterning, suggesting that relatively few cellular and molecular changes distinctively define adult human cortical structure.

KW - Animals

KW - Cognition

KW - Gene Expression Profiling

KW - Gorilla gorilla/genetics

KW - Hominidae/genetics

KW - Humans

KW - Macaca mulatta/genetics

KW - Neocortex/physiology

KW - Pan troglodytes/genetics

KW - Phylogeny

KW - Species Specificity

KW - Temporal Lobe/physiology

KW - Transcriptome

U2 - 10.1126/science.ade9516

DO - 10.1126/science.ade9516

M3 - Article

C2 - 37824638

SN - 0036-8075

VL - 382

JO - Science (New York, N.Y.)

JF - Science (New York, N.Y.)

IS - 6667

M1 - eade9516

ER -

Comparative transcriptomics reveals human-specific cortical features

Abstract

Keywords

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