Comparative cellular analysis of motor cortex in human, marmoset and mouse

Trygve E. Bakken (), Nikolas L. Jorstad, Qiwen Hu, Blue B. Lake, Wei Tian, Brian E. Kalmbach, Megan Crow, Rebecca D. Hodge, Fenna M. Krienen, Staci A. Sorensen, Jeroen Eggermont, Zizhen Yao, Brian D. Aevermann, Andrew I. Aldridge, Anna Bartlett, Darren Bertagnolli, Tamara Casper, Rosa G. Castanon, Kirsten Crichton, Tanya L. Daigle, Rachel Dalley, Nick Dee, Nikolai Dembrow, Dinh Diep, Song-Lin Ding, Weixiu Dong, Rongxin Fang, Stephan Fischer, Melissa Goldman, Jeff Goldy, Lucas T. Graybuck, Brian R. Herb, Xiaomeng Hou, Jayaram Kancherla, Matthew Kroll, Kanan Lathia, Baldur Lew, Yang Eric Li, Christine S. Liu, Hanqing Liu, Jacinta D. Lucero, Anup Mahurkar, Delissa McMillen, Jeremy A. Miller, Marmar Moussa, Joseph R. Nery, Philip R. Nicovich, Sheng-Yong Niu, Joshua Orvis, Julia K. Osteen, Scott Owen, Carter R. Palmer, Thanh Pham, Nongluk Plongthongkum, Olivier Poirion, Nora M. Reed, Christine Rimorin, Angeline Rivkin, William J. Romanow, Adriana E. Sedeño-Cortés, Kimberly Siletti, Saroja Somasundaram, Josef Sulc, Michael Tieu, Amy Torkelson, Herman Tung, Xinxin Wang, Fangming Xie, Anna Marie Yanny, Renee Zhang, Seth A. Ament, M. Margarita Behrens, Hector Corrada Bravo, Jerold Chun, Alexander Dobin, Jesse Gillis, Ronna Hertzano, Patrick R. Hof, Thomas Höllt, Gregory D. Horwitz, C. Dirk Keene, Peter V. Kharchenko, Andrew L. Ko, Boudewijn P. Lelieveldt, Chongyuan Luo, Eran A. Mukamel, António Pinto-Duarte, Sebastian Preissl, Aviv Regev, Bing Ren, Richard H. Scheuermann, Kimberly Smith, William J. Spain, Owen R. White, Christof Koch, Michael Hawrylycz, Bosiljka Tasic, Evan Z. Macosko, Steven A. McCarroll, Jonathan T. Ting, Hongkui Zeng, Kun Zhang, Guoping Feng, Joseph R. Ecker, Sten Linnarsson and Ed S. Lein ()
Additional contact information
Trygve E. Bakken: Allen Institute for Brain Science
Nikolas L. Jorstad: Allen Institute for Brain Science
Qiwen Hu: Harvard Medical School
Blue B. Lake: University of California, San Diego
Wei Tian: The Salk Institute for Biological Studies
Brian E. Kalmbach: Allen Institute for Brain Science
Megan Crow: Cold Spring Harbor Laboratory
Rebecca D. Hodge: Allen Institute for Brain Science
Fenna M. Krienen: Harvard Medical School
Staci A. Sorensen: Allen Institute for Brain Science
Jeroen Eggermont: Leiden University Medical Center
Zizhen Yao: Allen Institute for Brain Science
Brian D. Aevermann: J. Craig Venter Institute
Andrew I. Aldridge: The Salk Institute for Biological Studies
Anna Bartlett: The Salk Institute for Biological Studies
Darren Bertagnolli: Allen Institute for Brain Science
Tamara Casper: Allen Institute for Brain Science
Rosa G. Castanon: The Salk Institute for Biological Studies
Kirsten Crichton: Allen Institute for Brain Science
Tanya L. Daigle: Allen Institute for Brain Science
Rachel Dalley: Allen Institute for Brain Science
Nick Dee: Allen Institute for Brain Science
Nikolai Dembrow: University of Washington
Dinh Diep: University of California, San Diego
Song-Lin Ding: Allen Institute for Brain Science
Weixiu Dong: University of California, San Diego
Rongxin Fang: University of California, San Diego
Stephan Fischer: Cold Spring Harbor Laboratory
Melissa Goldman: Harvard Medical School
Jeff Goldy: Allen Institute for Brain Science
Lucas T. Graybuck: Allen Institute for Brain Science
Brian R. Herb: University of Maryland School of Medicine
Xiaomeng Hou: University of California, San Diego
Jayaram Kancherla: University of Maryland College Park
Matthew Kroll: Allen Institute for Brain Science
Kanan Lathia: Allen Institute for Brain Science
Baldur Lew: Leiden University Medical Center
Yang Eric Li: University of California, San Diego
Christine S. Liu: Sanford Burnham Prebys Medical Discovery Institute
Hanqing Liu: The Salk Institute for Biological Studies
Jacinta D. Lucero: The Salk Institute for Biological Studies
Anup Mahurkar: University of Maryland School of Medicine
Delissa McMillen: Allen Institute for Brain Science
Jeremy A. Miller: Allen Institute for Brain Science
Marmar Moussa: University of Connecticut
Joseph R. Nery: The Salk Institute for Biological Studies
Philip R. Nicovich: Allen Institute for Brain Science
Sheng-Yong Niu: The Salk Institute for Biological Studies
Joshua Orvis: University of Maryland School of Medicine
Julia K. Osteen: The Salk Institute for Biological Studies
Scott Owen: Allen Institute for Brain Science
Carter R. Palmer: Sanford Burnham Prebys Medical Discovery Institute
Thanh Pham: Allen Institute for Brain Science
Nongluk Plongthongkum: University of California, San Diego
Olivier Poirion: University of California, San Diego
Nora M. Reed: Harvard Medical School
Christine Rimorin: Allen Institute for Brain Science
Angeline Rivkin: The Salk Institute for Biological Studies
William J. Romanow: Sanford Burnham Prebys Medical Discovery Institute
Adriana E. Sedeño-Cortés: Allen Institute for Brain Science
Kimberly Siletti: Karolinska Institutet
Saroja Somasundaram: Allen Institute for Brain Science
Josef Sulc: Allen Institute for Brain Science
Michael Tieu: Allen Institute for Brain Science
Amy Torkelson: Allen Institute for Brain Science
Herman Tung: Allen Institute for Brain Science
Xinxin Wang: Washington University School of Medicine
Fangming Xie: University of California, San Diego
Anna Marie Yanny: Allen Institute for Brain Science
Renee Zhang: J. Craig Venter Institute
Seth A. Ament: University of Maryland School of Medicine
M. Margarita Behrens: The Salk Institute for Biological Studies
Hector Corrada Bravo: University of Maryland College Park
Jerold Chun: Sanford Burnham Prebys Medical Discovery Institute
Alexander Dobin: Cold Spring Harbor Laboratory
Jesse Gillis: Cold Spring Harbor Laboratory
Ronna Hertzano: University of Maryland School of Medicine
Patrick R. Hof: Icahn School of Medicine at Mount Sinai
Thomas Höllt: Computer Graphics and Visualization Group, Delt University of Technology
Gregory D. Horwitz: University of Washington
C. Dirk Keene: University of Washington
Peter V. Kharchenko: Harvard Medical School
Andrew L. Ko: University of Washington School of Medicine
Boudewijn P. Lelieveldt: Leiden University Medical Center
Chongyuan Luo: University of California, Los Angeles
Eran A. Mukamel: University of California, San Diego
António Pinto-Duarte: The Salk Institute for Biological Studies
Sebastian Preissl: University of California, San Diego
Aviv Regev: Broad Institute of MIT and Harvard
Bing Ren: University of California, San Diego
Richard H. Scheuermann: J. Craig Venter Institute
Kimberly Smith: Allen Institute for Brain Science
William J. Spain: University of Washington
Owen R. White: University of Maryland School of Medicine
Christof Koch: Allen Institute for Brain Science
Michael Hawrylycz: Allen Institute for Brain Science
Bosiljka Tasic: Allen Institute for Brain Science
Evan Z. Macosko: Broad Institute of MIT and Harvard
Steven A. McCarroll: Harvard Medical School
Jonathan T. Ting: Allen Institute for Brain Science
Hongkui Zeng: Allen Institute for Brain Science
Kun Zhang: University of California, San Diego
Guoping Feng: McGovern Institute for Brain Research, MIT
Joseph R. Ecker: The Salk Institute for Biological Studies
Sten Linnarsson: Karolinska Institutet
Ed S. Lein: Allen Institute for Brain Science

Nature, 2021, vol. 598, issue 7879, 111-119

Abstract: Abstract The primary motor cortex (M1) is essential for voluntary fine-motor control and is functionally conserved across mammals1. Here, using high-throughput transcriptomic and epigenomic profiling of more than 450,000 single nuclei in humans, marmoset monkeys and mice, we demonstrate a broadly conserved cellular makeup of this region, with similarities that mirror evolutionary distance and are consistent between the transcriptome and epigenome. The core conserved molecular identities of neuronal and non-neuronal cell types allow us to generate a cross-species consensus classification of cell types, and to infer conserved properties of cell types across species. Despite the overall conservation, however, many species-dependent specializations are apparent, including differences in cell-type proportions, gene expression, DNA methylation and chromatin state. Few cell-type marker genes are conserved across species, revealing a short list of candidate genes and regulatory mechanisms that are responsible for conserved features of homologous cell types, such as the GABAergic chandelier cells. This consensus transcriptomic classification allows us to use patch–seq (a combination of whole-cell patch-clamp recordings, RNA sequencing and morphological characterization) to identify corticospinal Betz cells from layer 5 in non-human primates and humans, and to characterize their highly specialized physiology and anatomy. These findings highlight the robust molecular underpinnings of cell-type diversity in M1 across mammals, and point to the genes and regulatory pathways responsible for the functional identity of cell types and their species-specific adaptations.

Date: 2021
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DOI: 10.1038/s41586-021-03465-8

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