A multimodal cell census and atlas of the mammalian primary motor cortex

Adkins, Ricky S.; Aldridge, Andrew I.; Allen, Shona; Ament, Seth A.; An, Xu; Armand, Ethan; Ascoli, Giorgio A.; Bakken, Trygve E.; Bandrowski, Anita; Banerjee, Samik; Barkas, Nikolaos; Bartlett, Anna; Bateup, Helen S.; Behrens, M. Margarita; Berens, Philipp; Berg, Jim; Bernabucci, Matteo; Bernaerts, Yves; Bertagnolli, Darren; Biancalani, Tommaso; Boggeman, Lara; Booeshaghi, A. Sina; Bowman, Ian; Bravo, Héctor Corrada; Cadwell, Cathryn René; Callaway, Edward M.; Carlin, Benjamin; O'Connor, Carolyn; Carter, Robert; Casper, Tamara; Castanon, Rosa G.; Castro, Jesus Ramon; Chance, Rebecca K.; Chatterjee, Apaala; Chen, Huaming; Chun, Jerold; Colantuoni, Carlo; Crabtree, Jonathan; Creasy, Heather; Crichton, Kirsten; Crow, Megan; D'Orazi, Florence D.; Daigle, Tanya L.; Dalley, Rachel; Dee, Nick; Degatano, Kylee; Dichter, Benjamin; Diep, Dinh; Ding, Liya; Ding, Song-Lin; Dominguez, Bertha; Dong, Hong-Wei; Dong, Weixiu; Dougherty, Elizabeth L.; Dudoit, Sandrine; Ecker, Joseph R.; Eichhorn, Stephen W.; Fang, Rongxin; Felix, Victor; Feng, Guoping; Feng, Zhao; Fischer, Stephan; Fitzpatrick, Conor; Fong, Olivia; Foster, Nicholas N.; Galbavy, William; Gee, James C.; Ghosh, Satrajit S.; Giglio, Michelle; Gillespie, Thomas H.; Gillis, Jesse; Goldman, Melissa; Goldy, Jeff; Gong, Hui; Gou, Lin; Grauer, Michael; Halchenko, Yaroslav O.; Harris, Julie A.; Hartmanis, Leonard; Hatfield, Joshua T.; Hawrylycz, Mike; Helba, Brian; Herb, Brian R.; Hertzano, Ronna; Hintiryan, Houri; Hirokawa, Karla E.; Hockemeyer, Dirk; Hodge, Rebecca D.; Hood, Greg; Horwitz, Gregory D.; Hou, Xiaomeng; Hu, Lijuan; Hu, Qiwen; Huang, Z. Josh; Huo, Bingxing; Ito-Cole, Tony; Jacobs, Matthew; Jia, Xueyan; Jiang, Shengdian; Jiang, Tao; Jiang, Xiaolong; Jin, Xin; Jorstad, Nikolas L.; Kalmbach, Brian E.; Kancherla, Jayaram; Keene, C. Dirk; Kelly, Kathleen; Khajouei, Farzaneh; Kharchenko, Peter V.; Kim, Gukhan; Ko, Andrew L.; Kobak, Dmitry; Konwar, Kishori; Kramer, Daniel J.; Krienen, Fenna M.; Kroll, Matthew; Kuang, Xiuli; Kuo, Hsien-Chi; Lake, Blue B.; Larsen, Rachael; Lathia, Kanan; Laturnus, Sophie; Lee, Angus Y.; Lee, Cheng-Ta; Lee, Kuo-Fen; Lein, Ed S.; Lesnar, Phil; Li, Anan; Li, Xiangning; Li, Xu; Li, Yang Eric; Li, Yaoyao; Li, Yuanyuan; Lim, Byungkook; Linnarsson, Sten; Liu, Christine S.; Liu, Hanqing; Liu, Lijuan; Lucero, Jacinta D.; Luo, Chongyuan; Luo, Qingming; Macosko, Evan Z.; Mahurkar, Anup; Martone, Maryann E.; Matho, Katherine S.; McCarroll, Steven A.; McCracken, Carrie; McMillen, Delissa; Miranda, Elanine; Mitra, Partha P; Miyazaki, Paula Assakura; Mizrachi, Judith; Mok, Stephanie; Mukamel, Eran A.; Mulherkar, Shalaka; Nadaf, Naeem M.; Naeemi, Maitham; Narasimhan, Arun; Nery, Joseph R.; Ng, Lydia; Ngai, John; Nguyen, Thuc Nghi; Nickel, Lance; Nicovich, Philip R.; Niu, Sheng-Yong; Ntranos, Vasilis; Nunn, Michael; Olley, Dustin; Orvis, Joshua; Osteen, Julia K.; Osten, Pavel; Owen, Scott F.; Pachter, Lior; Palaniswamy, Ramesh; Palmer, Carter R.; Pang, Yan; Peng, Hanchuan; Pham, Thanh; Pinto-Duarte, Antonio; Plongthongkum, Nongluk; Poirion, Olivier; Preissl, Sebastian; Purdom, Elizabeth; Qu, Lei; Rashid, Mohammad; Reed, Nora M.; Regev, Aviv; Ren, Bing; Ren, Miao; Rimorin, Christine; Risso, Davide; Rivkin, Angeline C.; Muñoz-Castañeda, Rodrigo; Romanow, William J.; Ropelewski, Alexander J.; Roux de Bézieux, Hector; Ruan, Zongcai; Sandberg, Rickard; Savoia, Steven; Scala, Federico; Schor, Michael; Shen, Elise; Siletti, Kimberly; Smith, Jared B.; Smith, Kimberly; Somasundaram, Saroja; Song, Yuanyuan; Sorensen, Staci A.; Stafford, David A.; Street, Kelly; Sulc, Josef; Sunkin, Susan; Svensson, Valentine; Tan, Pengcheng; Tan, Zheng Huan; Tasic, Bosiljka; Thompson, Carol; Tian, Wei; Tickle, Timothy L.; Tieu, Michael; Ting, Jonathan T.; Tolias, Andreas Savas; Torkelson, Amy; Tung, Herman; Vaishnav, Eeshit Dhaval; Van den Berge, Koen; van Velthoven, Cindy T.J.; Vanderburg, Charles R.; Veldman, Matthew B.; Vu, Minh; Wakeman, Wayne; Wang, Peng; Wang, Quanxin; Wang, Xinxin; Wang, Yimin; Wang, Yun; Welch, Joshua D.; White, Owen; Williams, Elora; Xie, Fangming; Xie, Peng; Xiong, Feng; Yang, X. William; Yanny, Anna Marie; Yao, Zizhen; Yin, Lulu; Yu, Yang; Yuan, Jing; Zeng, Hongkui; Zhang, Kun; Zhang, Meng; Zhang, Zhuzhu; Zhao, Sujun; Zhao, Xuan; Zhou, Jingtian; Zhuang, Xiaowei; Zingg, Brian; BRAIN Initiative Cell Census Network (BICCN)

doi:10.1038/s41586-021-03950-0

Published October 7, 2021 | Version Published + Submitted + Supplemental Material

Journal Article Open

A multimodal cell census and atlas of the mammalian primary motor cortex

1. Salk Institute for Biological Studies
2. University of California, Los Angeles
3. University of Southern California
4. Allen Institute for Brain Science
5. Cold Spring Harbor Laboratory
6. Duke University
7. University of California, Berkeley
8. National Institute of Neurological Disorders and Stroke
9. University of California, San Diego
10. Ludwig Cancer Research
11. Baylor College of Medicine
12. University of Maryland, Baltimore
13. Harvard University
14. George Mason University
15. Sanford Burnham Prebys Medical Discovery Institute
16. McGovern Institute for Brain Research
17. Massachusetts Institute of Technology
18. Broad Institute
19. University of Pennsylvania
20. Dartmouth College
21. California Institute of Technology
22. Carnegie Mellon University
23. University of Tübingen
24. Universitätsklinikum Tübingen
25. Cajal Neuroscience (United States)
26. University of Washington
27. Tsinghua University
28. Karolinska Institute
29. Roche (United States)
30. Washington University in St. Louis
31. East China Normal University
32. New York University Shanghai
33. University of California, San Francisco
34. University of Padua
35. Dana-Farber Cancer Institute
36. Ghent University
37. University of Michigan–Ann Arbor
38. CZ Biohub
39. Stony Brook University
40. Huazhong University of Science and Technology
41. Wuhan National Laboratory for Optoelectronics
42. Soochow University
43. Hainan University
44. Southeast University
45. Wenzhou Medical University
46. Anhui University
47. Shanghai University
48. Stanford University
49. Harborview Medical Center
50. Innovative Genomics Institute
51. University of Maryland, College Park
52. Johns Hopkins University
53. Kitware (United States)

Here we report the generation of a multimodal cell census and atlas of the mammalian primary motor cortex as the initial product of the BRAIN Initiative Cell Census Network (BICCN). This was achieved by coordinated large-scale analyses of single-cell transcriptomes, chromatin accessibility, DNA methylomes, spatially resolved single-cell transcriptomes, morphological and electrophysiological properties and cellular resolution input–output mapping, integrated through cross-modal computational analysis. Our results advance the collective knowledge and understanding of brain cell-type organization. First, our study reveals a unified molecular genetic landscape of cortical cell types that integrates their transcriptome, open chromatin and DNA methylation maps. Second, cross-species analysis achieves a consensus taxonomy of transcriptomic types and their hierarchical organization that is conserved from mouse to marmoset and human. Third, in situ single-cell transcriptomics provides a spatially resolved cell-type atlas of the motor cortex. Fourth, cross-modal analysis provides compelling evidence for the transcriptomic, epigenomic and gene regulatory basis of neuronal phenotypes such as their physiological and anatomical properties, demonstrating the biological validity and genomic underpinning of neuron types. We further present an extensive genetic toolset for targeting glutamatergic neuron types towards linking their molecular and developmental identity to their circuit function. Together, our results establish a unifying and mechanistic framework of neuronal cell-type organization that integrates multi-layered molecular genetic and spatial information with multi-faceted phenotypic properties.

Additional Information

© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 04 October 2020; Accepted 25 August 2021; Published 06 October 2021. We thank additional members of our laboratories and institutions who contributed to the experimental and analytical components of this project. This work was supported by grants from the National Institute of Mental Health (NIMH) of the National Institutes of Health (NIH) under: U24MH114827, U19MH114821, U19MH114830, U19MH114831, U01MH117072, U01MH114829, U01MH121282, U01MH117023, U01MH114825, U01MH114819, U01MH114812, U01MH121260, U01MH114824, U01MH117079, U01MH116990, U01MH114828, R24MH117295, R24MH114793, R24MH114788, R24MH114815. We thank NIH BICCN program officers, in particular Yong Yao, for their guidance and support throughout this study. Additional support: NIH grants R01NS39600 and R01NS86082 to G.A.A. H.S.B. is a Chan Zuckerberg Biohub Investigator. Deutsche Forschungsgemeinschaft through a Heisenberg Professorship (BE5601/4-1), the Cluster of Excellence Machine Learning—New Perspectives for Science (EXC 2064, project number 390727645) and the Collaborative Research Center 1233 Robust Vision (project number 276693517), the German Federal Ministry of Education and Research (FKZ 01GQ1601 and 01IS18039A) to P.B. This work was supported in part by the Flow Cytometry Core Facility of the Salk Institute with funding from NIH-NCI CCSG: P30 014195 and Shared Instrumentation Grant S10-OD023689. NIH grant R01MH094360 to H.-W.D. We thank M. Becerra, T. Boesen, C. Cao, M. Fayzullina, K. Cotter, L. Gao, L. Gacia, L. Korobkova, D. Lo, C. Mun, S. Yamashita and M Zhu for their technical and informatics support. Hearing Health Foundation Hearing Restoration Project grant to R.H. NIH grant OD010425 to G.D.H. NIH grant RF1MH114126 to E.S.L. and J.T.T. National Natural Science Foundation of China (NNSFC) grant 61890953 to H.G. NNSFC grant 81827901 to Q.L. This project was supported in part by NIH grants P51OD010425 from the Office of Research Infrastructure Programs (ORIP) and UL1TR000423 from the National Center for Advancing Translational Sciences (NCATS). Its contents are solely the responsibility of the authors and do not necessarily represent the official view of NIH, ORIP, NCATS or the Institute of Translational Health Sciences at the Washington National Primate Research Center. NNSFC grant 61871411 and the University Synergy Innovation Program of Anhui Province GXXT-2019-008 to L.Q. Howard Hughes Medical Institute and the Klarman Cell Observatory for A.R. Howard Hughes Medical Institute for J.R.E. and X. Zhuang. NNSFC Grant 32071367 and NSF Shanghai Grant 20ZR1420100 to Yimin Wang. NIH grants R01EY023173 and U01MH105982 to H.Z. Researchers from Allen Institute for Brain Science wish to thank the Allen Institute founder, P. G. Allen, for his vision, encouragement and support. Data availability: Primary data are accessible through the Brain Cell Data Center and data archives. Brain Cell Data Center (BCDC), Overall BICCN organization and data, www.biccn.org. Neuroscience Multi-omic Data Archive (NeMO), RRID:SCR_016152. Brain Image Library (BIL), RRID:SCR_017272. Distributed Archives for Neurophysiology Data Integration (DANDI), RRID:SCR_017571. Publicly used databases in study: NCBI Homologene, 11/22/2019, https://www.ncbi.nlm.nih.gov/homologene, GENCODE mm10 (v16), https://www.gencodegenes.org, JASPAR 2020 database, http://jaspar.genereg.net. All data resources associated with this publication are available as listed at: https://github.com/BICCN/CellCensusMotorCortex and https://doi.org/10.5281/zenodo.4726182. Code availability: All code and libraries used in the manuscript are available at https://github.com/BICCN/CellCensusMotorCortex and https://doi.org/10.5281/zenodo.4726182. Author Contributions: BICCN contributing principal investigators: G.A.A., M.M.B., E.M.C., J. Chun, J.R.E., G.F., J.C.G., S.S.G., Y.O.H., M.J.H., R.H., H.-W.D., Z.J.H., E.S.L., B.K.L., M.E.M., L. Ng, P.O., L.P., A.J.R., T.L.T., A.S.T., O.W., X.W.Y., H.Z., K.Z., X. Zhuang and J.N. Principal manuscript editors: Z.J.H., E.S.L. and H.Z. Manuscript writing and figure generation: G.A.A., T.E.B., P.B., E.M.C., T.L.D., J.A.H., J.R.E., M.J.H., H.-W.D., Z.J.H., N.L.J., B.E.K., D.K., E.S.L., Y.E.L., H.L., K.S.M., E.A.M., M. Naeemi, B.Z., P.O., B.R., F.S., P.T., J.T.T., A.S.T., F. Xie, H.Z., M.Z., Z.Z., J.Z., X. Zhuang and J.N. Analysis coordination: T.E.B., E.M.C., J.A.H., J.R.E., M.J.H., H.-W.D., Z.J.H., E.S.L., E.A.M., P.O., B.R., A.S.T., H.Z., X. Zhuang and J.N. Integrated data analysis: E.A., T.E.B., P.B., J.A.H., J.R.E., H.-W.D., Z.J.H., N.L.J., B.E.K., D.K., E.S.L., Y.E.L., H.L., E.A.M., P.O., B.R., F.S., P.T., A.S.T., F. Xie, Z.Y., H.Z., M.Z., Z.Z., J.Z. and X. Zhuang. scRNA-seq and snRNA-seq data generation and processing: D.B., T.N.N., T.C., J. Chun, K.C., N.D., D.D., S.D., W.D., E.L.D., G.F., O.F., M. Goldman, J. Goldy, R.D.H., L. Hu, C.D.K., F.M.K., M.K., B.B.L., K.L., E.S.L., S. Linnarsson, C.S.L., E.Z.M., S.A.M., D.M., N.M.N., C.R.P., T.P., N.P., N.M.R., A.R., C.R., W.J.R., S. Savoia, K. Siletti, K. Smith, J.S., B.T., M.T., A.T., H.T., C.T.J.v.V., C.R.V., A.M.Y., H.Z. and K.Z. ATAC-seq data generation and processing: M.M.B., J. Chun, D.D., W.D., R.F., X.H., B.B.L., Y.E.L., C.S.L., J.D.L., J.K.O., C.R.P., A.P.-D., N.P., O.P., S.P., B.R., W.J.R., X.W. and K.Z. Methylcytosine data production and analysis: A.I.A., A. Bartlett, M.M.B., L.B., C.O., R.G.C., H.C., J.R.E., C.F., C.L., H.L., J.D.L., J.R.N., M. Nunn, J.K.O., A.P.-D., A.C.R., W.T. and J.Z. Epi-retro-seq data generation and processing: A. Bartlett, M.M.B., L.B., E.M.C., C.O., R.G.C., B. Dominguez, J.R.E., C.F., T.I.-C., M.J., X. Jin, C.L., K.L., P.A.M., E.A.M., J.R.N., M. Nunn, Y.P., A.P.-D., M. Rashid, A.C.R., J.B.S., P.T., M.V., E.W., Z.Z. and J.Z. 'Omics data analysis: E.A., T.E.B., T.B., A.S.B., M.C., D.D., S.D., J.R.E., R.F., S.F., O.F., J. Gillis, J. Goldy, Q.H., N.L.J., P.V.K., F.M.K., B.B.L., E.S.L., Y.E.L., S. Linnarsson, H.L., E.Z.M., E.A.M., S.-Y.N., V.N., L.P., O.P., E.P., A.R., D.R., H.R.d.B., K. Siletti, K. Smith, S. Somasundaram, K. Street, V.S., B.T., W.T., E.D.V., K.V.d.B., C.T.J.v.V., J.D.W., F. Xie, Z.Y., H.Z., J.Z. and J.N. Tracing and connectivity data generation: X.A., H.S.B., R.K.C., J.A.H., K.E.H., W.G., H.G., J.T.H., I.B., H.-W.D., Z.J.H., G.K., D.J.K., A.L., Xiangning Li, B.K.L., Q.L., K.S.M., L. Ng, L.G., H.H., B.Z., R.M.-C., D.A.S., H.Z. and J.N. Morphology data generation and reconstruction: T.L.D., J.A.H., Z.F., K.E.H., H.G., H.-W.D., Z.J.H., X. Jia, S.J., T.J., X.K., R.L., P.L., Xiangning Li, Yaoyao Li, Yuanyuan Li, L.L., Q.L., H.P., L.Q., M. Ren, Z.R., E.S., Y.S., W.W., P.W., Yimin Wang, Yun Wang, L.Y., J.Y., H.Z., S.Z. and X. Zhao. OLST/STPT and other data generation: X.A., W.G., J.T.H., Z.J.H., G.K., K.S.M., A.N., P.O., R.P. and R.M.-C. Morphology, connectivity and imaging analysis: X.A., G.A.A., S.B., L.D., J.A.H., Z.F., W.G., H.G., J.T.H., H.-W.D., Z.J.H., D. Huilgol, B. Huo, X. Jia, G.K., H.-C.K., S. Laturnus, A.L., Xu Li, N.N.F., K.S.M., P.P.M., J.M., M. Naeemi, A.N., L. Ng, P.O., R.P., H.P., R.M.-C., Q.W., Yimin Wang, Yun Wang, P.X., F. Xiong, Y.Y. and H.Z. Spatially resolved single-cell transcriptomics (MERFISH): M.Z., S.W.E., B.Z., Z.Y., H.Z., H.-W.D. and X. Zhuang. Multimodal profiling (Patch-seq): P.B., J.B., M.B., Y.B., C.R.C., J.R.C., R.D., P.R.N., L. Hartmanis, G.D.H., X. Jiang, B.E.K., C.D.K., A.L.K., D.K., S. Laturnus, E.S.L., E.M., S. Mulherkar, S.F.O., R.S., F.S., K. Smith, S.A.S., Z.H.T., J.T.T., A.S.T. and H.Z. Transgenic tools: S.A., X.A., H.S.B., R.K.C., T.L.D., W.G., J.T.H., D. Hockemeyer, Z.J.H., D. Huilgol, G.K., D.J.K., A.Y.L., K.S.M., D.A.S., B.T., M.B.V., X.W.Y., Z.Y., H.Z. and J.N. NeMO archive and analytics: R.S.A., S.A.A., H.C.B., R.C., A.C., C.C., J. Crabtree, H.C., V.F., M. Giglio, B.R.H., R.H., J.K., A.M., C.M., L. Nickel, D.O., J.O., M.S. and O.W. Brain Image Library (BIL) archive: G.H. and A.J.R. DANDI archive: B. Dichter, S.S.G., M. Grauer, Y.O.H. and B. Helba. Brain Cell Data Center (BCDC): A. Bandrowski, N.B., B.C., F.D.D., K.D., J.C.G., T.H.G., M.J.H., F.K., K. Konwar, M.E.M., L. Ng, C.T. and T.L.T. Project management: F.D.D., H.G., K. Kelly, B.B.L., K.S.M., S. Mok, H.H., M. Nunn, S. Sunkin and C.T. Manuscript correspondence: H.Z. Competing interests: A. Bandrowski is a cofounder of SciCrunch, a company devoted to improving scientific communication. J.R.E. is a member of Zymo Research SAB. J.A.H., K.E.H., T.N.N. and P.R.N. are currently employed by Cajal Neuroscience. P.V.K. serves on the Scientific Advisory Board of Celsius Therapeutics Inc. M.E.M. is a founder and CSO of SciCrunch Inc., a UCSD tech start up that produces tools in support of reproducibility including RRIDs. A.R. is a founder and equity holder of Celsius Therapeutics, an equity holder in Immunitas Therapeutics and until 31 August 2020 was a member of the scientific advisory board of Syros Pharmaceuticals, Neogene Therapeutics, Asimov and ThermoFisher Scientific. From 1 August 2020, A.R. has been an employee of Genentech. B.R. is a co-founder of Arima Genomics, Inc. and Epigenome Technologies, Inc. K.Z. is a co-founder, equity holder and serves on the Scientific Advisor Board of Singlera Genomics. X. Zhuang is a co-founder and consultant of Vizgen. Peer review information: Nature thanks Peter Jones, Manolis Kellis and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Additional details

Eprint ID: 106288
Resolver ID: CaltechAUTHORS:20201027-075126222

Describes: 10.1101/2020.10.19.343129 (DOI); 10.5281/zenodo.4726182 (DOI); https://github.com/BICCN/CellCensusMotorCortex (URL)

NIH
U24MH114827
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U19MH114821
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U19MH114830
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U19MH114831
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U01MH117072
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U01MH114829
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U01MH117023
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U01MH114825
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U01MH114819
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R24MH114793
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R24MH114788
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R24MH114815
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R01NS39600
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R01NS86082
Chan Zuckerberg Initiative
Deutsche Forschungsgemeinschaft (DFG)
BE5601/4-1
Deutsche Forschungsgemeinschaft (DFG)
EXC 2064
Deutsche Forschungsgemeinschaft (DFG)
390727645
Deutsche Forschungsgemeinschaft (DFG)
276693517
Bundesministerium für Bildung und Forschung (BMBF)
FKZ 01GQ1601
Bundesministerium für Bildung und Forschung (BMBF)
FKZ 01IS18039A
NIH
P30 014195
NIH
S10-OD023689
NIH
R01MH094360
NIH
OD010425
NIH
RF1MH114126
National Natural Science Foundation of China
61890953
National Natural Science Foundation of China
81827901
NIH
P51OD010425
NIH
UL1TR000423
National Natural Science Foundation of China
61871411
Anhui Province
GXXT-2019-008
Howard Hughes Medical Institute (HHMI)
Klarman Cell Observatory
National Natural Science Foundation of China
32071367
National Natural Science Foundation of China
20ZR1420100
NIH
R01EY023173
NIH
U01MH105982
Allen Institute for Brain Science
Salk Institute

Created: 2020-10-27

Created from EPrint's datestamp field
Updated: 2021-10-29

Created from EPrint's last_modified field

Caltech groups: Division of Biology and Biological Engineering (BBE)

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A multimodal cell census and atlas of the mammalian primary motor cortex

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A multimodal cell census and atlas of the mammalian primary motor cortex

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2020.10.19.343129v1.full.pdf

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