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Cellular Anatomy of the Mouse Primary Motor Cortex

Rodrigo Muñoz-Castañeda, View ORCID ProfileBrian Zingg, View ORCID ProfileKatherine S. Matho, View ORCID ProfileQuanxin Wang, View ORCID ProfileXiaoyin Chen, View ORCID ProfileNicholas N. Foster, View ORCID ProfileArun Narasimhan, Anan Li, View ORCID ProfileKarla E. Hirokawa, View ORCID ProfileBingxing Huo, View ORCID ProfileSamik Bannerjee, View ORCID ProfileLaura Korobkova, Chris Sin Park, View ORCID ProfileYoung-Gyun Park, View ORCID ProfileMichael S. Bienkowski, View ORCID ProfileUree Chon, View ORCID ProfileDiek W. Wheeler, Xiangning Li, Yun Wang, View ORCID ProfileKathleen Kelly, View ORCID ProfileXu An, View ORCID ProfileSarojini M. Attili, View ORCID ProfileIan Bowman, View ORCID ProfileAnastasiia Bludova, View ORCID ProfileAli Cetin, Liya Ding, View ORCID ProfileRhonda Drewes, View ORCID ProfileFlorence D’Orazi, View ORCID ProfileCorey Elowsky, View ORCID ProfileStephan Fischer, View ORCID ProfileWilliam Galbavy, View ORCID ProfileLei Gao, View ORCID ProfileJesse Gillis, View ORCID ProfilePeter A. Groblewski, Lin Gou, View ORCID ProfileJoel D. Hahn, View ORCID ProfileJoshua T. Hatfield, View ORCID ProfileHouri Hintiryan, Jason Huang, Hideki Kondo, Xiuli Kuang, Philip Lesnar, Xu Li, View ORCID ProfileYaoyao Li, Mengkuan Lin, Lijuan Liu, View ORCID ProfileDarrick Lo, View ORCID ProfileJudith Mizrachi, Stephanie Mok, View ORCID ProfileMaitham Naeemi, View ORCID ProfilePhilip R. Nicovich, View ORCID ProfileRamesh Palaniswamy, View ORCID ProfileJason Palmer, View ORCID ProfileXiaoli Qi, View ORCID ProfileElise Shen, View ORCID ProfileYu-Chi Sun, View ORCID ProfileHuizhong Tao, View ORCID ProfileWayne Wakemen, Yimin Wang, Peng Xie, View ORCID ProfileShenqin Yao, Jin Yuan, View ORCID ProfileMuye Zhu, View ORCID ProfileLydia Ng, Li I. Zhang, Byung Kook Lim, View ORCID ProfileMichael Hawrylycz, Hui Gong, View ORCID ProfileJames C. Gee, View ORCID ProfileYongsoo Kim, View ORCID ProfileHanchuan Peng, View ORCID ProfileKwanghun Chuang, View ORCID ProfileX William Yang, Qingming Luo, View ORCID ProfilePartha P. Mitra, View ORCID ProfileAnthony M. Zador, View ORCID ProfileHongkui Zeng, View ORCID ProfileGiorgio A. Ascoli, View ORCID ProfileZ Josh Huang, Pavel Osten, View ORCID ProfileJulie A. Harris, View ORCID ProfileHong-Wei Dong
doi: https://doi.org/10.1101/2020.10.02.323154
Rodrigo Muñoz-Castañeda
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Brian Zingg
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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  • ORCID record for Brian Zingg
Katherine S. Matho
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Quanxin Wang
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Xiaoyin Chen
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Nicholas N. Foster
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Arun Narasimhan
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Anan Li
4Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan 430074, China; HUST-Suzhou Institute for Brainsmatics, Suzhou 215123, China
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Karla E. Hirokawa
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Bingxing Huo
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Samik Bannerjee
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Laura Korobkova
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Chris Sin Park
6Center for Neurobehavioral Genetics, Jane and Terry Semel Institute for Neuroscience and Human Behavior; Department of Psychiatry and Biobehavioral Sciences; Brain Research Institute, David Geffen School of Medicine at UCLA, Los Angeles, CA, 90095, USA
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Young-Gyun Park
7Institute for Medical Engineering and Science, Department of Chemical Engineering, Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
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Michael S. Bienkowski
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
5Department of Physiology & Neuroscience, Zilkha Neurogenetic Institute, Keck School of Medicine of USC, University of Southern California
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Uree Chon
8Department of Neural and Behavioral Sciences, College of Medicine, Penn State University, Hershey, PA, USA
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Diek W. Wheeler
9Center for Neural Informatics, Structures, & Plasticity, Bioengineering Department, and Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA (USA)
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Xiangning Li
4Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan 430074, China; HUST-Suzhou Institute for Brainsmatics, Suzhou 215123, China
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Yun Wang
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Kathleen Kelly
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Xu An
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Sarojini M. Attili
9Center for Neural Informatics, Structures, & Plasticity, Bioengineering Department, and Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA (USA)
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Ian Bowman
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Anastasiia Bludova
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Ali Cetin
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Liya Ding
10SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Rhonda Drewes
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Florence D’Orazi
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Corey Elowsky
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Stephan Fischer
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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William Galbavy
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Lei Gao
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Jesse Gillis
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Peter A. Groblewski
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Lin Gou
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Joel D. Hahn
11Department of Biological Sciences, University of Southern California, California, Los Angeles, USA
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Joshua T. Hatfield
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Houri Hintiryan
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Jason Huang
12Center for Neural Circuits & Sensory Processing Disorders, Zilkha Neurogenetics Institute (ZNI), Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California
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Hideki Kondo
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Xiuli Kuang
13School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Philip Lesnar
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Xu Li
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Yaoyao Li
13School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Mengkuan Lin
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Lijuan Liu
10SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Darrick Lo
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Judith Mizrachi
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Stephanie Mok
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Maitham Naeemi
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Philip R. Nicovich
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Ramesh Palaniswamy
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Jason Palmer
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Xiaoli Qi
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Elise Shen
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Yu-Chi Sun
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Huizhong Tao
12Center for Neural Circuits & Sensory Processing Disorders, Zilkha Neurogenetics Institute (ZNI), Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California
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Wayne Wakemen
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Yimin Wang
10SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
17School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Peng Xie
10SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Shenqin Yao
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Jin Yuan
4Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan 430074, China; HUST-Suzhou Institute for Brainsmatics, Suzhou 215123, China
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Muye Zhu
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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Lydia Ng
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Li I. Zhang
12Center for Neural Circuits & Sensory Processing Disorders, Zilkha Neurogenetics Institute (ZNI), Department of Physiology and Neuroscience, Keck School of Medicine, University of Southern California
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Byung Kook Lim
14Division of Biological Science, Neurobiology section, University of California, San Diego
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Michael Hawrylycz
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Hui Gong
4Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan 430074, China; HUST-Suzhou Institute for Brainsmatics, Suzhou 215123, China
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James C. Gee
15Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104
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Yongsoo Kim
8Department of Neural and Behavioral Sciences, College of Medicine, Penn State University, Hershey, PA, USA
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Hanchuan Peng
10SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Kwanghun Chuang
7Institute for Medical Engineering and Science, Department of Chemical Engineering, Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
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X William Yang
6Center for Neurobehavioral Genetics, Jane and Terry Semel Institute for Neuroscience and Human Behavior; Department of Psychiatry and Biobehavioral Sciences; Brain Research Institute, David Geffen School of Medicine at UCLA, Los Angeles, CA, 90095, USA
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Qingming Luo
4Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan 430074, China; HUST-Suzhou Institute for Brainsmatics, Suzhou 215123, China
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Partha P. Mitra
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Anthony M. Zador
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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Hongkui Zeng
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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Giorgio A. Ascoli
9Center for Neural Informatics, Structures, & Plasticity, Bioengineering Department, and Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA (USA)
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  • For correspondence: HongWeiD@mednet.ucla.edu jharris@cajalneuro.com osten@cshl.edu huangj@cshl.edu ascoli@gmu.edu
Z Josh Huang
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
16Department of Neurobiology, Duke University School of Medicine, Durham, NC27705
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  • ORCID record for Z Josh Huang
  • For correspondence: HongWeiD@mednet.ucla.edu jharris@cajalneuro.com osten@cshl.edu huangj@cshl.edu ascoli@gmu.edu
Pavel Osten
1Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
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  • For correspondence: HongWeiD@mednet.ucla.edu jharris@cajalneuro.com osten@cshl.edu huangj@cshl.edu ascoli@gmu.edu
Julie A. Harris
3Allen Institute for Brain Science, Seattle, WA 98109, USA
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  • For correspondence: HongWeiD@mednet.ucla.edu jharris@cajalneuro.com osten@cshl.edu huangj@cshl.edu ascoli@gmu.edu
Hong-Wei Dong
2USC Stevens Neuroimaging and Informatics Institute (INI), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA 90033
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  • For correspondence: HongWeiD@mednet.ucla.edu jharris@cajalneuro.com osten@cshl.edu huangj@cshl.edu ascoli@gmu.edu
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Abstract

An essential step toward understanding brain function is to establish a cellular-resolution structural framework upon which multi-scale and multi-modal information spanning molecules, cells, circuits and systems can be integrated and interpreted. Here, through a collaborative effort from the Brain Initiative Cell Census Network (BICCN), we derive a comprehensive cell type-based description of one brain structure - the primary motor cortex upper limb area (MOp-ul) of the mouse. Applying state-of-the-art labeling, imaging, computational, and neuroinformatics tools, we delineated the MOp-ul within the Mouse Brain 3D Common Coordinate Framework (CCF). We defined over two dozen MOp-ul projection neuron (PN) types by their anterograde targets; the spatial distribution of their somata defines 11 cortical sublayers, a significant refinement of the classic notion of cortical laminar organization. We further combine multiple complementary tracing methods (classic tract tracing, cell type-based anterograde, retrograde, and transsynaptic viral tracing, high-throughput BARseq, and complete single cell reconstruction) to systematically chart cell type-based MOp input-output streams. As PNs link distant brain regions at synapses as well as host cellular gene expression, our construction of a PN type resolution MOp-ul wiring diagram will facilitate an integrated analysis of motor control circuitry across the molecular, cellular, and systems levels. This work further provides a roadmap towards a cellular resolution description of mammalian brain architecture.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵* Co-first authors

  • ↵† Current affiliation/address of these authors: Department of Neurobiology, David Geffen School of Medicine at UCLA, Los Angeles, CA 90089

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Cellular Anatomy of the Mouse Primary Motor Cortex
Rodrigo Muñoz-Castañeda, Brian Zingg, Katherine S. Matho, Quanxin Wang, Xiaoyin Chen, Nicholas N. Foster, Arun Narasimhan, Anan Li, Karla E. Hirokawa, Bingxing Huo, Samik Bannerjee, Laura Korobkova, Chris Sin Park, Young-Gyun Park, Michael S. Bienkowski, Uree Chon, Diek W. Wheeler, Xiangning Li, Yun Wang, Kathleen Kelly, Xu An, Sarojini M. Attili, Ian Bowman, Anastasiia Bludova, Ali Cetin, Liya Ding, Rhonda Drewes, Florence D’Orazi, Corey Elowsky, Stephan Fischer, William Galbavy, Lei Gao, Jesse Gillis, Peter A. Groblewski, Lin Gou, Joel D. Hahn, Joshua T. Hatfield, Houri Hintiryan, Jason Huang, Hideki Kondo, Xiuli Kuang, Philip Lesnar, Xu Li, Yaoyao Li, Mengkuan Lin, Lijuan Liu, Darrick Lo, Judith Mizrachi, Stephanie Mok, Maitham Naeemi, Philip R. Nicovich, Ramesh Palaniswamy, Jason Palmer, Xiaoli Qi, Elise Shen, Yu-Chi Sun, Huizhong Tao, Wayne Wakemen, Yimin Wang, Peng Xie, Shenqin Yao, Jin Yuan, Muye Zhu, Lydia Ng, Li I. Zhang, Byung Kook Lim, Michael Hawrylycz, Hui Gong, James C. Gee, Yongsoo Kim, Hanchuan Peng, Kwanghun Chuang, X William Yang, Qingming Luo, Partha P. Mitra, Anthony M. Zador, Hongkui Zeng, Giorgio A. Ascoli, Z Josh Huang, Pavel Osten, Julie A. Harris, Hong-Wei Dong
bioRxiv 2020.10.02.323154; doi: https://doi.org/10.1101/2020.10.02.323154
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Cellular Anatomy of the Mouse Primary Motor Cortex
Rodrigo Muñoz-Castañeda, Brian Zingg, Katherine S. Matho, Quanxin Wang, Xiaoyin Chen, Nicholas N. Foster, Arun Narasimhan, Anan Li, Karla E. Hirokawa, Bingxing Huo, Samik Bannerjee, Laura Korobkova, Chris Sin Park, Young-Gyun Park, Michael S. Bienkowski, Uree Chon, Diek W. Wheeler, Xiangning Li, Yun Wang, Kathleen Kelly, Xu An, Sarojini M. Attili, Ian Bowman, Anastasiia Bludova, Ali Cetin, Liya Ding, Rhonda Drewes, Florence D’Orazi, Corey Elowsky, Stephan Fischer, William Galbavy, Lei Gao, Jesse Gillis, Peter A. Groblewski, Lin Gou, Joel D. Hahn, Joshua T. Hatfield, Houri Hintiryan, Jason Huang, Hideki Kondo, Xiuli Kuang, Philip Lesnar, Xu Li, Yaoyao Li, Mengkuan Lin, Lijuan Liu, Darrick Lo, Judith Mizrachi, Stephanie Mok, Maitham Naeemi, Philip R. Nicovich, Ramesh Palaniswamy, Jason Palmer, Xiaoli Qi, Elise Shen, Yu-Chi Sun, Huizhong Tao, Wayne Wakemen, Yimin Wang, Peng Xie, Shenqin Yao, Jin Yuan, Muye Zhu, Lydia Ng, Li I. Zhang, Byung Kook Lim, Michael Hawrylycz, Hui Gong, James C. Gee, Yongsoo Kim, Hanchuan Peng, Kwanghun Chuang, X William Yang, Qingming Luo, Partha P. Mitra, Anthony M. Zador, Hongkui Zeng, Giorgio A. Ascoli, Z Josh Huang, Pavel Osten, Julie A. Harris, Hong-Wei Dong
bioRxiv 2020.10.02.323154; doi: https://doi.org/10.1101/2020.10.02.323154

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