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Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types

View ORCID ProfileHanchuan Peng, Peng Xie, View ORCID ProfileLijuan Liu, Xiuli Kuang, Yimin Wang, Lei Qu, Hui Gong, Shengdian Jiang, Anan Li, Zongcai Ruan, Liya Ding, Chao Chen, Mengya Chen, Tanya L. Daigle, Zhangcan Ding, Yanjun Duan, Aaron Feiner, Ping He, Chris Hill, Karla E. Hirokawa, Guodong Hong, Lei Huang, Sara Kebede, Hsien-Chi Kuo, Rachael Larsen, Phil Lesnar, Longfei Li, Qi Li, Xiangning Li, Yaoyao Li, Yuanyuan Li, An Liu, Donghuan Lu, Stephanie Mok, Lydia Ng, Thuc Nghi Nguyen, Qiang Ouyang, Jintao Pan, Elise Shen, Yuanyuan Song, Susan M. Sunkin, Bosiljka Tasic, Matthew B. Veldman, Wayne Wakeman, Wan Wan, Peng Wang, Quanxin Wang, Tao Wang, Yaping Wang, Feng Xiong, Wei Xiong, Wenjie Xu, Zizhen Yao, Min Ye, Lulu Yin, Yang Yu, Jia Yuan, Jing Yuan, Zhixi Yun, Shaoqun Zeng, Shichen Zhang, Sujun Zhao, Zijun Zhao, Zhi Zhou, Z. Josh Huang, Luke Esposito, Michael J. Hawrylycz, Staci A. Sorensen, X. William Yang, Yefeng Zheng, Zhongze Gu, Wei Xie, Christof Koch, Qingming Luo, Julie A. Harris, Yun Wang, View ORCID ProfileHongkui Zeng
doi: https://doi.org/10.1101/675280
Hanchuan Peng
1Allen Institute for Brain Science, Seattle, WA 98109, USA
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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  • ORCID record for Hanchuan Peng
  • For correspondence: h@braintell.org hongkuiz@alleninstitute.org
Peng Xie
1Allen Institute for Brain Science, Seattle, WA 98109, USA
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Lijuan Liu
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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  • ORCID record for Lijuan Liu
Xiuli Kuang
3School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Yimin Wang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
4School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Lei Qu
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
5Key Laboratory of Intelligent Computation & Signal Processing, Ministry of Education, Anhui University, Hefei, Anhui, China
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Hui Gong
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
7HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics, Suzhou, Jiangsu, China
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Shengdian Jiang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Anan Li
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
7HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics, Suzhou, Jiangsu, China
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Zongcai Ruan
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Liya Ding
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Chao Chen
3School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Mengya Chen
4School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Tanya L. Daigle
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Zhangcan Ding
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Yanjun Duan
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Aaron Feiner
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Ping He
4School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Chris Hill
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Karla E. Hirokawa
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Guodong Hong
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Lei Huang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Sara Kebede
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Hsien-Chi Kuo
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Rachael Larsen
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Phil Lesnar
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Longfei Li
5Key Laboratory of Intelligent Computation & Signal Processing, Ministry of Education, Anhui University, Hefei, Anhui, China
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Qi Li
4School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Xiangning Li
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
7HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics, Suzhou, Jiangsu, China
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Yaoyao Li
3School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Yuanyuan Li
5Key Laboratory of Intelligent Computation & Signal Processing, Ministry of Education, Anhui University, Hefei, Anhui, China
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An Liu
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Donghuan Lu
8Tencent Jarvis Lab, Shenzhen, Guangdong, China
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Stephanie Mok
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Lydia Ng
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Thuc Nghi Nguyen
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Qiang Ouyang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Jintao Pan
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Elise Shen
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Yuanyuan Song
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Susan M. Sunkin
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Bosiljka Tasic
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Matthew B. Veldman
9Center for Neurobehavioral Genetics, Jane and Terry Semel Institute for Neuroscience and Human Behavior; Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA
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Wayne Wakeman
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Wan Wan
5Key Laboratory of Intelligent Computation & Signal Processing, Ministry of Education, Anhui University, Hefei, Anhui, China
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Peng Wang
4School of Computer Engineering and Science, Shanghai University, Shanghai, China
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Quanxin Wang
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Tao Wang
5Key Laboratory of Intelligent Computation & Signal Processing, Ministry of Education, Anhui University, Hefei, Anhui, China
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Yaping Wang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Feng Xiong
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Wei Xiong
3School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Wenjie Xu
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Zizhen Yao
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Min Ye
3School of Optometry and Ophthalmology, Wenzhou Medical University, Wenzhou, Zhejiang, China
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Lulu Yin
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Yang Yu
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Jia Yuan
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Jing Yuan
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
7HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics, Suzhou, Jiangsu, China
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Zhixi Yun
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Shaoqun Zeng
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
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Shichen Zhang
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Sujun Zhao
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Zijun Zhao
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Zhi Zhou
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Z. Josh Huang
10Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
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Luke Esposito
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Michael J. Hawrylycz
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Staci A. Sorensen
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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X. William Yang
9Center for Neurobehavioral Genetics, Jane and Terry Semel Institute for Neuroscience and Human Behavior; Department of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA
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Yefeng Zheng
8Tencent Jarvis Lab, Shenzhen, Guangdong, China
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Zhongze Gu
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Wei Xie
2SEU-ALLEN Joint Center, Institute for Brain and Intelligence, Southeast University, Nanjing, Jiangsu, China
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Christof Koch
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Qingming Luo
6Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics, Huazhong University of Science and Technology, Wuhan, Hubei, China
11School of Biomedical Engineering, Hainan University, Haikou, Hainan, China
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Julie A. Harris
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Yun Wang
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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Hongkui Zeng
1Allen Institute for Brain Science, Seattle, WA 98109, USA
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  • ORCID record for Hongkui Zeng
  • For correspondence: h@braintell.org hongkuiz@alleninstitute.org
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ABSTRACT

Ever since the seminal findings of Ramon y Cajal, dendritic and axonal morphology has been recognized as a defining feature of neuronal types. Yet our knowledge concerning the diversity of neuronal morphologies, in particular distal axonal projection patterns, is extremely limited. To systematically obtain single neuron full morphology on a brain-wide scale, we established a platform with five major components: sparse labeling, whole-brain imaging, reconstruction, registration, and classification. We achieved sparse, robust and consistent fluorescent labeling of a wide range of neuronal types by combining transgenic or viral Cre delivery with novel transgenic reporter lines. We acquired high-resolution whole-brain fluorescent images from a large set of sparsely labeled brains using fluorescence micro-optical sectioning tomography (fMOST). We developed a set of software tools for efficient large-volume image data processing, registration to the Allen Mouse Brain Common Coordinate Framework (CCF), and computer-assisted morphological reconstruction. We reconstructed and analyzed the complete morphologies of 1,708 neurons from the striatum, thalamus, cortex and claustrum. Finally, we classified these cells into multiple morphological and projection types and identified a set of region-specific organizational rules of long-range axonal projections at the single cell level. Specifically, different neuron types from different regions follow highly distinct rules in convergent or divergent projection, feedforward or feedback axon termination patterns, and between-cell homogeneity or heterogeneity. Major molecularly defined classes or types of neurons have correspondingly distinct morphological and projection patterns, however, we also identify further remarkably extensive morphological and projection diversity at more fine-grained levels within the major types that cannot presently be accounted for by preexisting transcriptomic subtypes. These insights reinforce the importance of full morphological characterization of brain cell types and suggest a plethora of ways different cell types and individual neurons may contribute to the function of their respective circuits.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version of the manuscript has been revised to correct a typo in the title.

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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Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types
Hanchuan Peng, Peng Xie, Lijuan Liu, Xiuli Kuang, Yimin Wang, Lei Qu, Hui Gong, Shengdian Jiang, Anan Li, Zongcai Ruan, Liya Ding, Chao Chen, Mengya Chen, Tanya L. Daigle, Zhangcan Ding, Yanjun Duan, Aaron Feiner, Ping He, Chris Hill, Karla E. Hirokawa, Guodong Hong, Lei Huang, Sara Kebede, Hsien-Chi Kuo, Rachael Larsen, Phil Lesnar, Longfei Li, Qi Li, Xiangning Li, Yaoyao Li, Yuanyuan Li, An Liu, Donghuan Lu, Stephanie Mok, Lydia Ng, Thuc Nghi Nguyen, Qiang Ouyang, Jintao Pan, Elise Shen, Yuanyuan Song, Susan M. Sunkin, Bosiljka Tasic, Matthew B. Veldman, Wayne Wakeman, Wan Wan, Peng Wang, Quanxin Wang, Tao Wang, Yaping Wang, Feng Xiong, Wei Xiong, Wenjie Xu, Zizhen Yao, Min Ye, Lulu Yin, Yang Yu, Jia Yuan, Jing Yuan, Zhixi Yun, Shaoqun Zeng, Shichen Zhang, Sujun Zhao, Zijun Zhao, Zhi Zhou, Z. Josh Huang, Luke Esposito, Michael J. Hawrylycz, Staci A. Sorensen, X. William Yang, Yefeng Zheng, Zhongze Gu, Wei Xie, Christof Koch, Qingming Luo, Julie A. Harris, Yun Wang, Hongkui Zeng
bioRxiv 675280; doi: https://doi.org/10.1101/675280
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Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types
Hanchuan Peng, Peng Xie, Lijuan Liu, Xiuli Kuang, Yimin Wang, Lei Qu, Hui Gong, Shengdian Jiang, Anan Li, Zongcai Ruan, Liya Ding, Chao Chen, Mengya Chen, Tanya L. Daigle, Zhangcan Ding, Yanjun Duan, Aaron Feiner, Ping He, Chris Hill, Karla E. Hirokawa, Guodong Hong, Lei Huang, Sara Kebede, Hsien-Chi Kuo, Rachael Larsen, Phil Lesnar, Longfei Li, Qi Li, Xiangning Li, Yaoyao Li, Yuanyuan Li, An Liu, Donghuan Lu, Stephanie Mok, Lydia Ng, Thuc Nghi Nguyen, Qiang Ouyang, Jintao Pan, Elise Shen, Yuanyuan Song, Susan M. Sunkin, Bosiljka Tasic, Matthew B. Veldman, Wayne Wakeman, Wan Wan, Peng Wang, Quanxin Wang, Tao Wang, Yaping Wang, Feng Xiong, Wei Xiong, Wenjie Xu, Zizhen Yao, Min Ye, Lulu Yin, Yang Yu, Jia Yuan, Jing Yuan, Zhixi Yun, Shaoqun Zeng, Shichen Zhang, Sujun Zhao, Zijun Zhao, Zhi Zhou, Z. Josh Huang, Luke Esposito, Michael J. Hawrylycz, Staci A. Sorensen, X. William Yang, Yefeng Zheng, Zhongze Gu, Wei Xie, Christof Koch, Qingming Luo, Julie A. Harris, Yun Wang, Hongkui Zeng
bioRxiv 675280; doi: https://doi.org/10.1101/675280

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