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Morphological diversity of single neurons in molecularly defined cell types

Author

Listed:
  • Hanchuan Peng

    (Allen Institute for Brain Science
    Southeast University)

  • Peng Xie

    (Southeast University)

  • Lijuan Liu

    (Southeast University
    Southeast University)

  • Xiuli Kuang

    (Wenzhou Medical University)

  • Yimin Wang

    (Southeast University
    Shanghai University)

  • Lei Qu

    (Southeast University
    Anhui University)

  • Hui Gong

    (Huazhong University of Science and Technology
    HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics)

  • Shengdian Jiang

    (Southeast University)

  • Anan Li

    (Huazhong University of Science and Technology
    HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics)

  • Zongcai Ruan

    (Southeast University)

  • Liya Ding

    (Southeast University)

  • Zizhen Yao

    (Allen Institute for Brain Science)

  • Chao Chen

    (Wenzhou Medical University)

  • Mengya Chen

    (Shanghai University)

  • Tanya L. Daigle

    (Allen Institute for Brain Science)

  • Rachel Dalley

    (Allen Institute for Brain Science)

  • Zhangcan Ding

    (Southeast University)

  • Yanjun Duan

    (Southeast University)

  • Aaron Feiner

    (Allen Institute for Brain Science)

  • Ping He

    (Shanghai University)

  • Chris Hill

    (Allen Institute for Brain Science)

  • Karla E. Hirokawa

    (Allen Institute for Brain Science
    Cajal Neuroscience)

  • Guodong Hong

    (Southeast University
    Southeast University)

  • Lei Huang

    (Southeast University)

  • Sara Kebede

    (Allen Institute for Brain Science)

  • Hsien-Chi Kuo

    (Allen Institute for Brain Science)

  • Rachael Larsen

    (Allen Institute for Brain Science)

  • Phil Lesnar

    (Allen Institute for Brain Science)

  • Longfei Li

    (Anhui University)

  • Qi Li

    (Shanghai University)

  • Xiangning Li

    (Huazhong University of Science and Technology
    HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics)

  • Yaoyao Li

    (Wenzhou Medical University)

  • Yuanyuan Li

    (Anhui University)

  • An Liu

    (Southeast University
    Southeast University)

  • Donghuan Lu

    (Tencent Jarvis Lab)

  • Stephanie Mok

    (Allen Institute for Brain Science)

  • Lydia Ng

    (Allen Institute for Brain Science)

  • Thuc Nghi Nguyen

    (Allen Institute for Brain Science
    Cajal Neuroscience)

  • Qiang Ouyang

    (Southeast University)

  • Jintao Pan

    (Southeast University)

  • Elise Shen

    (Allen Institute for Brain Science)

  • Yuanyuan Song

    (Southeast University)

  • Susan M. Sunkin

    (Allen Institute for Brain Science)

  • Bosiljka Tasic

    (Allen Institute for Brain Science)

  • Matthew B. Veldman

    (University of California, Los Angeles)

  • Wayne Wakeman

    (Allen Institute for Brain Science)

  • Wan Wan

    (Anhui University)

  • Peng Wang

    (Shanghai University)

  • Quanxin Wang

    (Allen Institute for Brain Science)

  • Tao Wang

    (Anhui University)

  • Yaping Wang

    (Southeast University)

  • Feng Xiong

    (Southeast University)

  • Wei Xiong

    (Wenzhou Medical University)

  • Wenjie Xu

    (Allen Institute for Brain Science)

  • Min Ye

    (Wenzhou Medical University)

  • Lulu Yin

    (Southeast University)

  • Yang Yu

    (Allen Institute for Brain Science)

  • Jia Yuan

    (Southeast University
    Southeast University)

  • Jing Yuan

    (Huazhong University of Science and Technology
    HUST-Suzhou Institute for Brainsmatics, JITRI Institute for Brainsmatics)

  • Zhixi Yun

    (Southeast University)

  • Shaoqun Zeng

    (Huazhong University of Science and Technology)

  • Shichen Zhang

    (Southeast University)

  • Sujun Zhao

    (Southeast University)

  • Zijun Zhao

    (Southeast University)

  • Zhi Zhou

    (Allen Institute for Brain Science)

  • Z. Josh Huang

    (Cold Spring Harbor Laboratory
    Duke University School of Medicine)

  • Luke Esposito

    (Allen Institute for Brain Science)

  • Michael J. Hawrylycz

    (Allen Institute for Brain Science)

  • Staci A. Sorensen

    (Allen Institute for Brain Science)

  • X. William Yang

    (University of California, Los Angeles)

  • Yefeng Zheng

    (Tencent Jarvis Lab)

  • Zhongze Gu

    (Southeast University)

  • Wei Xie

    (Southeast University
    Southeast University)

  • Christof Koch

    (Allen Institute for Brain Science)

  • Qingming Luo

    (Huazhong University of Science and Technology
    Hainan University)

  • Julie A. Harris

    (Allen Institute for Brain Science
    Cajal Neuroscience)

  • Yun Wang

    (Allen Institute for Brain Science)

  • Hongkui Zeng

    (Allen Institute for Brain Science)

Abstract

Dendritic and axonal morphology reflects the input and output of neurons and is a defining feature of neuronal types1,2, yet our knowledge of its diversity remains limited. Here, to systematically examine complete single-neuron morphologies on a brain-wide scale, we established a pipeline encompassing sparse labelling, whole-brain imaging, reconstruction, registration and analysis. We fully reconstructed 1,741 neurons from cortex, claustrum, thalamus, striatum and other brain regions in mice. We identified 11 major projection neuron types with distinct morphological features and corresponding transcriptomic identities. Extensive projectional diversity was found within each of these major types, on the basis of which some types were clustered into more refined subtypes. This diversity follows a set of generalizable principles that govern long-range axonal projections at different levels, including molecular correspondence, divergent or convergent projection, axon termination pattern, regional specificity, topography, and individual cell variability. Although clear concordance with transcriptomic profiles is evident at the level of major projection type, fine-grained morphological diversity often does not readily correlate with transcriptomic subtypes derived from unsupervised clustering, highlighting the need for single-cell cross-modality studies. Overall, our study demonstrates the crucial need for quantitative description of complete single-cell anatomy in cell-type classification, as single-cell morphological diversity reveals a plethora of ways in which different cell types and their individual members may contribute to the configuration and function of their respective circuits.

Suggested Citation

  • Hanchuan Peng & Peng Xie & Lijuan Liu & Xiuli Kuang & Yimin Wang & Lei Qu & Hui Gong & Shengdian Jiang & Anan Li & Zongcai Ruan & Liya Ding & Zizhen Yao & Chao Chen & Mengya Chen & Tanya L. Daigle & R, 2021. "Morphological diversity of single neurons in molecularly defined cell types," Nature, Nature, vol. 598(7879), pages 174-181, October.
  • Handle: RePEc:nat:nature:v:598:y:2021:i:7879:d:10.1038_s41586-021-03941-1
    DOI: 10.1038/s41586-021-03941-1
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    Citations

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    Cited by:

    1. Olga Gliko & Matt Mallory & Rachel Dalley & Rohan Gala & James Gornet & Hongkui Zeng & Staci A. Sorensen & Uygar Sümbül, 2024. "High-throughput analysis of dendrite and axonal arbors reveals transcriptomic correlates of neuroanatomy," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Zengpeng Han & Nengsong Luo & Wenyu Ma & Xiaodong Liu & Yuxiang Cai & Jiaxin Kou & Jie Wang & Lei Li & Siqi Peng & Zihong Xu & Wen Zhang & Yuxiang Qiu & Yang Wu & Chaohui Ye & Kunzhang Lin & Fuqiang X, 2023. "AAV11 enables efficient retrograde targeting of projection neurons and enhances astrocyte-directed transduction," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Marcus N. Leiwe & Satoshi Fujimoto & Toshikazu Baba & Daichi Moriyasu & Biswanath Saha & Richi Sakaguchi & Shigenori Inagaki & Takeshi Imai, 2024. "Automated neuronal reconstruction with super-multicolour Tetbow labelling and threshold-based clustering of colour hues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Zhenjia Chen & Zhenyuan Lin & Ji Yang & Cong Chen & Di Liu & Liuting Shan & Yuanyuan Hu & Tailiang Guo & Huipeng Chen, 2024. "Cross-layer transmission realized by light-emitting memristor for constructing ultra-deep neural network with transfer learning ability," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. Chen-Rui Xia & Zhi-Jie Cao & Xin-Ming Tu & Ge Gao, 2023. "Spatial-linked alignment tool (SLAT) for aligning heterogenous slices," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Diek W. Wheeler & Shaina Banduri & Sruthi Sankararaman & Samhita Vinay & Giorgio A. Ascoli, 2024. "Unsupervised classification of brain-wide axons reveals the presubiculum neuronal projection blueprint," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Ioannis Mantas & Ivana Flais & Yuvarani Masarapu & Tudor Ionescu & Solène Frapard & Felix Jung & Pierre Merre & Marcus Saarinen & Katarina Tiklova & Behzad Yaghmaeian Salmani & Linda Gillberg & Xiaoqu, 2024. "Claustrum and dorsal endopiriform cortex complex cell-identity is determined by Nurr1 and regulates hallucinogenic-like states in mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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