Transcriptomic encoding of sensorimotor transformation in the midbrain

  1. Zhiyong Xie
  2. Mengdi Wang
  3. Zeyuan Liu
  4. Congping Shang
  5. Changjiang Zhang
  6. Le Sun
  7. Huating Gu
  8. Gengxin Ran
  9. Qing Pei
  10. Qiang Ma
  11. Meizhu Huang
  12. Junjing Zhang
  13. Rui Lin
  14. Youtong Zhou
  15. Jiyao Zhang
  16. Miao Zhao
  17. Minmin Luo
  18. Qian Wu  Is a corresponding author
  19. Peng Cao  Is a corresponding author
  20. Xiaoqun Wang  Is a corresponding author
  1. National Institute of Biological Sciences, China
  2. Institute of Biophysics, Chinese Academy of Sciences, China
  3. Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), China
  4. Capital Medical University, China
  5. Beijing Normal University, China
  6. National Institute of Biological Science, China
  7. National Institute of Biological Sciences, Beijing, China

Abstract

Sensorimotor transformation, a process that converts sensory stimuli into motor actions, is critical for the brain to initiate behaviors. Although the circuitry involved in sensorimotor transformation has been well delineated, the molecular logic behind this process remains poorly understood. Here, we performed high-throughput and circuit-specific single-cell transcriptomic analyses of neurons in the superior colliculus (SC), a midbrain structure implicated in early sensorimotor transformation. We found that SC neurons in distinct laminae express discrete marker genes. Of particular interest, Cbln2 and Pitx2 are key markers that define glutamatergic projection neurons in the optic nerve (Op) and intermediate gray (InG) layers, respectively. The Cbln2+ neurons responded to visual stimuli mimicking cruising predators, while the Pitx2+ neurons encoded prey-derived vibrissal tactile cues. By forming distinct input and output connections with other brain areas, these neuronal subtypes independently mediate behaviors of predator avoidance and prey capture. Our results reveal that, in the midbrain, sensorimotor transformation for different behaviors may be performed by separate circuit modules that are molecularly defined by distinct transcriptomic codes.

Data availability

The scRNA-seq data used in this study have been deposited in the Gene Expression Omnibus (GEO) under accession numbers GSE162404 (https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE162404).

The following data sets were generated

Article and author information

Author details

  1. Zhiyong Xie

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Mengdi Wang

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zeyuan Liu

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0007-9874
  4. Congping Shang

    Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Changjiang Zhang

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Le Sun

    Capital Medical University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Huating Gu

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Gengxin Ran

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Qing Pei

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Qiang Ma

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Meizhu Huang

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Junjing Zhang

    Beijing Normal University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Rui Lin

    National Institute of Biological Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Youtong Zhou

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Jiyao Zhang

    Beijing Normal University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  16. Miao Zhao

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  17. Minmin Luo

    National Institute of Biological Science, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3535-6624
  18. Qian Wu

    Beijing Normal University, Beijing, China
    For correspondence
    qianwu@ibp.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
  19. Peng Cao

    National Institute of Biological Sciences, Beijing, China
    For correspondence
    caopeng@nibs.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
  20. Xiaoqun Wang

    Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
    For correspondence
    xiaoqunwang@ibp.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3440-2617

Funding

Ministry of Science and Technology of the People's Republic of China (2019YFA0110100; 2017YFA0103303)

  • Xiaoqun Wang

Ministry of Science and Technology of the People's Republic of China (2017YFA0102601)

  • Qian Wu

Chinese Academy of Sciences (XDB32010100)

  • Xiaoqun Wang

National Natural Science Foundation of China (31925019)

  • Peng Cao

National Natural Science Foundation of China (31771140; 81891001)

  • Xiaoqun Wang

BUAA-CCMU Big Data and Precision Medicine Advanced Innovation Center Project (BHME-2019001)

  • Xiaoqun Wang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Ethics

Animal experimentation: All experimental procedures were conducted following protocols approved by the Administrative Panel on Laboratory Animal Care at the National Institute of Biological Sciences, Beijing (NIBS) (NIBS2021M0006) and Institute of Biophysics, Chinese Academy of Sciences (SYXK2019015).

Version history

  1. Received: April 27, 2021
  2. Preprint posted: April 28, 2021 (view preprint)
  3. Accepted: July 25, 2021
  4. Accepted Manuscript published: July 28, 2021 (version 1)
  5. Version of Record published: August 5, 2021 (version 2)

Copyright

© 2021, Xie et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Zhiyong Xie
  2. Mengdi Wang
  3. Zeyuan Liu
  4. Congping Shang
  5. Changjiang Zhang
  6. Le Sun
  7. Huating Gu
  8. Gengxin Ran
  9. Qing Pei
  10. Qiang Ma
  11. Meizhu Huang
  12. Junjing Zhang
  13. Rui Lin
  14. Youtong Zhou
  15. Jiyao Zhang
  16. Miao Zhao
  17. Minmin Luo
  18. Qian Wu
  19. Peng Cao
  20. Xiaoqun Wang
(2021)
Transcriptomic encoding of sensorimotor transformation in the midbrain
eLife 10:e69825.
https://doi.org/10.7554/eLife.69825

Share this article

https://doi.org/10.7554/eLife.69825

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