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Transcriptomic encoding of sensorimotor transformation in the midbrain

Zhiyong Xie, Mengdi Wang, Zeyuan Liu, Congping Shang, Changjiang Zhang, Le Sun, Huating Gu, Gengxin Ran, Qing Pei, Qiang Ma, Meizhu Huang, Junjing Zhang, Jiyao Zhang, Miao Zhao, Qian Wu, Peng Cao, Xiaoqun Wang
doi: https://doi.org/10.1101/2021.04.27.441692
Zhiyong Xie
1National Institute of Biological Sciences, Beijing 102206, China
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Mengdi Wang
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
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Zeyuan Liu
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
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Congping Shang
4Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, 510005, China
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Changjiang Zhang
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
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Le Sun
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
9Beijing Institute for Brain Disorders, Capital Medical University, Beijing 100069, China
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Huating Gu
1National Institute of Biological Sciences, Beijing 102206, China
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Gengxin Ran
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
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Qing Pei
1National Institute of Biological Sciences, Beijing 102206, China
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Qiang Ma
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
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Meizhu Huang
4Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, 510005, China
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Junjing Zhang
5State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
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Jiyao Zhang
5State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
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Miao Zhao
1National Institute of Biological Sciences, Beijing 102206, China
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Qian Wu
5State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
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  • For correspondence: [email protected] [email protected] [email protected]
Peng Cao
1National Institute of Biological Sciences, Beijing 102206, China
8Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing 100084, China
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  • For correspondence: [email protected] [email protected] [email protected]
Xiaoqun Wang
2State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
3University of Chinese Academy of Sciences, Beijing, 100049, China
4Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, 510005, China
6Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Beihang University & Capital Medical University, Beijing, 100069, China
7Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, Beijing, 100101, China
9Beijing Institute for Brain Disorders, Capital Medical University, Beijing 100069, China
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  • For correspondence: [email protected] [email protected] [email protected]
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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.

Competing Interest Statement

The authors have declared no competing interest.

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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Posted April 28, 2021.
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Transcriptomic encoding of sensorimotor transformation in the midbrain
Zhiyong Xie, Mengdi Wang, Zeyuan Liu, Congping Shang, Changjiang Zhang, Le Sun, Huating Gu, Gengxin Ran, Qing Pei, Qiang Ma, Meizhu Huang, Junjing Zhang, Jiyao Zhang, Miao Zhao, Qian Wu, Peng Cao, Xiaoqun Wang
bioRxiv 2021.04.27.441692; doi: https://doi.org/10.1101/2021.04.27.441692
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Transcriptomic encoding of sensorimotor transformation in the midbrain
Zhiyong Xie, Mengdi Wang, Zeyuan Liu, Congping Shang, Changjiang Zhang, Le Sun, Huating Gu, Gengxin Ran, Qing Pei, Qiang Ma, Meizhu Huang, Junjing Zhang, Jiyao Zhang, Miao Zhao, Qian Wu, Peng Cao, Xiaoqun Wang
bioRxiv 2021.04.27.441692; doi: https://doi.org/10.1101/2021.04.27.441692

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