Transcriptomic encoding of sensorimotor transformation in the midbrain

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,...

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Main Authors: Zhiyong Xie, Mengdi Wang, Zeyuan Liu, Congping Shang, Changjiang Zhang, Le Sun, Huating Gu, Gengxin Ran, Qing Pei, Qiang Ma, Meizhu Huang, Junjing Zhang, Rui Lin, Youtong Zhou, Jiyao Zhang, Miao Zhao, Minmin Luo, Qian Wu, Peng Cao, Xiaoqun Wang
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/69825
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author Zhiyong Xie
Mengdi Wang
Zeyuan Liu
Congping Shang
Changjiang Zhang
Le Sun
Huating Gu
Gengxin Ran
Qing Pei
Qiang Ma
Meizhu Huang
Junjing Zhang
Rui Lin
Youtong Zhou
Jiyao Zhang
Miao Zhao
Minmin Luo
Qian Wu
Peng Cao
Xiaoqun Wang
author_facet Zhiyong Xie
Mengdi Wang
Zeyuan Liu
Congping Shang
Changjiang Zhang
Le Sun
Huating Gu
Gengxin Ran
Qing Pei
Qiang Ma
Meizhu Huang
Junjing Zhang
Rui Lin
Youtong Zhou
Jiyao Zhang
Miao Zhao
Minmin Luo
Qian Wu
Peng Cao
Xiaoqun Wang
author_sort Zhiyong Xie
collection DOAJ
description 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 expressed discrete marker genes. Of particular interest, Cbln2 and Pitx2 were 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 mediated 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.
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spelling doaj.art-f42a6fea9b044ddd91d7f048786a77102022-12-22T03:24:45ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.69825Transcriptomic encoding of sensorimotor transformation in the midbrainZhiyong Xie0https://orcid.org/0000-0002-5691-3357Mengdi Wang1https://orcid.org/0000-0002-0214-2913Zeyuan Liu2https://orcid.org/0000-0003-0007-9874Congping Shang3Changjiang Zhang4Le Sun5Huating Gu6Gengxin Ran7Qing Pei8Qiang Ma9Meizhu Huang10Junjing Zhang11Rui Lin12Youtong Zhou13Jiyao Zhang14Miao Zhao15Minmin Luo16https://orcid.org/0000-0003-3535-6624Qian Wu17https://orcid.org/0000-0002-7469-1583Peng Cao18https://orcid.org/0000-0001-7739-6857Xiaoqun Wang19https://orcid.org/0000-0003-3440-2617National Institute of Biological Sciences, Beijing, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, ChinaBioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, ChinaBeijing Institute for Brain Disorders, Capital Medical University, Beijing, ChinaNational Institute of Biological Sciences, Beijing, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, ChinaNational Institute of Biological Sciences, Beijing, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, ChinaBioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, ChinaState Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, ChinaNational Institute of Biological Sciences, Beijing, ChinaNational Institute of Biological Sciences, Beijing, ChinaState Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, ChinaNational Institute of Biological Sciences, Beijing, ChinaNational Institute of Biological Sciences, Beijing, China; Chinese Institute for Brain Research, Beijing, ChinaState Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, ChinaNational Institute of Biological Sciences, Beijing, China; Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, ChinaState 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, China; University of Chinese Academy of Sciences, Beijing, China; Bioland Laboratory (Guangzhou Regenerative Medicine and Health Guangdong Laboratory), Guangzhou, China; Beijing Institute for Brain Disorders, Capital Medical University, Beijing, China; Chinese Institute for Brain Research, Beijing, China; Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Beihang University & Capital Medical University, Beijing, ChinaSensorimotor 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 expressed discrete marker genes. Of particular interest, Cbln2 and Pitx2 were 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 mediated 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.https://elifesciences.org/articles/69825superior colliculussensorimotor transformationsingle-cell transcriptomeCbln2Pitx2
spellingShingle Zhiyong Xie
Mengdi Wang
Zeyuan Liu
Congping Shang
Changjiang Zhang
Le Sun
Huating Gu
Gengxin Ran
Qing Pei
Qiang Ma
Meizhu Huang
Junjing Zhang
Rui Lin
Youtong Zhou
Jiyao Zhang
Miao Zhao
Minmin Luo
Qian Wu
Peng Cao
Xiaoqun Wang
Transcriptomic encoding of sensorimotor transformation in the midbrain
eLife
superior colliculus
sensorimotor transformation
single-cell transcriptome
Cbln2
Pitx2
title Transcriptomic encoding of sensorimotor transformation in the midbrain
title_full Transcriptomic encoding of sensorimotor transformation in the midbrain
title_fullStr Transcriptomic encoding of sensorimotor transformation in the midbrain
title_full_unstemmed Transcriptomic encoding of sensorimotor transformation in the midbrain
title_short Transcriptomic encoding of sensorimotor transformation in the midbrain
title_sort transcriptomic encoding of sensorimotor transformation in the midbrain
topic superior colliculus
sensorimotor transformation
single-cell transcriptome
Cbln2
Pitx2
url https://elifesciences.org/articles/69825
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