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A Brainstem reticulotegmental neural ensemble drives acoustic startle reflexes

Author

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  • Weiwei Guo

    (University of Science and Technology of China)

  • Sijia Fan

    (University of Science and Technology of China)

  • Dan Xiao

    (University of Science and Technology of China)

  • Hui Dong

    (Peking University School of Life Sciences)

  • Guangwei Xu

    (University of Science and Technology of China)

  • Zhikun Wan

    (University of Science and Technology of China)

  • Yuqian Ma

    (University of Science and Technology of China)

  • Zhen Wang

    (Shanghai Jiao Tong University School of Medicine)

  • Tian Xue

    (University of Science and Technology of China
    Chinese Academy of Sciences)

  • Yifeng Zhou

    (University of Science and Technology of China)

  • Yulong Li

    (Peking University School of Life Sciences
    PKU-IDG–McGovern Institute for Brain Research)

  • Wei Xiong

    (University of Science and Technology of China
    Chinese Academy of Sciences)

Abstract

The reticulotegmental nucleus (RtTg) has long been recognized as a crucial component of brainstem reticular formation (RF). However, the function of RtTg and its related circuits remain elusive. Here, we report a role of the RtTg in startle reflex, a highly conserved innate defensive behaviour. Optogenetic activation of RtTg neurons evokes robust startle responses in mice. The glutamatergic neurons in the RtTg are significantly activated during acoustic startle reflexes (ASR). Chemogenetic inhibition of the RtTg glutamatergic neurons decreases the ASR amplitudes. Viral tracing reveals an ASR neural circuit that the cochlear nucleus carrying auditory information sends direct excitatory innervations to the RtTg glutamatergic neurons, which in turn project to spinal motor neurons. Together, our findings describe a functional role of RtTg and its related neural circuit in startle reflexes, and demonstrate how the RF connects auditory system with motor functions.

Suggested Citation

  • Weiwei Guo & Sijia Fan & Dan Xiao & Hui Dong & Guangwei Xu & Zhikun Wan & Yuqian Ma & Zhen Wang & Tian Xue & Yifeng Zhou & Yulong Li & Wei Xiong, 2021. "A Brainstem reticulotegmental neural ensemble drives acoustic startle reflexes," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26723-9
    DOI: 10.1038/s41467-021-26723-9
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    References listed on IDEAS

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    1. Maria Soledad Esposito & Paolo Capelli & Silvia Arber, 2014. "Brainstem nucleus MdV mediates skilled forelimb motor tasks," Nature, Nature, vol. 508(7496), pages 351-356, April.
    2. Yi Li & Weixin Zhong & Daqing Wang & Qiru Feng & Zhixiang Liu & Jingfeng Zhou & Chunying Jia & Fei Hu & Jiawei Zeng & Qingchun Guo & Ling Fu & Minmin Luo, 2016. "Serotonin neurons in the dorsal raphe nucleus encode reward signals," Nature Communications, Nature, vol. 7(1), pages 1-15, April.
    3. Leopoldo Petreanu & Tianyi Mao & Scott M. Sternson & Karel Svoboda, 2009. "The subcellular organization of neocortical excitatory connections," Nature, Nature, vol. 457(7233), pages 1142-1145, February.
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