PBN-PVT projections modulate negative affective states in mice

  1. Ya-Bing Zhu
  2. Yan Wang
  3. Xiao-Xiao Hua
  4. Ling Xu
  5. Ming-Zhe Liu
  6. Rui Zhang
  7. Peng-Fei Liu
  8. Jin-Bao Li
  9. Ling Zhang  Is a corresponding author
  10. Di Mu  Is a corresponding author
  1. Shanghai Jiao Tong University School of Medicine, China
  2. Tongji University School of Medicine, China
  3. The First Affiliated Hospital of Guangzhou Medical University, China

Abstract

Long-lasting negative affections dampen enthusiasm for life, and dealing with negative affective states is essential for individual survival. The parabrachial nucleus (PBN) and thalamic paraventricular nucleus (PVT) are critical for modulating affective states in mice. However, the functional roles of PBN-PVT projections in modulating affective states remain elusive. Here, we show that PBN neurons send dense projection fibers to the PVT and form direct excitatory synapses with PVT neurons. Activation of the PBN-PVT pathway induces robust behaviors associated with negative affective states without affecting nociceptive behaviors. Inhibition of the PBN-PVT pathway reduces aversion-like and fear-like behaviors. Furthermore, the PVT neurons innervated by the PBN are activated by aversive stimulation, and activation of PBN-PVT projections enhances the neuronal activity of PVT neurons in response to the aversive stimulus. Consistently, activation of PVT neurons that received PBN-PVT projections induces anxiety-like behaviors. Thus, our study indicates that PBN-PVT projections modulate negative affective states in mice.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file. The behavioral data and imaging analysis results have been made available on Dryad Digital Repository (https://doi:10.5061/dryad.1rn8pk0w4). All MATLAB code has been deposited at: https://github.com/laizishangalali/Xiang/blob/main/zscore_KS_test.m and is publicly available.

The following data sets were generated

Article and author information

Author details

  1. Ya-Bing Zhu

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Yan Wang

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xiao-Xiao Hua

    Tongji University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Ling Xu

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ming-Zhe Liu

    Department of Respiratory, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Rui Zhang

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Peng-Fei Liu

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Jin-Bao Li

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Ling Zhang

    Tongji University School of Medicine, Shanghai, China
    For correspondence
    lzhang0808@tongji.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  10. Di Mu

    Department of Anesthesiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China
    For correspondence
    damonmu@163.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1209-9311

Funding

National Natural Science Foundation of China (31900717)

  • Di Mu

China Association for Science and Technology (2019QNRC001)

  • Di Mu

Shanghai Association for Science and Technology (19YF1438700)

  • Di Mu

National Natural Science Foundation of China (31571086)

  • Ling Zhang

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

Reviewing Editor

  1. Mario Penzo, National Institute of Mental Health, United States

Ethics

Animal experimentation: All animal experiment procedures were approved by the Animal Care and Use Committee of Shanghai General Hospital (2019AW008).

Version history

  1. Preprint posted: March 12, 2021 (view preprint)
  2. Received: March 13, 2021
  3. Accepted: January 30, 2022
  4. Accepted Manuscript published: February 15, 2022 (version 1)
  5. Version of Record published: March 17, 2022 (version 2)

Copyright

© 2022, Zhu 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. Ya-Bing Zhu
  2. Yan Wang
  3. Xiao-Xiao Hua
  4. Ling Xu
  5. Ming-Zhe Liu
  6. Rui Zhang
  7. Peng-Fei Liu
  8. Jin-Bao Li
  9. Ling Zhang
  10. Di Mu
(2022)
PBN-PVT projections modulate negative affective states in mice
eLife 11:e68372.
https://doi.org/10.7554/eLife.68372

Share this article

https://doi.org/10.7554/eLife.68372

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