Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability

Abstract

Consolation is a common response to the distress of others in humans and some social animals, but the neural mechanisms underlying this behavior are not well characterized. By using socially monogamous mandarin voles, we found that optogenetic or chemogenetic inhibition of 5-HTergic neurons in the dorsal raphe nucleus (DR) or optogenetic inhibition of 5-HT terminals in the anterior cingulate cortex (ACC) significantly decreased allogrooming time in the consolation test and reduced sociability in the three-chamber test. The release of 5-HT within the ACC and the activity of DR neurons were significantly increased during allogrooming, sniffing and social approaching. Finally, we found that the activation of 5-HT1A receptors in the ACC was sufficient to reverse consolation and sociability deficits induced by the chemogenetic inhibition of 5-HTergic neurons in the DR. Our study provided first direct evidence that DR-ACC 5-HTergic neural circuit is implicated in consolation-like behaviors and sociability.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. We had also deposited the datasets of this manuscript into the Dyrad.

The following data sets were generated

Article and author information

Author details

  1. Laifu Li

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Li-Zi Zhang

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhi-Xiong He

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Huan Ma

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yu-Ting Zhang

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yu-Feng Xun

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Wei Yuan

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Wen-Juan Hou

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Yi-Tong Li

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Zi-Jian Lv

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Rui Jia

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Fa-Dao Tai

    College of Life Sciences, Shaanxi Normal University, Xi'an, China
    For correspondence
    taifadao@snnu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6804-4179

Funding

National Natural Science Foundation of China (31970424,31670421,31372213 and 31772473)

  • Fa-Dao Tai

Natural Science Basic Research Program of Shaanxi Province (2018JM3032)

  • Fa-Dao Tai

Fundamental Research Funds for the Central Universities (GK201903059)

  • Fa-Dao Tai

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

Ethics

Animal experimentation: All the breeding, housing, and experimental procedures in this study were in accordance with Chinese guidelines for the care and use of laboratory animals and were approved by the Animal Care and Use Committee of Shaanxi Normal University (SNNU_20190501001). All efforts were made to minimize suffering and the number of animals used during the studies.

Reviewing Editor

  1. Peggy Mason, University of Chicago, United States

Version history

  1. Received: February 17, 2021
  2. Accepted: June 2, 2021
  3. Accepted Manuscript published: June 3, 2021 (version 1)
  4. Version of Record published: June 18, 2021 (version 2)

Copyright

© 2021, Li 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. Laifu Li
  2. Li-Zi Zhang
  3. Zhi-Xiong He
  4. Huan Ma
  5. Yu-Ting Zhang
  6. Yu-Feng Xun
  7. Wei Yuan
  8. Wen-Juan Hou
  9. Yi-Tong Li
  10. Zi-Jian Lv
  11. Rui Jia
  12. Fa-Dao Tai
(2021)
Dorsal raphe nucleus to anterior cingulate cortex 5-HTergic neural circuit modulates consolation and sociability
eLife 10:e67638.
https://doi.org/10.7554/eLife.67638

Share this article

https://doi.org/10.7554/eLife.67638

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