Activation of the dopaminergic pathway from VTA to the medial olfactory tubercle generates odor-preference and reward

  1. Zhijian Zhang
  2. Qing Liu
  3. Pengjie Wen
  4. Jiaozhen Zhang
  5. Xiaoping Rao
  6. Ziming Zhou
  7. Hongruo Zhang
  8. Xiaobin He
  9. Juan Li
  10. Zheng Zhou
  11. Xiaoran Xu
  12. Xueyi Zhang
  13. Rui Luo
  14. Guanghui Lv
  15. Haohong Li
  16. Pei Cao
  17. Liping Wang
  18. Fuqiang Xu  Is a corresponding author
  1. Wuhan Institute of Physics and Mathematics, China
  2. Wuhan University, China
  3. Shenzhen Institutes of Advanced Technology, China
  4. Wuhan National Laboratory for Optoelectronics, China

Abstract

Odor-preferences are usually influenced by life experiences. However, the neural circuit mechanisms remain unclear. The medial olfactory tubercle (mOT) is involved in both reward and olfaction, while the ventral tegmental area (VTA) dopaminergic (DAergic) neurons are considered to be engaged in reward and motivation. Here, we found that the VTA (DAergic)-mOT pathway could be activated by different types of naturalistic rewards as well as odors in DAT-cre mice. Optogenetic activation of the VTA-mOT DAergic fibers was able to elicit preferences for space, location and neutral odor, while pharmacological blockade of the dopamine receptors in the mOT fully prevented the odor-preference formation. Furthermore, inactivation of the mOT-projecting VTA DAergic neurons eliminated the previously formed odor-preference and strongly affected the Go-no go learning efficiency. In summary, our results revealed that the VTA (DAergic)-mOT pathway mediates a variety of naturalistic reward processes and different types of preferences including odor-preference in mice.

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Author details

  1. Zhijian Zhang

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Qing Liu

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Pengjie Wen

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Jiaozhen Zhang

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Xiaoping Rao

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Ziming Zhou

    College of Life Sciences, Wuhan University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Hongruo Zhang

    College of Life Sciences, Wuhan University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Xiaobin He

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Juan Li

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Zheng Zhou

    CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Shenzhen, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Xiaoran Xu

    College of Life Sciences, Wuhan University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  12. Xueyi Zhang

    College of Life Sciences, Wuhan University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Rui Luo

    College of Life Sciences, Wuhan University, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  14. Guanghui Lv

    Wuhan National Laboratory for Optoelectronics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  15. Haohong Li

    Wuhan National Laboratory for Optoelectronics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  16. Pei Cao

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  17. Liping Wang

    CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Shenzhen, China
    Competing interests
    The authors declare that no competing interests exist.
  18. Fuqiang Xu

    Center for Brain Science, Wuhan Institute of Physics and Mathematics, Wuhan, China
    For correspondence
    fuqiang.xu@wipm.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4382-9797

Funding

Ministry of Science and Technology of the People's Republic of China (2015CB755600)

  • Fuqiang Xu

Chinese Academy of Sciences (XDB02050005)

  • Fuqiang Xu

National Natural Science Foundation of China (81661148053)

  • Fuqiang Xu

National Natural Science Foundation of China (91632303)

  • Fuqiang Xu

National Natural Science Foundation of China (31400945)

  • Qing Liu

National Natural Science Foundation of China (31400946)

  • Xiaoping Rao

National Natural Science Foundation of China (31400977)

  • Xiaobin He

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

Reviewing Editor

  1. Rui M Costa, Columbia University in the City of New York, United States

Ethics

Animal experimentation: All surgical and experimental procedures were conducted in accordance with the guidelines of the Animal Care and Use Committee at the Wuhan Institute of Physics and Mathematics, the Chinese Academy of Sciences (reference number: WIPM-(2014)39). All Animals were housed with their littermates in a dedicated housing room with a 12/12 h light/dark cycle. Food and water were available free unless specifically noted. During the surgery, every effort was made to minimize suffering.

Version history

  1. Received: January 24, 2017
  2. Accepted: December 15, 2017
  3. Accepted Manuscript published: December 18, 2017 (version 1)
  4. Version of Record published: January 22, 2018 (version 2)

Copyright

© 2017, Zhang 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. Zhijian Zhang
  2. Qing Liu
  3. Pengjie Wen
  4. Jiaozhen Zhang
  5. Xiaoping Rao
  6. Ziming Zhou
  7. Hongruo Zhang
  8. Xiaobin He
  9. Juan Li
  10. Zheng Zhou
  11. Xiaoran Xu
  12. Xueyi Zhang
  13. Rui Luo
  14. Guanghui Lv
  15. Haohong Li
  16. Pei Cao
  17. Liping Wang
  18. Fuqiang Xu
(2017)
Activation of the dopaminergic pathway from VTA to the medial olfactory tubercle generates odor-preference and reward
eLife 6:e25423.
https://doi.org/10.7554/eLife.25423

Share this article

https://doi.org/10.7554/eLife.25423

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