Learning shapes the aversion and reward responses of lateral habenula neurons

  1. Daqing Wang
  2. Yi Li
  3. Qiru Feng
  4. Qingchun Guo
  5. Jingfeng Zhou
  6. Minmin Luo  Is a corresponding author
  1. Tsinghua University, China
  2. National Institute of Biological Sciences, China

Abstract

The lateral habenula (LHb) is believed to encode negative motivational values. It remains unknown how LHb neurons respond to various stressors and how learning shapes their responses. Here, we used fiber-photometry and electrophysiology to track LHb neuronal activity in freely-behaving mice. Bitterness, pain, and social attack by aggressors intensively excite LHb neurons. Aversive Pavlovian conditioning induced activation by the aversion-predicting cue in a few trials. The experience of social defeat also conditioned excitatory responses to previously neutral social stimuli. In contrast, fiber photometry and signle-unit recordings revealed that sucrose reward inhibited LHb neurons and often produced excitatory rebound. It required prolonged conditioning and high reward probability to induce inhibition by reward-predicting cues. Therefore, LHb neurons can bidirectionally process a diverse array of aversive and reward signals. Importantly, their responses are dynamically shaped by learning, suggesting that the LHb participates in experience-dependent selection of behavioral responses to stressors and rewards.

Article and author information

Author details

  1. Daqing Wang

    School of Life Sciences, Tsinghua University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8132-3976
  2. Yi Li

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Qiru Feng

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Qingchun Guo

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Jingfeng Zhou

    National Institute of Biological Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Minmin Luo

    School of Life Sciences, Tsinghua University, Beijing, China
    For correspondence
    luominmin@nibs.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3535-6624

Funding

National Natural Science Foundation of China (91432114)

  • Minmin Luo

Ministry of Science and Technology of the People's Republic of China (2012YQ03026005)

  • Minmin Luo

The Beijing Municipal Government

  • Minmin Luo

National Natural Science Foundation of China (91632302)

  • Minmin Luo

Ministry of Science and Technology of the People's Republic of China (2013ZX0950910)

  • Minmin Luo

Ministry of Science and Technology of the People's Republic of China (2015BAI08B02)

  • Minmin Luo

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

Ethics

Animal experimentation: Animal care and use followed the institutional guidelines of the National Institute of Biological Sciences (NIBS), Beijing (Approval ID: NIBSLuoM15C) and the Regulations for the Administration of Affairs Concerning Experimental Animals of China.

Reviewing Editor

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

Publication history

  1. Received: November 7, 2016
  2. Accepted: May 30, 2017
  3. Accepted Manuscript published: May 31, 2017 (version 1)
  4. Accepted Manuscript updated: June 3, 2017 (version 2)
  5. Version of Record published: June 13, 2017 (version 3)

Copyright

© 2017, Wang 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. Daqing Wang
  2. Yi Li
  3. Qiru Feng
  4. Qingchun Guo
  5. Jingfeng Zhou
  6. Minmin Luo
(2017)
Learning shapes the aversion and reward responses of lateral habenula neurons
eLife 6:e23045.
https://doi.org/10.7554/eLife.23045

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