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.

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.

Metrics

  • 6,162
    views
  • 1,530
    downloads
  • 116
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.23045

Further reading

    1. Neuroscience
    Hans Martin Kjer, Mariam Andersson ... Tim B Dyrby
    Research Article

    We used diffusion MRI and x-ray synchrotron imaging on monkey and mice brains to examine the organisation of fibre pathways in white matter across anatomical scales. We compared the structure in the corpus callosum and crossing fibre regions and investigated the differences in cuprizone-induced demyelination in mouse brains versus healthy controls. Our findings revealed common principles of fibre organisation that apply despite the varying patterns observed across species; small axonal fasciculi and major bundles formed laminar structures with varying angles, according to the characteristics of major pathways. Fasciculi exhibited non-straight paths around obstacles like blood vessels, comparable across the samples of varying fibre complexity and demyelination. Quantifications of fibre orientation distributions were consistent across anatomical length scales and modalities, whereas tissue anisotropy had a more complex relationship, both dependent on the field-of-view. Our study emphasises the need to balance field-of-view and voxel size when characterising white matter features across length scales.

    1. Neuroscience
    Paul I Jaffe, Gustavo X Santiago-Reyes ... Russell A Poldrack
    Research Article

    Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.