Immediate perception of a reward is distinct from the reward's long-term salience

  1. John P McGinnis
  2. Huoqing Jiang
  3. Moutaz Ali Agha
  4. Consuelo Perez Sanchez
  5. Jeffrey J Lange
  6. Zulin Yu
  7. Frederic Marion-Poll
  8. Kausik Si  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
  2. Evolution, Génomes, Comportement & Ecologie, CNRS, IRD, Université Paris-Sud, Université Paris-Saclay Gif-sur-Yvette, France

Abstract

Reward perception guides all aspects of animal behavior. However, the relationship between the perceived value of a reward, the latent value of a reward, and the behavioral response remains unclear. Here we report that, given a choice between two sweet and chemically similar sugars-L- and D-arabinose-Drosophila melanogaster prefers D- over L-arabinose, but forms long-term memories of L-arabinose (the isomer present in ripening fruits) more reliably. Behavioral assays indicate that L-arabinose-generated memories require sugar receptor Gr43a, and calcium imaging and electrophysiological recording indicate that L- and D-arabinose differentially activate Gr43a-expressing neurons. We posit that the immediate valence of a reward is not always predictive of the long-term reinforcement value of that reward, and that a subset of sugar-sensing neurons may generate distinct representations of similar sugars, allowing for rapid assessment of the salient features of various sugar rewards and generation of reward-specific behaviors. However, how sensory neurons communicate information about L-arabinose quality and concentration-features relevant for long-term memory-remains unknown.

Article and author information

Author details

  1. John P McGinnis

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Huoqing Jiang

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Moutaz Ali Agha

    Evolution, Génomes, Comportement & Ecologie, CNRS, IRD, Université Paris-Sud, Université Paris-Saclay Gif-sur-Yvette, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Consuelo Perez Sanchez

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jeffrey J Lange

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Zulin Yu

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Frederic Marion-Poll

    Evolution, Génomes, Comportement & Ecologie, CNRS, IRD, Université Paris-Sud, Université Paris-Saclay Gif-sur-Yvette, Gif-sur-Yvette, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Kausik Si

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    ksi@stowers.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9613-6273

Funding

Stowers Institute for Medical Research (SIMR funding)

  • Kausik Si

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: October 11, 2016
  2. Accepted: December 16, 2016
  3. Accepted Manuscript published: December 22, 2016 (version 1)
  4. Version of Record published: January 18, 2017 (version 2)

Copyright

© 2016, McGinnis 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. John P McGinnis
  2. Huoqing Jiang
  3. Moutaz Ali Agha
  4. Consuelo Perez Sanchez
  5. Jeffrey J Lange
  6. Zulin Yu
  7. Frederic Marion-Poll
  8. Kausik Si
(2016)
Immediate perception of a reward is distinct from the reward's long-term salience
eLife 5:e22283.
https://doi.org/10.7554/eLife.22283

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