Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits

Abstract

The internal state of an organism influences its perception of attractive or aversive stimuli and thus promotes adaptive behaviors that increase its likelihood of survival. The mechanisms underlying these perceptual shifts are critical to our understanding of how neural circuits support animal cognition and behavior. Starved flies exhibit enhanced sensitivity to attractive odors and reduced sensitivity to aversive odors. Here, we show that a functional remodeling of the olfactory map is mediated by two parallel neuromodulatory systems that act in opposing directions on olfactory attraction and aversion at the level of the first synapse. Short neuropeptide F (sNPF) sensitizes an antennal lobe glomerulus wired for attraction, while tachykinin (DTK) suppresses activity of a glomerulus wired for aversion. Thus we show parallel neuromodulatory systems functionally reconfigure early olfactory processing to optimize detection of nutrients at the risk of ignoring potentially toxic food resources.

Article and author information

Author details

  1. Kang I Ko

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Cory M Root

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Scott A Lindsay

    Cell and Developmental Biology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Orel A Zaninovich

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Andrew K Shepherd

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Steven A Wasserman

    Cell and Developmental Biology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Susy M Kim

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jing W Wang

    Neurobiology Section, Division of Biological Sciences, University of California, San Diego, San Diego, United States
    For correspondence
    jw800@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Version history

  1. Received: April 23, 2015
  2. Accepted: July 24, 2015
  3. Accepted Manuscript published: July 24, 2015 (version 1)
  4. Version of Record published: August 11, 2015 (version 2)

Copyright

© 2015, Ko 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. Kang I Ko
  2. Cory M Root
  3. Scott A Lindsay
  4. Orel A Zaninovich
  5. Andrew K Shepherd
  6. Steven A Wasserman
  7. Susy M Kim
  8. Jing W Wang
(2015)
Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits
eLife 4:e08298.
https://doi.org/10.7554/eLife.08298

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https://doi.org/10.7554/eLife.08298