Long-range projection neurons in the taste circuit of Drosophila

  1. Heesoo Kim  Is a corresponding author
  2. Colleen Kirkhart
  3. Kristin Scott  Is a corresponding author
  1. University of California, Berkeley, United States
  2. University of California, Berkeley, Berkeley, United States

Abstract

Taste compounds elicit innate feeding behaviors and act as rewards or punishments to entrain other cues. The neural pathways by which taste compounds influence innate and learned behaviors have not been resolved. Here, we identify three classes of taste projection neurons (TPNs) in Drosophila melanogaster distinguished by their morphology and taste selectivity. TPNs receive input from gustatory receptor neurons and respond selectively to sweet or bitter stimuli, demonstrating segregated processing of different taste modalities. Activation of TPNs influences innate feeding behavior, whereas inhibition has little effect, suggesting parallel pathways. Moreover, two TPN classes are absolutely required for conditioned taste aversion, a learned behavior. The TPNs essential for conditioned aversion project to the superior lateral protocerebrum (SLP) and convey taste information to mushroom body learning centers. These studies identify taste pathways from sensory detection to higher brain that influence innate behavior and are essential for learned responses to taste compounds.

Article and author information

Author details

  1. Heesoo Kim

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    heesoo@berkeley.edu
    Competing interests
    No competing interests declared.
  2. Colleen Kirkhart

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  3. Kristin Scott

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, Berkeley, United States
    For correspondence
    kscott@berkeley.edu
    Competing interests
    Kristin Scott, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3150-7210

Funding

National Institute of Dental and Craniofacial Research (DC013280)

  • Kristin Scott

National Science Foundation

  • Colleen Kirkhart

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

Reviewing Editor

  1. Hugo J Bellen, Baylor College of Medicine, United States

Version history

  1. Received: November 16, 2016
  2. Accepted: February 6, 2017
  3. Accepted Manuscript published: February 6, 2017 (version 1)
  4. Version of Record published: February 15, 2017 (version 2)

Copyright

© 2017, Kim 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

  • 5,049
    views
  • 1,088
    downloads
  • 68
    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. Heesoo Kim
  2. Colleen Kirkhart
  3. Kristin Scott
(2017)
Long-range projection neurons in the taste circuit of Drosophila
eLife 6:e23386.
https://doi.org/10.7554/eLife.23386

Share this article

https://doi.org/10.7554/eLife.23386

Further reading

    1. Neuroscience
    Ivan Tomić, Paul M Bays
    Research Article

    Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.

    1. Neuroscience
    Emilio Salinas, Bashirul I Sheikh
    Insight

    Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.