Acetic acid activates distinct taste pathways in Drosophila to elicit opposing, state-dependent feeding responses

• Type of Material: Article
• Authors: Anita V. Devineni, Emory University; Bei Sun, Columbia University; Anna Zhukovskaya, Columbia University; Richard Axel, Columbia University
• Language: English
• Date: 2019-06-17
• Publisher: eLife Sciences Publications Ltd.
• Publication Version: Final Published Version
• Copyright Statement: © 2019, Devineni et al
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): https://doi.org/10.7554/eLife.47677
• Title of Journal or Parent Work: eLife
• Volume: 8
• Start Page: e47677
• Grant/Funding Agency: Howard Hughes Medical Institute to Richard Axel.; Simons Foundation 54951 to Richard Axel.
• Grant/Funding Information: The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
• Keywords: Drosophila melanogaster; metabolic resource; taste circuit; aversive response; acetic acid; toxicity; appetitive response
• Research Categories: Genetics; Nutrition; Toxicology

Abstract

Taste circuits are genetically determined to elicit an innate appetitive or aversive response, ensuring that animals consume nutritious foods and avoid the ingestion of toxins. We have examined the response of Drosophila melanogaster to acetic acid, a tastant that can be a metabolic resource but can also be toxic to the fly. Our data reveal that flies accommodate these conflicting attributes of acetic acid by virtue of a hunger-dependent switch in their behavioral response to this stimulus. Fed flies show taste aversion to acetic acid, whereas starved flies show a robust appetitive response. These opposing responses are mediated by two different classes of taste neurons, the sugar- and bitter-sensing neurons. Hunger shifts the behavioral response from aversion to attraction by enhancing the appetitive sugar pathway as well as suppressing the aversive bitter pathway. Thus a single tastant can drive opposing behaviors by activating distinct taste pathways modulated by internal state.