Taste quality and hunger interactions in a feeding sensorimotor circuit

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Abstract

Taste detection and hunger state dynamically regulate the decision to initiate feeding. To study how context-appropriate feeding decisions are generated, we combined synaptic resolution circuit reconstruction with targeted genetic access to specific neurons to elucidate a gustatory sensorimotor circuit for feeding initiation in adult Drosophila melanogaster. This circuit connects gustatory sensory neurons to proboscis motor neurons through three intermediate layers. Most neurons in this pathway are necessary and sufficient for proboscis extension, a feeding initiation behavior, and respond selectively to sugar taste detection. Pathway activity is amplified by hunger signals that act at select second-order neurons to promote feeding initiation in food-deprived animals. In contrast, the feeding initiation circuit is inhibited by a bitter taste pathway that impinges on premotor neurons, illuminating a local motif that weighs sugar and bitter taste detection to adjust behavioral outcome. Together, these studies reveal central mechanisms for the integration of external taste detection and internal nutritive state to flexibly execute a critical feeding decision.

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All data is included in the manuscript or available at https://catmaid-fafb.virtualflybrain.org.

Article and author information

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Philip K Shiu

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Gabriella R Sterne

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

For correspondence
sternegr@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7221-648X
Stefanie Engert

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0644-8116
Barry J Dickson

Queensland Brain Institute, University of Queensland, Queensland, Australia

Competing interests
The authors declare that no competing interests exist.
Kristin Scott

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

For correspondence
kscott@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3150-7210

Funding

National Institutes of Health (R01DC013280)

Kristin Scott

National Institutes of Health (F32DK117671)

Gabriella R Sterne

National Institutes of Health (F32DC018225)

Philip K Shiu

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

Copyright

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.