Taste triggers a homeostatic temperature control in hungry flies

Hungry animals consistently show a desire to obtain food. Even a brief sensory detection of food can trigger bursts of physiological and behavioral changes. However, the underlying mechanisms by which the sensation of food triggers the acute behavioral response remain elusive. We have previously sho...

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Main Authors: Yujiro Umezaki, Sergio Hidalgo, Erika Nguyen, Tiffany Nguyen, Jay Suh, Sheena S Uchino, Joanna Chiu, Fumika Hamada
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/94703
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author Yujiro Umezaki
Sergio Hidalgo
Erika Nguyen
Tiffany Nguyen
Jay Suh
Sheena S Uchino
Joanna Chiu
Fumika Hamada
author_facet Yujiro Umezaki
Sergio Hidalgo
Erika Nguyen
Tiffany Nguyen
Jay Suh
Sheena S Uchino
Joanna Chiu
Fumika Hamada
author_sort Yujiro Umezaki
collection DOAJ
description Hungry animals consistently show a desire to obtain food. Even a brief sensory detection of food can trigger bursts of physiological and behavioral changes. However, the underlying mechanisms by which the sensation of food triggers the acute behavioral response remain elusive. We have previously shown in Drosophila that hunger drives a preference for low temperature. Because Drosophila is a small ectotherm, a preference for low temperature implies a low body temperature and a low metabolic rate. Here, we show that taste-sensing triggers a switch from a low to a high temperature preference in hungry flies. We show that taste stimulation by artificial sweeteners or optogenetics triggers an acute warm preference, but is not sufficient to reach the fed state. Instead, nutrient intake is required to reach the fed state. The data suggest that starvation recovery is controlled by two components: taste-evoked and nutrient-induced warm preferences, and that taste and nutrient quality play distinct roles in starvation recovery. Animals are motivated to eat based on time of day or hunger. We found that clock genes and hunger signals profoundly control the taste-evoked warm preferences. Thus, our data suggest that the taste-evoked response is one of the critical layers of regulatory mechanisms representing internal energy homeostasis and metabolism.
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spelling doaj-art-f57298654fa045a0aba69832f8e73b152024-12-02T14:59:33ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.94703Taste triggers a homeostatic temperature control in hungry fliesYujiro Umezaki0https://orcid.org/0009-0008-1136-8464Sergio Hidalgo1https://orcid.org/0000-0002-2604-156XErika Nguyen2Tiffany Nguyen3Jay Suh4Sheena S Uchino5Joanna Chiu6https://orcid.org/0000-0001-7613-8127Fumika Hamada7https://orcid.org/0009-0003-6537-7386Department of Neurobiology, Physiology and Behavior, University of California, Davis, Davis, United StatesDepartment of Entomology and Nematology, University of California, Davis, Davis, United StatesDivision of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, United StatesDivision of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, United StatesDivision of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, United StatesDepartment of Neurobiology, Physiology and Behavior, University of California, Davis, Davis, United StatesDepartment of Entomology and Nematology, University of California, Davis, Davis, United StatesDepartment of Neurobiology, Physiology and Behavior, University of California, Davis, Davis, United StatesHungry animals consistently show a desire to obtain food. Even a brief sensory detection of food can trigger bursts of physiological and behavioral changes. However, the underlying mechanisms by which the sensation of food triggers the acute behavioral response remain elusive. We have previously shown in Drosophila that hunger drives a preference for low temperature. Because Drosophila is a small ectotherm, a preference for low temperature implies a low body temperature and a low metabolic rate. Here, we show that taste-sensing triggers a switch from a low to a high temperature preference in hungry flies. We show that taste stimulation by artificial sweeteners or optogenetics triggers an acute warm preference, but is not sufficient to reach the fed state. Instead, nutrient intake is required to reach the fed state. The data suggest that starvation recovery is controlled by two components: taste-evoked and nutrient-induced warm preferences, and that taste and nutrient quality play distinct roles in starvation recovery. Animals are motivated to eat based on time of day or hunger. We found that clock genes and hunger signals profoundly control the taste-evoked warm preferences. Thus, our data suggest that the taste-evoked response is one of the critical layers of regulatory mechanisms representing internal energy homeostasis and metabolism.https://elifesciences.org/articles/94703gustatory receptorstemperature-sensing neuronscircadian clockbody temperaturestarvationcephalic phase response
spellingShingle Yujiro Umezaki
Sergio Hidalgo
Erika Nguyen
Tiffany Nguyen
Jay Suh
Sheena S Uchino
Joanna Chiu
Fumika Hamada
Taste triggers a homeostatic temperature control in hungry flies
eLife
gustatory receptors
temperature-sensing neurons
circadian clock
body temperature
starvation
cephalic phase response
title Taste triggers a homeostatic temperature control in hungry flies
title_full Taste triggers a homeostatic temperature control in hungry flies
title_fullStr Taste triggers a homeostatic temperature control in hungry flies
title_full_unstemmed Taste triggers a homeostatic temperature control in hungry flies
title_short Taste triggers a homeostatic temperature control in hungry flies
title_sort taste triggers a homeostatic temperature control in hungry flies
topic gustatory receptors
temperature-sensing neurons
circadian clock
body temperature
starvation
cephalic phase response
url https://elifesciences.org/articles/94703
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