Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.

Food presents a multisensory experience, with visual, taste, and olfactory cues being important in allowing an animal to determine the safety and nutritional value of a given substance. Texture, however, remains a surprisingly unexplored aspect, despite providing key information about the state of t...

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Main Authors: Nikita Komarov, Cornelia Fritsch, G Larisa Maier, Johannes Bues, Marjan Biočanin, Clarisse Brunet Avalos, Andrea Dodero, Jae Young Kwon, Bart Deplancke, Simon G Sprecher
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002730
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author Nikita Komarov
Cornelia Fritsch
G Larisa Maier
Johannes Bues
Marjan Biočanin
Clarisse Brunet Avalos
Andrea Dodero
Jae Young Kwon
Bart Deplancke
Simon G Sprecher
author_facet Nikita Komarov
Cornelia Fritsch
G Larisa Maier
Johannes Bues
Marjan Biočanin
Clarisse Brunet Avalos
Andrea Dodero
Jae Young Kwon
Bart Deplancke
Simon G Sprecher
author_sort Nikita Komarov
collection DOAJ
description Food presents a multisensory experience, with visual, taste, and olfactory cues being important in allowing an animal to determine the safety and nutritional value of a given substance. Texture, however, remains a surprisingly unexplored aspect, despite providing key information about the state of the food through properties such as hardness, liquidity, and granularity. Food perception is achieved by specialised sensory neurons, which themselves are defined by the receptor genes they express. While it was assumed that sensory neurons respond to one or few closely related stimuli, more recent findings challenge this notion and support evidence that certain sensory neurons are more broadly tuned. In the Drosophila taste system, gustatory neurons respond to cues of opposing hedonic valence or to olfactory cues. Here, we identified that larvae ingest and navigate towards specific food substrate hardnesses and probed the role of gustatory organs in this behaviour. By developing a genetic tool targeting specifically gustatory organs, we show that these organs are major contributors for evaluation of food hardness and ingestion decision-making. We find that ablation of gustatory organs not only results in loss of chemosensation, but also navigation and ingestion preference to varied substrate hardnesses. Furthermore, we show that certain neurons in the primary taste organ exhibit varied and concurrent physiological responses to mechanical and multimodal stimulation. We show that individual neurons house independent mechanisms for multiple sensory modalities, challenging assumptions about capabilities of sensory neurons. We propose that further investigations, across the animal kingdom, may reveal higher sensory complexity than currently anticipated.
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issn 1544-9173
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spelling doaj-art-bf5f3670331e4f859ebe99bdd6eb687f2025-02-07T05:30:17ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-01-01231e300273010.1371/journal.pbio.3002730Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.Nikita KomarovCornelia FritschG Larisa MaierJohannes BuesMarjan BiočaninClarisse Brunet AvalosAndrea DoderoJae Young KwonBart DeplanckeSimon G SprecherFood presents a multisensory experience, with visual, taste, and olfactory cues being important in allowing an animal to determine the safety and nutritional value of a given substance. Texture, however, remains a surprisingly unexplored aspect, despite providing key information about the state of the food through properties such as hardness, liquidity, and granularity. Food perception is achieved by specialised sensory neurons, which themselves are defined by the receptor genes they express. While it was assumed that sensory neurons respond to one or few closely related stimuli, more recent findings challenge this notion and support evidence that certain sensory neurons are more broadly tuned. In the Drosophila taste system, gustatory neurons respond to cues of opposing hedonic valence or to olfactory cues. Here, we identified that larvae ingest and navigate towards specific food substrate hardnesses and probed the role of gustatory organs in this behaviour. By developing a genetic tool targeting specifically gustatory organs, we show that these organs are major contributors for evaluation of food hardness and ingestion decision-making. We find that ablation of gustatory organs not only results in loss of chemosensation, but also navigation and ingestion preference to varied substrate hardnesses. Furthermore, we show that certain neurons in the primary taste organ exhibit varied and concurrent physiological responses to mechanical and multimodal stimulation. We show that individual neurons house independent mechanisms for multiple sensory modalities, challenging assumptions about capabilities of sensory neurons. We propose that further investigations, across the animal kingdom, may reveal higher sensory complexity than currently anticipated.https://doi.org/10.1371/journal.pbio.3002730
spellingShingle Nikita Komarov
Cornelia Fritsch
G Larisa Maier
Johannes Bues
Marjan Biočanin
Clarisse Brunet Avalos
Andrea Dodero
Jae Young Kwon
Bart Deplancke
Simon G Sprecher
Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
PLoS Biology
title Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
title_full Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
title_fullStr Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
title_full_unstemmed Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
title_short Food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology.
title_sort food hardness preference reveals multisensory contributions of fly larval gustatory organs in behaviour and physiology
url https://doi.org/10.1371/journal.pbio.3002730
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