Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence

Abstract Habitual consumption of low-calorie sweeteners (LCS) during juvenile-adolescence can lead to greater sugar intake later in life. Here, we investigated if exposure to the LCS Acesulfame Potassium (Ace-K) during this critical period of development reprograms the taste system in a way that wou...

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Main Authors: Clare M. Mathes, Sarah J. Terrill, Juan P. Taborda-Bejarano, Sandrine Chometton, Mallory J. Witt, Gaurikka Mendiratta, Emily G. Gilman, Delenn R. Hartswick, Bo M. Anderson, Lindsey A. Schier
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-84391-3
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author Clare M. Mathes
Sarah J. Terrill
Juan P. Taborda-Bejarano
Sandrine Chometton
Mallory J. Witt
Gaurikka Mendiratta
Emily G. Gilman
Delenn R. Hartswick
Bo M. Anderson
Lindsey A. Schier
author_facet Clare M. Mathes
Sarah J. Terrill
Juan P. Taborda-Bejarano
Sandrine Chometton
Mallory J. Witt
Gaurikka Mendiratta
Emily G. Gilman
Delenn R. Hartswick
Bo M. Anderson
Lindsey A. Schier
author_sort Clare M. Mathes
collection DOAJ
description Abstract Habitual consumption of low-calorie sweeteners (LCS) during juvenile-adolescence can lead to greater sugar intake later in life. Here, we investigated if exposure to the LCS Acesulfame Potassium (Ace-K) during this critical period of development reprograms the taste system in a way that would alter hedonic responding for common dietary compounds. Results revealed that early-life LCS intake not only enhanced the avidity for a caloric sugar (fructose) when rats were in a state of caloric need, it increased acceptance of a bitterant (quinine) in Ace-K-exposed rats tested when middle-aged. These behavior shifts, which endured months after the end of Ace-K exposure, were accompanied by widespread changes in the peripheral taste system. The anterior tongue had fewer fungiform taste papillae, and the circumvallate papillae had a reduced anterior to posterior span and diminished expression of genes involved in sweet reception, sweet and bitter intracellular signaling, fructose transport, and cellular progeneration in the Ace-K-exposed rats. Ace-K exposure also led to a significant reduction in dopamine-producing cells of the ventral tegmental area. The collective findings reveal that LCS intake early in life alters the taste-brain axis and the behavioral responsiveness to both positive and negative tastants that are important determinants of dietary preferences.
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spelling doaj-art-44afb96eec214f3186b4c7ef11a46fe52025-01-19T12:18:07ZengNature PortfolioScientific Reports2045-23222025-01-0115111110.1038/s41598-024-84391-3Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescenceClare M. Mathes0Sarah J. Terrill1Juan P. Taborda-Bejarano2Sandrine Chometton3Mallory J. Witt4Gaurikka Mendiratta5Emily G. Gilman6Delenn R. Hartswick7Bo M. Anderson8Lindsey A. Schier9Department of Neuroscience, Baldwin Wallace UniversityDepartment of Neuroscience, Carthage CollegeDepartment of Neuroscience, Baldwin Wallace UniversityDepartment of Biological Sciences, University of Southern CaliforniaDepartment of Neuroscience, Baldwin Wallace UniversityDepartment of Neuroscience, Baldwin Wallace UniversityDepartment of Neuroscience, Baldwin Wallace UniversityDepartment of Neuroscience, Baldwin Wallace UniversityDepartment of Neuroscience, Carthage CollegeDepartment of Biological Sciences, University of Southern CaliforniaAbstract Habitual consumption of low-calorie sweeteners (LCS) during juvenile-adolescence can lead to greater sugar intake later in life. Here, we investigated if exposure to the LCS Acesulfame Potassium (Ace-K) during this critical period of development reprograms the taste system in a way that would alter hedonic responding for common dietary compounds. Results revealed that early-life LCS intake not only enhanced the avidity for a caloric sugar (fructose) when rats were in a state of caloric need, it increased acceptance of a bitterant (quinine) in Ace-K-exposed rats tested when middle-aged. These behavior shifts, which endured months after the end of Ace-K exposure, were accompanied by widespread changes in the peripheral taste system. The anterior tongue had fewer fungiform taste papillae, and the circumvallate papillae had a reduced anterior to posterior span and diminished expression of genes involved in sweet reception, sweet and bitter intracellular signaling, fructose transport, and cellular progeneration in the Ace-K-exposed rats. Ace-K exposure also led to a significant reduction in dopamine-producing cells of the ventral tegmental area. The collective findings reveal that LCS intake early in life alters the taste-brain axis and the behavioral responsiveness to both positive and negative tastants that are important determinants of dietary preferences.https://doi.org/10.1038/s41598-024-84391-3
spellingShingle Clare M. Mathes
Sarah J. Terrill
Juan P. Taborda-Bejarano
Sandrine Chometton
Mallory J. Witt
Gaurikka Mendiratta
Emily G. Gilman
Delenn R. Hartswick
Bo M. Anderson
Lindsey A. Schier
Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
Scientific Reports
title Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
title_full Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
title_fullStr Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
title_full_unstemmed Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
title_short Neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low-calorie sweetener during adolescence
title_sort neurobehavioral plasticity in the rodent gustatory system induced by regular consumption of a low calorie sweetener during adolescence
url https://doi.org/10.1038/s41598-024-84391-3
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