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Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption

Eating behavior is not only influenced by the current energy balance, but also by the behavioral characteristics of eating. One of the recognized eating behavior constructs is ‘disinhibited eating,’ which refers to the tendency to overeat in response to negative emotional states or the presence of h...

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Autores principales: Nakamura, Yuko, Koike, Shinsuke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8128107/
https://www.ncbi.nlm.nih.gov/pubmed/34012386
http://dx.doi.org/10.3389/fnsys.2021.647143
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author Nakamura, Yuko
Koike, Shinsuke
author_facet Nakamura, Yuko
Koike, Shinsuke
author_sort Nakamura, Yuko
collection PubMed
description Eating behavior is not only influenced by the current energy balance, but also by the behavioral characteristics of eating. One of the recognized eating behavior constructs is ‘disinhibited eating,’ which refers to the tendency to overeat in response to negative emotional states or the presence of highly palatable foods. Food-related disinhibition is involved in binge eating, weight gain, and obesity and is also associated with the trait of impulsivity, which in turn, is linked to weight gain or maladaptive eating. However, the relationships among food-related disinhibition, the trait of impulsivity, and the neural substrates of eating behaviors in adolescence remain unclear. Therefore, we designed a functional magnetic resonance imaging (fMRI) study to examine the associations between brain responses to palatable liquid consumption and disinhibited eating behavior or impulsivity in healthy adolescents. Thirty-four adolescents (mean age ± standard deviation = 17.12 ± 1.91 years, age range = 14–19 years, boys = 15, girls = 19) participated in this study. Disinhibited eating was assessed with the disinhibition subscale of the Three-Factor Eating Questionnaire, while impulsivity was assessed using the Barratt impulsiveness scale. Participants received two fMRI sessions−a palatable liquid consumption fMRI and a resting-state fMRI. The fMRI experiment showed that increased disinhibited eating was positively associated with a greater insular response to palatable liquid consumption, while increased impulsivity was positively correlated with a greater amygdala response. The resting-state fMRI experiment showed that increased disinhibited eating was positively correlated with strengthened intrinsic functional connectivity between the insula and the amygdala, adjusting for sex (estimates of the beta coefficients = 0.146, standard error = 0.068, p = 0.040). Given that the amygdala and insular cortex are structurally and functionally connected and involved in trait impulsivity and ingestive behavior, our findings suggest that increased disinhibited eating would be associated with impulsivity via strengthened intrinsic functional connectivity between the insula and amygdala and linked to maladaptive eating.
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spelling pubmed-81281072021-05-18 Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption Nakamura, Yuko Koike, Shinsuke Front Syst Neurosci Neuroscience Eating behavior is not only influenced by the current energy balance, but also by the behavioral characteristics of eating. One of the recognized eating behavior constructs is ‘disinhibited eating,’ which refers to the tendency to overeat in response to negative emotional states or the presence of highly palatable foods. Food-related disinhibition is involved in binge eating, weight gain, and obesity and is also associated with the trait of impulsivity, which in turn, is linked to weight gain or maladaptive eating. However, the relationships among food-related disinhibition, the trait of impulsivity, and the neural substrates of eating behaviors in adolescence remain unclear. Therefore, we designed a functional magnetic resonance imaging (fMRI) study to examine the associations between brain responses to palatable liquid consumption and disinhibited eating behavior or impulsivity in healthy adolescents. Thirty-four adolescents (mean age ± standard deviation = 17.12 ± 1.91 years, age range = 14–19 years, boys = 15, girls = 19) participated in this study. Disinhibited eating was assessed with the disinhibition subscale of the Three-Factor Eating Questionnaire, while impulsivity was assessed using the Barratt impulsiveness scale. Participants received two fMRI sessions−a palatable liquid consumption fMRI and a resting-state fMRI. The fMRI experiment showed that increased disinhibited eating was positively associated with a greater insular response to palatable liquid consumption, while increased impulsivity was positively correlated with a greater amygdala response. The resting-state fMRI experiment showed that increased disinhibited eating was positively correlated with strengthened intrinsic functional connectivity between the insula and the amygdala, adjusting for sex (estimates of the beta coefficients = 0.146, standard error = 0.068, p = 0.040). Given that the amygdala and insular cortex are structurally and functionally connected and involved in trait impulsivity and ingestive behavior, our findings suggest that increased disinhibited eating would be associated with impulsivity via strengthened intrinsic functional connectivity between the insula and amygdala and linked to maladaptive eating. Frontiers Media S.A. 2021-05-03 /pmc/articles/PMC8128107/ /pubmed/34012386 http://dx.doi.org/10.3389/fnsys.2021.647143 Text en Copyright © 2021 Nakamura and Koike. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Nakamura, Yuko
Koike, Shinsuke
Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title_full Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title_fullStr Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title_full_unstemmed Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title_short Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption
title_sort association of disinhibited eating and trait of impulsivity with insula and amygdala responses to palatable liquid consumption
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8128107/
https://www.ncbi.nlm.nih.gov/pubmed/34012386
http://dx.doi.org/10.3389/fnsys.2021.647143
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