Influence of insulin sensitivity on food cue evoked functional brain connectivity in children

Objective: Insulin resistance during childhood is a risk factor for developing type 2 diabetes and other health problems later in life. Studies in adults have shown that insulin resistance affects regional and network activity in the brain which are vital for behavior, including ingestion and metabo...

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Main Authors: Lorenzo Semeia, Ralf Veit, Sixiu Zhao, Shan Luo, Brendan Angelo, Andreas L. Birkenfeld, Hubert Preissl, Anny H. Xiang, Stephanie Kullmann, Kathleen A. Page
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811925001569
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author Lorenzo Semeia
Ralf Veit
Sixiu Zhao
Shan Luo
Brendan Angelo
Andreas L. Birkenfeld
Hubert Preissl
Anny H. Xiang
Stephanie Kullmann
Kathleen A. Page
author_facet Lorenzo Semeia
Ralf Veit
Sixiu Zhao
Shan Luo
Brendan Angelo
Andreas L. Birkenfeld
Hubert Preissl
Anny H. Xiang
Stephanie Kullmann
Kathleen A. Page
author_sort Lorenzo Semeia
collection DOAJ
description Objective: Insulin resistance during childhood is a risk factor for developing type 2 diabetes and other health problems later in life. Studies in adults have shown that insulin resistance affects regional and network activity in the brain which are vital for behavior, including ingestion and metabolic control. To date, no study has investigated how brain connections during exposure to food cues are association with peripheral insulin sensitivity in children. Methods: We included 53 children (36 girls) between the age of 7–11 years, who underwent an oral Glucose Tolerance Test (oGTT) to estimate peripheral insulin sensitivity (ISI). Brain responses were measured using functional magnetic resonance imaging (fMRI) before and after glucose ingestion. We compared food-cue task-based activity and functional connectivity (FC) between children with lower and higher ISI, adjusted for age and BMIz. Results: Independent of prandial state (i.e., glucose ingestion), children with lower ISI showed higher FC between the anterior insula and caudate and lower FC between the posterior insula and mid temporal cortex than children with higher ISI. Sex differences were found based on prandial state and peripheral insulin sensitivity in the insular FC. No differences were found on mean brain responses to food cues. Conclusions: In response to food cues, children with lower peripheral insulin sensitivity exhibited distinctive patterns of neural connectivity, notably in the insula's functional connections, when contrasted with their counterparts with higher peripheral insulin sensitivity. These differences might influence eating behavior and future risk of developing diabetes.
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spelling doaj-art-d95311b41d8f413588bc4be232d3196f2025-08-20T01:54:11ZengElsevierNeuroImage1095-95722025-04-0131012115410.1016/j.neuroimage.2025.121154Influence of insulin sensitivity on food cue evoked functional brain connectivity in childrenLorenzo Semeia0Ralf Veit1Sixiu Zhao2Shan Luo3Brendan Angelo4Andreas L. Birkenfeld5Hubert Preissl6Anny H. Xiang7Stephanie Kullmann8Kathleen A. Page9Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, Germany; Graduate Training Centre of Neuroscience, International Max Planck Research School, Tübingen, Germany; Corresponding author at: Institute for Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University of Tübingen, fMEG-Center, Otfried-Müller-Str. 47, 72076 Tübingen, Germany.Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, GermanyInstitute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, GermanyDivision of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USADivision of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USAInstitute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, Germany; Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, GermanyInstitute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, Germany; Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany; Department of Pharmacy and Biochemistry, University of Tübingen, GermanyDepartment of Research and Evaluation, Kaiser Permanente Southern California, Pasadena, CA, USAInstitute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD), Tübingen, Germany; Department of Internal Medicine, Division of Endocrinology, Diabetology and Nephrology, Eberhard Karls University Tübingen, Tübingen, GermanyDivision of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA; Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA; Corresponding author.Objective: Insulin resistance during childhood is a risk factor for developing type 2 diabetes and other health problems later in life. Studies in adults have shown that insulin resistance affects regional and network activity in the brain which are vital for behavior, including ingestion and metabolic control. To date, no study has investigated how brain connections during exposure to food cues are association with peripheral insulin sensitivity in children. Methods: We included 53 children (36 girls) between the age of 7–11 years, who underwent an oral Glucose Tolerance Test (oGTT) to estimate peripheral insulin sensitivity (ISI). Brain responses were measured using functional magnetic resonance imaging (fMRI) before and after glucose ingestion. We compared food-cue task-based activity and functional connectivity (FC) between children with lower and higher ISI, adjusted for age and BMIz. Results: Independent of prandial state (i.e., glucose ingestion), children with lower ISI showed higher FC between the anterior insula and caudate and lower FC between the posterior insula and mid temporal cortex than children with higher ISI. Sex differences were found based on prandial state and peripheral insulin sensitivity in the insular FC. No differences were found on mean brain responses to food cues. Conclusions: In response to food cues, children with lower peripheral insulin sensitivity exhibited distinctive patterns of neural connectivity, notably in the insula's functional connections, when contrasted with their counterparts with higher peripheral insulin sensitivity. These differences might influence eating behavior and future risk of developing diabetes.http://www.sciencedirect.com/science/article/pii/S1053811925001569fMRIFood cueFunctional connectivityChildrenInsulin sensitivityObesity
spellingShingle Lorenzo Semeia
Ralf Veit
Sixiu Zhao
Shan Luo
Brendan Angelo
Andreas L. Birkenfeld
Hubert Preissl
Anny H. Xiang
Stephanie Kullmann
Kathleen A. Page
Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
NeuroImage
fMRI
Food cue
Functional connectivity
Children
Insulin sensitivity
Obesity
title Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
title_full Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
title_fullStr Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
title_full_unstemmed Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
title_short Influence of insulin sensitivity on food cue evoked functional brain connectivity in children
title_sort influence of insulin sensitivity on food cue evoked functional brain connectivity in children
topic fMRI
Food cue
Functional connectivity
Children
Insulin sensitivity
Obesity
url http://www.sciencedirect.com/science/article/pii/S1053811925001569
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