Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity

To study the interplay of metabolic state (hungry vs. satiated) and glucose administration (including hormonal modulation) on brain function, resting-state functional magnetic resonance imaging (rs-fMRI) and blood samples were obtained in 24 healthy normal-weight men in a repeated measurement design...

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Main Authors: Arkan Al-Zubaidi, Marcus Heldmann, Alfred Mertins, Georg Brabant, Janis Marc Nolde, Kamila Jauch-Chara, Thomas F. Münte
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2019.00162/full
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author Arkan Al-Zubaidi
Marcus Heldmann
Marcus Heldmann
Alfred Mertins
Georg Brabant
Janis Marc Nolde
Kamila Jauch-Chara
Thomas F. Münte
Thomas F. Münte
author_facet Arkan Al-Zubaidi
Marcus Heldmann
Marcus Heldmann
Alfred Mertins
Georg Brabant
Janis Marc Nolde
Kamila Jauch-Chara
Thomas F. Münte
Thomas F. Münte
author_sort Arkan Al-Zubaidi
collection DOAJ
description To study the interplay of metabolic state (hungry vs. satiated) and glucose administration (including hormonal modulation) on brain function, resting-state functional magnetic resonance imaging (rs-fMRI) and blood samples were obtained in 24 healthy normal-weight men in a repeated measurement design. Participants were measured twice: once after a 36 h fast (except water) and once under satiation (three meals/day for 36 h). During each session, rs-fMRI and hormone concentrations were recorded before and after a 75 g oral dose of glucose. We calculated the amplitude map from blood-oxygen-level-dependent (BOLD) signals by using the fractional amplitude of low-frequency fluctuation (fALFF) approach for each volunteer per condition. Using multiple linear regression analysis (MLRA) the interdependence of brain activity, plasma insulin and blood glucose was investigated. We observed a modulatory impact of fasting state on intrinsic brain activity in the posterior cingulate cortex (PCC). Strikingly, differences in plasma insulin levels between hunger and satiety states after glucose administration at the time of the scan were negatively related to brain activity in the posterior insula and superior frontal gyrus (SFG), while plasma glucose levels were positively associated with activity changes in the fusiform gyrus. Furthermore, we could show that changes in plasma insulin enhanced the connectivity between the posterior insula and SFG. Our results indicate that hormonal signals like insulin alleviate an acute hemostatic energy deficit by modifying the homeostatic and frontal circuitry of the human brain.
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spelling doaj.art-f0a8242c24ac483794b376c89b4a66bd2022-12-21T22:25:14ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612019-05-011310.3389/fnhum.2019.00162420805Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain ActivityArkan Al-Zubaidi0Marcus Heldmann1Marcus Heldmann2Alfred Mertins3Georg Brabant4Janis Marc Nolde5Kamila Jauch-Chara6Thomas F. Münte7Thomas F. Münte8Department of Neurology, University of Lübeck, Lübeck, GermanyDepartment of Neurology, University of Lübeck, Lübeck, GermanyInstitute of Psychology II, University of Lübeck, Lübeck, GermanyInstitute for Signal Processing, University of Lübeck, Lübeck, GermanyDepartment of Internal Medicine I, University of Lübeck, Lübeck, GermanyDepartment of Neurology, University of Lübeck, Lübeck, GermanyDepartment of Psychiatry and Psychotherapy, Christian-Albrechts-University, Kiel, GermanyDepartment of Neurology, University of Lübeck, Lübeck, GermanyInstitute of Psychology II, University of Lübeck, Lübeck, GermanyTo study the interplay of metabolic state (hungry vs. satiated) and glucose administration (including hormonal modulation) on brain function, resting-state functional magnetic resonance imaging (rs-fMRI) and blood samples were obtained in 24 healthy normal-weight men in a repeated measurement design. Participants were measured twice: once after a 36 h fast (except water) and once under satiation (three meals/day for 36 h). During each session, rs-fMRI and hormone concentrations were recorded before and after a 75 g oral dose of glucose. We calculated the amplitude map from blood-oxygen-level-dependent (BOLD) signals by using the fractional amplitude of low-frequency fluctuation (fALFF) approach for each volunteer per condition. Using multiple linear regression analysis (MLRA) the interdependence of brain activity, plasma insulin and blood glucose was investigated. We observed a modulatory impact of fasting state on intrinsic brain activity in the posterior cingulate cortex (PCC). Strikingly, differences in plasma insulin levels between hunger and satiety states after glucose administration at the time of the scan were negatively related to brain activity in the posterior insula and superior frontal gyrus (SFG), while plasma glucose levels were positively associated with activity changes in the fusiform gyrus. Furthermore, we could show that changes in plasma insulin enhanced the connectivity between the posterior insula and SFG. Our results indicate that hormonal signals like insulin alleviate an acute hemostatic energy deficit by modifying the homeostatic and frontal circuitry of the human brain.https://www.frontiersin.org/article/10.3389/fnhum.2019.00162/fullresting state fMRIhungersatietyglucose administrationfALFFinsulin levels
spellingShingle Arkan Al-Zubaidi
Marcus Heldmann
Marcus Heldmann
Alfred Mertins
Georg Brabant
Janis Marc Nolde
Kamila Jauch-Chara
Thomas F. Münte
Thomas F. Münte
Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
Frontiers in Human Neuroscience
resting state fMRI
hunger
satiety
glucose administration
fALFF
insulin levels
title Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
title_full Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
title_fullStr Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
title_full_unstemmed Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
title_short Impact of Hunger, Satiety, and Oral Glucose on the Association Between Insulin and Resting-State Human Brain Activity
title_sort impact of hunger satiety and oral glucose on the association between insulin and resting state human brain activity
topic resting state fMRI
hunger
satiety
glucose administration
fALFF
insulin levels
url https://www.frontiersin.org/article/10.3389/fnhum.2019.00162/full
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