The effect of hunger state on hypothalamic functional connectivity in response to food cues

Stephanie Kullmann; Ralf Veit; Daniel R Crabtree; William Buosi; Odysseas Androutsos; Alexandra M Johnstone; Yannis Manios; Hubert Preissl; Paul A M Smeets

doi:10.1002/hbm.26059

The effect of hunger state on hypothalamic functional connectivity in response to food cues

Stephanie Kullmann^* (Corresponding Author), Ralf Veit, Daniel R Crabtree, William Buosi, Odysseas Androutsos, Alexandra M Johnstone, Yannis Manios, Hubert Preissl, Paul A M Smeets

^*Corresponding author for this work

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Abstract

The neural underpinnings of the integration of internal and external cues that reflect nutritional status are poorly understood in humans. The hypothalamus is a key integrative area involved in short- and long-term energy intake regulation. Hence, we examined the effect of hunger state on the hypothalamus network using functional magnetic resonance imaging. In a multicenter study, participants performed a food cue viewing task either fasted or sated on two separate days. We evaluated hypothalamic functional connectivity (FC) using psychophysiological interactions during high versus low caloric food cue viewing in 107 adults (divided into four groups based on age and body mass index [BMI]; age range 24-76 years; BMI range 19.5-41.5 kg/m 2 ). In the sated compared to the fasted condition, the hypothalamus showed significantly higher FC with the bilateral caudate, the left insula and parts of the left inferior frontal cortex. Interestingly, we observed a significant interaction between hunger state and BMI group in the dorsolateral prefrontal cortex (DLPFC). Participants with normal weight compared to overweight and obesity showed higher FC between the hypothalamus and DLPFC in the fasted condition. The current study showed that task-based FC of the hypothalamus can be modulated by internal (hunger state) and external cues (i.e., food cues with varying caloric content) with a general enhanced communication in the sated state and obesity-associated differences in hypothalamus to DLPFC communication. This could potentially promote overeating in persons with obesity.

Original language	English
Pages (from-to)	418-428
Number of pages	11
Journal	Human Brain Mapping
Volume	44
Issue number	2
Early online date	3 Sept 2022
DOIs	https://doi.org/10.1002/hbm.26059
Publication status	Published - 1 Feb 2023

Bibliographical note

ACKNOWLEDGMENT
The authors thank Lisette Charbonnier for her relentless efforts in setting up the study at all three sites and collecting the Dutch data. Open Access funding enabled and organized by Projekt DEAL.

FUNDING INFORMATION
This work was financially supported by the European Union Seventh Framework Programme (FP7/2007–2013) for research, technological development, and demonstration under grant agreement 266408 (Full4Health, www.full4health.eu). Furthermore, the study was supported in parts by a grant (01GI0925) from the Federal Ministry of Education and Research (BMBF) to the German Center for Diabetes Research (DZD e.V.).

Data Availability Statement

The authors have documented all data, methods, and materials used to conduct this research study, and anonymized data will be shared by request from any qualified investigator.

Keywords

fMRI
food cue reactivity
functional connectivity
hunger
insulin resistance
obesity
satiety

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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© 2022 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. https://creativecommons.org/licenses/by-nc/4.0/
Final published version, 1 MBLicence: CC BY-NC

Cite this

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title = "The effect of hunger state on hypothalamic functional connectivity in response to food cues",

abstract = "The neural underpinnings of the integration of internal and external cues that reflect nutritional status are poorly understood in humans. The hypothalamus is a key integrative area involved in short- and long-term energy intake regulation. Hence, we examined the effect of hunger state on the hypothalamus network using functional magnetic resonance imaging. In a multicenter study, participants performed a food cue viewing task either fasted or sated on two separate days. We evaluated hypothalamic functional connectivity (FC) using psychophysiological interactions during high versus low caloric food cue viewing in 107 adults (divided into four groups based on age and body mass index [BMI]; age range 24-76 years; BMI range 19.5-41.5 kg/m 2 ). In the sated compared to the fasted condition, the hypothalamus showed significantly higher FC with the bilateral caudate, the left insula and parts of the left inferior frontal cortex. Interestingly, we observed a significant interaction between hunger state and BMI group in the dorsolateral prefrontal cortex (DLPFC). Participants with normal weight compared to overweight and obesity showed higher FC between the hypothalamus and DLPFC in the fasted condition. The current study showed that task-based FC of the hypothalamus can be modulated by internal (hunger state) and external cues (i.e., food cues with varying caloric content) with a general enhanced communication in the sated state and obesity-associated differences in hypothalamus to DLPFC communication. This could potentially promote overeating in persons with obesity. ",

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author = "Stephanie Kullmann and Ralf Veit and Crabtree, {Daniel R} and William Buosi and Odysseas Androutsos and Johnstone, {Alexandra M} and Yannis Manios and Hubert Preissl and Smeets, {Paul A M}",

note = "ACKNOWLEDGMENT The authors thank Lisette Charbonnier for her relentless efforts in setting up the study at all three sites and collecting the Dutch data. Open Access funding enabled and organized by Projekt DEAL. FUNDING INFORMATION This work was financially supported by the European Union Seventh Framework Programme (FP7/2007–2013) for research, technological development, and demonstration under grant agreement 266408 (Full4Health, www.full4health.eu). Furthermore, the study was supported in parts by a grant (01GI0925) from the Federal Ministry of Education and Research (BMBF) to the German Center for Diabetes Research (DZD e.V.).",

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AU - Johnstone, Alexandra M

AU - Manios, Yannis

AU - Preissl, Hubert

AU - Smeets, Paul A M

N1 - ACKNOWLEDGMENT The authors thank Lisette Charbonnier for her relentless efforts in setting up the study at all three sites and collecting the Dutch data. Open Access funding enabled and organized by Projekt DEAL. FUNDING INFORMATION This work was financially supported by the European Union Seventh Framework Programme (FP7/2007–2013) for research, technological development, and demonstration under grant agreement 266408 (Full4Health, www.full4health.eu). Furthermore, the study was supported in parts by a grant (01GI0925) from the Federal Ministry of Education and Research (BMBF) to the German Center for Diabetes Research (DZD e.V.).

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AB - The neural underpinnings of the integration of internal and external cues that reflect nutritional status are poorly understood in humans. The hypothalamus is a key integrative area involved in short- and long-term energy intake regulation. Hence, we examined the effect of hunger state on the hypothalamus network using functional magnetic resonance imaging. In a multicenter study, participants performed a food cue viewing task either fasted or sated on two separate days. We evaluated hypothalamic functional connectivity (FC) using psychophysiological interactions during high versus low caloric food cue viewing in 107 adults (divided into four groups based on age and body mass index [BMI]; age range 24-76 years; BMI range 19.5-41.5 kg/m 2 ). In the sated compared to the fasted condition, the hypothalamus showed significantly higher FC with the bilateral caudate, the left insula and parts of the left inferior frontal cortex. Interestingly, we observed a significant interaction between hunger state and BMI group in the dorsolateral prefrontal cortex (DLPFC). Participants with normal weight compared to overweight and obesity showed higher FC between the hypothalamus and DLPFC in the fasted condition. The current study showed that task-based FC of the hypothalamus can be modulated by internal (hunger state) and external cues (i.e., food cues with varying caloric content) with a general enhanced communication in the sated state and obesity-associated differences in hypothalamus to DLPFC communication. This could potentially promote overeating in persons with obesity.

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KW - food cue reactivity

KW - functional connectivity

KW - hunger

KW - insulin resistance

KW - obesity

KW - satiety

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DO - 10.1002/hbm.26059

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SN - 1065-9471

VL - 44

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JO - Human Brain Mapping

JF - Human Brain Mapping

IS - 2

ER -

The effect of hunger state on hypothalamic functional connectivity in response to food cues

Abstract

Bibliographical note

Data Availability Statement

Keywords

UN SDGs

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