Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat

Background: Consumption of fat is regulated by reward and homeostatic pathways, but no studies have examined the role of the intake of a high fat meal (HFM) on subsequent brain activation to oral stimuli. Objective: We evaluated how prior consumption of a HFM or water load (WL) modulates reward, ho...

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Main Authors: Eldeghaidy, Sally, Marciani, Luca, Hort, Joanne, Hollowood, Tracey Ann, Singh, Gulzar, Bush, Debbie, Foster, Tim, Taylor, Andrew J., Busch, Johanneke, Spiller, Robin C., Gowland, Penny A., Francis, Susan T.
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Published: American Society for Nutrition 2016
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Online Access:https://eprints.nottingham.ac.uk/37047/
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author Eldeghaidy, Sally
Marciani, Luca
Hort, Joanne
Hollowood, Tracey Ann
Singh, Gulzar
Bush, Debbie
Foster, Tim
Taylor, Andrew J.
Busch, Johanneke
Spiller, Robin C.
Gowland, Penny A.
Francis, Susan T.
author_facet Eldeghaidy, Sally
Marciani, Luca
Hort, Joanne
Hollowood, Tracey Ann
Singh, Gulzar
Bush, Debbie
Foster, Tim
Taylor, Andrew J.
Busch, Johanneke
Spiller, Robin C.
Gowland, Penny A.
Francis, Susan T.
author_sort Eldeghaidy, Sally
building Nottingham Research Data Repository
collection Online Access
description Background: Consumption of fat is regulated by reward and homeostatic pathways, but no studies have examined the role of the intake of a high fat meal (HFM) on subsequent brain activation to oral stimuli. Objective: We evaluated how prior consumption of a HFM or water load (WL) modulates reward, homeostatic and taste brain responses to subsequent delivery of oral fat. Methods: A randomized 2-way crossover design (1-week apart) was used to compare prior consumption of a 250mL HFM (520kcal) (rapeseed oil (440kcal), emulsifier, sucrose, flavor cocktail) or non-caloric WL on brain activation to the delivery of repeated trials of an oral flavored no-fat control stimulus (CS) or flavored fat stimulus (FS) in 17 healthy adults (11 male, age=25±2 years, BMI=22.4±0.8kg/m2). Analyses tested differences in brain activation to the CS and FS, and baseline cerebral blood flow (CBF), following the HFM and WL. Individual’s plasma cholecystokinin (CCK) concentration following the HFM was correlated with their BOLD activation. Results: Prior consumption of the HFM compared to the WL led to decreased anterior insula taste activation in response to both the CS (36.3%,P<0.05) and FS (26.5%,P<0.05). The HFM caused reduced amygdala activation (25.1%,P<0.01) in response to the FS compared to the CS (fat-related satiety). Baseline CBF significantly reduced in taste (insula (5.7%,P<0.01)), homeostatic (hypothalamus (9.2%,P<0.01), thalamus (5.1%,P<0.05))), and reward areas (striatum (9.2%,P<0.01)) following the HFM. Individual’s plasma CCK concentration negatively correlated with brain activation in taste, oral somatosensory and reward areas. Conclusions: To reduce obesity, policy in industry is to lower the fat content of foods. Our results in healthy adults show that a HFM suppresses BOLD activation in taste and reward areas compared to a WL. This understanding will help inform the reformulation of reduced-fat foods that mimic the brain’s response to high fat counterparts, and guide future interventions to reduce obesity.
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spelling nottingham-370472024-08-15T15:20:14Z https://eprints.nottingham.ac.uk/37047/ Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat Eldeghaidy, Sally Marciani, Luca Hort, Joanne Hollowood, Tracey Ann Singh, Gulzar Bush, Debbie Foster, Tim Taylor, Andrew J. Busch, Johanneke Spiller, Robin C. Gowland, Penny A. Francis, Susan T. Background: Consumption of fat is regulated by reward and homeostatic pathways, but no studies have examined the role of the intake of a high fat meal (HFM) on subsequent brain activation to oral stimuli. Objective: We evaluated how prior consumption of a HFM or water load (WL) modulates reward, homeostatic and taste brain responses to subsequent delivery of oral fat. Methods: A randomized 2-way crossover design (1-week apart) was used to compare prior consumption of a 250mL HFM (520kcal) (rapeseed oil (440kcal), emulsifier, sucrose, flavor cocktail) or non-caloric WL on brain activation to the delivery of repeated trials of an oral flavored no-fat control stimulus (CS) or flavored fat stimulus (FS) in 17 healthy adults (11 male, age=25±2 years, BMI=22.4±0.8kg/m2). Analyses tested differences in brain activation to the CS and FS, and baseline cerebral blood flow (CBF), following the HFM and WL. Individual’s plasma cholecystokinin (CCK) concentration following the HFM was correlated with their BOLD activation. Results: Prior consumption of the HFM compared to the WL led to decreased anterior insula taste activation in response to both the CS (36.3%,P<0.05) and FS (26.5%,P<0.05). The HFM caused reduced amygdala activation (25.1%,P<0.01) in response to the FS compared to the CS (fat-related satiety). Baseline CBF significantly reduced in taste (insula (5.7%,P<0.01)), homeostatic (hypothalamus (9.2%,P<0.01), thalamus (5.1%,P<0.05))), and reward areas (striatum (9.2%,P<0.01)) following the HFM. Individual’s plasma CCK concentration negatively correlated with brain activation in taste, oral somatosensory and reward areas. Conclusions: To reduce obesity, policy in industry is to lower the fat content of foods. Our results in healthy adults show that a HFM suppresses BOLD activation in taste and reward areas compared to a WL. This understanding will help inform the reformulation of reduced-fat foods that mimic the brain’s response to high fat counterparts, and guide future interventions to reduce obesity. American Society for Nutrition 2016-09-21 Article PeerReviewed Eldeghaidy, Sally, Marciani, Luca, Hort, Joanne, Hollowood, Tracey Ann, Singh, Gulzar, Bush, Debbie, Foster, Tim, Taylor, Andrew J., Busch, Johanneke, Spiller, Robin C., Gowland, Penny A. and Francis, Susan T. (2016) Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat. Journal of Nutrition . ISSN 1541-6100 fMRI BOLD CBF CCK habituation oral fat insula subjective rating satiety http://jn.nutrition.org/content/early/2016/09/20/jn.116.234104 doi:10.3945/jn.116.234104 doi:10.3945/jn.116.234104
spellingShingle fMRI
BOLD
CBF
CCK
habituation
oral fat
insula
subjective rating satiety
Eldeghaidy, Sally
Marciani, Luca
Hort, Joanne
Hollowood, Tracey Ann
Singh, Gulzar
Bush, Debbie
Foster, Tim
Taylor, Andrew J.
Busch, Johanneke
Spiller, Robin C.
Gowland, Penny A.
Francis, Susan T.
Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title_full Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title_fullStr Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title_full_unstemmed Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title_short Prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
title_sort prior consumption of a fat meal in healthy adults modulates the brain’s response to fat
topic fMRI
BOLD
CBF
CCK
habituation
oral fat
insula
subjective rating satiety
url https://eprints.nottingham.ac.uk/37047/
https://eprints.nottingham.ac.uk/37047/
https://eprints.nottingham.ac.uk/37047/