Prior Consumption of a Fat Meal in Healthy Adults Modulates the Brain's Response to Fat

Sally Eldeghaidy, Luca Marciani, Joanne Hort, Tracey Hollowood, Gulzar Singh, Debbie Bush, Tim Foster, Andy J Taylor, Johanneke Busch, Robin C Spiller, Penny A Gowland, Susan T Francis, Sally Eldeghaidy, Luca Marciani, Joanne Hort, Tracey Hollowood, Gulzar Singh, Debbie Bush, Tim Foster, Andy J Taylor, Johanneke Busch, Robin C Spiller, Penny A Gowland, Susan T Francis

Abstract

Background: The consumption of fat is regulated by reward and homeostatic pathways, but no studies to our knowledge have examined the role of high-fat meal (HFM) intake on subsequent brain activation to oral stimuli.

Objective: We evaluated how prior consumption of an HFM or water load (WL) modulates reward, homeostatic, and taste brain responses to the subsequent delivery of oral fat.

Methods: A randomized 2-way crossover design spaced 1 wk apart was used to compare the prior consumption of a 250-mL HFM (520 kcal) [rapeseed oil (440 kcal), emulsifier, sucrose, flavor cocktail] or noncaloric WL on brain activation to the delivery of repeated trials of a flavored no-fat control stimulus (CS) or flavored fat stimulus (FS) in 17 healthy adults (11 men) aged 25 ± 2 y and with a body mass index (in kg/m2) of 22.4 ± 0.8. We tested differences in brain activation to the CS and FS and baseline cerebral blood flow (CBF) after the HFM and WL. We also tested correlations between an individual's plasma cholecystokinin (CCK) concentration after the HFM and blood oxygenation level-dependent (BOLD) activation of brain regions.

Results: Compared to the WL, consuming the HFM 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) after the HFM. An individual's plasma CCK concentration correlated negatively with brain activation in taste and oral somatosensory (ρ = -0.39; P < 0.05) and reward areas (ρ = -0.36; P < 0.05).

Conclusions: Our results in healthy adults show that an 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.

Keywords: BOLD; CBF; CCK; fMRI; habituation; insula; oral fat; subjective rating satiety.

Conflict of interest statement

2 Author disclosures: S Eldeghaidy, L Marciani, J Hort, T Hollowood, G Singh, D Bush, T Foster, AJ Taylor, J Busch, RC Spiller, PA Gowland, and ST Francis, no conflicts of interest. The views expressed herein are those of the author(s) and not necessarily those of the National Health Service, the National Institute of Health Research, or the United Kingdom Department of Health.

Figures

FIGURE 1
FIGURE 1
Overall design of study day (A) and a single fMRI trial (B). The WL and HFM conditions had the same design. During the fMRI scan, 18 trials of both the CS and FS were delivered in a pseudorandomized order. CBF, cerebral blood flow; CCK, cholecystokinin; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal; VAS, visual analog scale; WL, water load.
FIGURE 2
FIGURE 2
Subjective ratings of fullness (A), hunger (B), and appetite (C) and plasma CCK concentration (D) at baseline and at 30 and 80 min postmeal for HFM and WL in healthy adults. Data are means ± SEMs (A, B, and C), n = 16. Median, first, and third quartiles and minor and major outliers are shown in (D). Differences between WL and HFM: *P < 0.05, **P < 0.01, and ***P < 0.001. CCK, cholecystokinin; HFM, high-fat meal; WL, water load.
FIGURE 3
FIGURE 3
Activated brain regions in response to the fat stimulus after the high-fat meal in healthy adults, n = 16. The activation map had a false-discovery rate–corrected threshold of P < 0.05. ACC, anterior cingulate cortex; SI, primary somatosensory cortex; SII, secondary somatosensory cortex.
FIGURE 4
FIGURE 4
Decrease in BOLD response after the HFM in healthy adult subjects, n = 16. (A) Activation maps of the WL > HFM contrast for the CS and the FS displayed at P < 0.05 (uncorrected). (B) Mean ± SEM BOLD β-values (combined across hemispheres) in a priori cortical areas. *Difference between the HFM and WL for the CS and FS, P < 0.05. **Difference between the FS compared to the CS (fat-related satiety) for the HFM, P < 0.01. ACC, anterior cingulate cortex; a.u., arbitrary unit; BOLD, blood oxygenation level–dependent; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal; OFC, orbitofrontal cortex; WL, water load.
FIGURE 5
FIGURE 5
Habituation in BOLD percentage signal change after HFM consumption across the 18 CS and FS trials. Data are shown for the amygdala response to CS (A) and FS (B) and midinsula response to CS (C) and FS (D). Data are pooled from both hemispheres for each subject, n = 36. BOLD, blood oxygenation level–dependent; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal.
FIGURE 6
FIGURE 6
Change in CBF after the HFM and WL. (A) Baseline CBF image, n = 16 (i); ROIs interrogated in the CBF analysis: insula (green), hypothalamus (pink), thalamus (blue), striatum (yellow), and visual cortex (red) (ii). (B) Maps of the CBF change after the HFM (baseline to 65 min postmeal) and WL (baseline to 40 min postmeal). CBF was reduced (blue) in the hypothalamus, thalamus, striatum, and insula after the HFM. CBF was increased (orange) in the thalamus and insula after the WL. The yellow outline shows the insula BOLD response to the CS and FS as seen in Figure 3. Maps are displayed at P < 0.001 (uncorrected). BOLD, blood oxygenation level–dependent; CBF, cerebral blood flow; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal; WL, water load.
FIGURE 7
FIGURE 7
Mean ± SEM percentage change in CBF after the WL and HFM for hypothalamus (A), thalamus (B), striatum (C), insula (D), and visual cortex (E), n = 16. Different from baseline: *P < 0.05 and **P < 0.01. CBF, cerebral blood flow; HFM, high-fat meal; WL, water load.
FIGURE 8
FIGURE 8
BOLD signal change to CS and FS after the WL and HFM plot against associated CBF percentage change (mean CBF at 40 and 65 min postmeal) for hypothalamus (A), thalamus (B), and insula (C). BOLD, blood oxygenation level–dependent; CBF, cerebral blood flow; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal; WL, water load.
FIGURE 9
FIGURE 9
Negative correlation of the BOLD activation to the CS and FS with plasma CCK concentration after the HFM in individual healthy adult subjects; n = 16. (A) Brain regions in which individual’s BOLD response to the CS and FS after the HFM negatively correlated with plasma CCK concentration; maps are displayed at P < 0.005 (uncorrected). Scatter plots show increased plasma CCK concentration results in decreased BOLD β-values to the CS and FS after the HFM in the amygdala (B) and midinsula (C) (data points shown for each hemisphere and subject, n = 32). BOLD, blood oxygenation level–dependent; CCK, cholecystokinin; CS, control stimulus; FS, fat stimulus; HFM, high-fat meal; SI, primary somatosensory cortex; SII, secondary somatosensory cortex.

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Source: PubMed

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