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

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.

Brain Imaging of Taste Perception in Obesity: a Review

“…Brain responses to fat in healthy volunteers can also be used to elucidate eating patterns and BMI gain. Eldeghaidy et al [ 54 ] showed that amygdala BOLD response to a fatty stimulus is attenuated after a high-fat meal compared to water intake. This suggests that satiety from a high-fat meal reduces the reward response to fat.…”

Functional Connectivity Within the Gustatory Network Is Altered by Fat Content and Oral Fat Sensitivity – A Pilot Study

“…Thus, it was shown that the hypothalamic activation is markedly lower after sugar intake or after a high-fat meal than after the intake of water or of a low-fat meal (Smeets et al, 2005a,b; Frank et al, 2012; Eldeghaidy et al, 2016). Homeostatic processes including hunger and satiety are mainly processed in predesignated nuclei within the hypothalamus (Morton et al, 2014).…”

Fatty Acid Lingual Application Activates Gustatory and Reward Brain Circuits in the Mouse

“…Tzieropoulos et al (2013) reported that dietary fat was able to induce sustained reward response in human brains. Eldeghaidy et al [ 12 ] used functional magnetic resonance imaging (fMRI) in human subjects, and suggested that taste, appetite, and reward-related brain areas were responsive to nutritional status and received sensory and interoceptive signals of motivation and hedonic value in response to a fat-rich diet. Other fMRI studies in humans have also demonstrated that administration of dietary lipids activates cerebral taste, texture, and reward areas [ 13 , 14 , 15 , 16 ].…”