Journal
JOURNAL OF NEUROSCIENCE
Volume 43, Issue 47, Pages 8000-8017Publisher
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1473-23.2023
Keywords
dietary fat; oral food processing; neuroeconomics; preference; reward value
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This study reveals how the human orbitofrontal cortex translates the oral sensations of high-fat foods into subjective economic valuations, guiding eating behavior. The findings suggest that the reward systems in the brain can sense dietary fat through oral sliding friction, which plays a specific role in regulating our preference for high-fat foods.
Although overconsumption of high-fat foods is a major driver of weight gain, the neural mechanisms that link the oral sensory properties of dietary fat to reward valuation and eating behavior remain unclear. Here we combine novel food-engineering approaches with functional neuroimaging to show that the human orbitofrontal cortex (OFC) translates oral sensations evoked by high-fat foods into subjective economic valuations that guide eating behavior. Male and female volunteers sampled and evaluated nutrient-controlled liquid foods that varied in fat and sugar (milkshakes). During oral food processing, OFC activity encoded a specific oral-sensory parameter that mediated the influence of the foods' fat content on reward value: the coefficient of sliding friction. Specifically, OFC responses to foods in the mouth reflected the smooth, oily texture (i.e., mouthfeel) produced by fatty liquids on oral surfaces. Distinct activity patterns in OFC encoded the economic values associated with particular foods, which reflected the subjective integration of sliding friction with other food properties (sugar, fat, viscosity). Critically, neural sensitivity of OFC to oral texture predicted individuals' fat preferences in a naturalistic eating test: individuals whose OFC was more sensitive to fat-related oral texture consumed more fat during ad libitum eating. Our findings suggest that reward systems of the human brain sense dietary fat from oral sliding friction, a mechanical food parameter that likely governs our daily eating experiences by mediating interactions between foods and oral surfaces. These findings identify a specific role for the human OFC in evaluating oral food textures to mediate preference for high-fat foods.
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