Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3DY, United Kingdom.
Department of Experimental Psychology, University of Oxford, Oxford OX1 3TA, United Kingdom.
J Neurosci. 2023 Nov 22;43(47):8000-8017. doi: 10.1523/JNEUROSCI.1473-23.2023.
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 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. Fat and sugar enhance the reward value of food by imparting a sweet taste and rich mouthfeel but also contribute to overeating and obesity. Here we used a novel food-engineering approach to realistically quantify the physical-mechanical properties of high-fat liquid foods on oral surfaces and used functional neuroimaging while volunteers sampled these foods and placed monetary bids to consume them. We found that a specific area of the brain's reward system, the orbitofrontal cortex, detects the smooth texture of fatty foods in the mouth and links these sensory inputs to economic valuations that guide eating behavior. These findings can inform the design of low-calorie fat-replacement foods that mimic the impact of dietary fat on oral surfaces and neural reward systems.
虽然高脂肪食物的过度摄入是体重增加的一个主要驱动因素，但将饮食脂肪的口腔感觉特性与奖励评估和进食行为联系起来的神经机制仍不清楚。在这里，我们结合新的食品工程方法和功能神经影像学，表明人类眶额皮层（OFC）将高脂肪食物的口腔感觉转化为指导进食行为的主观经济价值。男性和女性志愿者品尝和评估了营养控制的液体食物，这些食物的脂肪和糖含量不同（“奶昔”）。在口腔食物加工过程中，OFC 活动编码了一个特定的口腔感觉参数，该参数介导了食物脂肪含量对奖励价值的影响：滑动摩擦系数。具体来说，OFC 对口中食物的反应反映了脂肪液体在口腔表面产生的光滑、油性质地（即口感）。OFC 中独特的活动模式编码了与特定食物相关的经济价值，这反映了滑动摩擦与其他食物特性（糖、脂肪、粘度）的主观整合。至关重要的是，OFC 对口腔质地的神经敏感性预测了个体在自然进食测试中的脂肪偏好：OFC 对脂肪相关口腔质地更敏感的个体在进食过程中消耗了更多的脂肪。我们的研究结果表明，人类大脑的奖励系统从口腔滑动摩擦中感知膳食脂肪，这是一种机械食物参数，可能通过调节食物与口腔表面之间的相互作用来控制我们的日常进食体验。这些发现确定了人类 OFC 在评估口腔食物质地以介导对高脂肪食物的偏好方面的特定作用。脂肪和糖通过赋予甜味和丰富的口感来提高食物的奖励价值，但也会导致暴饮暴食和肥胖。在这里，我们使用了一种新的食品工程方法来真实地量化高脂肪液体食物在口腔表面的物理机械特性，并在志愿者品尝这些食物并出价消费时使用功能神经影像学。我们发现，大脑奖励系统的一个特定区域，即眶额皮层，检测到口中高脂肪食物的光滑质地，并将这些感官输入与指导进食行为的经济价值联系起来。这些发现可以为设计模仿饮食脂肪对口腔表面和神经奖励系统影响的低卡路里脂肪替代食品提供信息。
