Preferences for fat, sugar, and oral-sensory food qualities in monkeys and humans

Abstract

In humans and other primates, food intake depends on sophisticated, individualized preferences for nutrients and oral-sensory food qualities that guide decision-making and eating behavior. The neural and behavioral mechanisms for such primate-typical food preferences remain poorly understood, despite their importance for human health and their targeting by pharmacological obesity treatments. Here, we review a series of experiments that investigated how the biologically critical properties of foods-their nutrients (sugar, fat, protein) and oral-sensory qualities (viscosity, oral sliding friction)-influence food preferences in monkeys and humans. In an economic nutrient-choice paradigm, macaques flexibly trade nutrients and oral-sensory food qualities against varying food amounts, consistent with the assignment of subjective values. Nutrient-value functions that link objective nutrient content to subjective values accurately model these preferences, predict choices across contexts, and explain individual differences. The monkeys' aggregated choice patterns resulting from their nutrient preferences lead to daily nutrient balances that deviate from dietary reference points, resembling suboptimal human eating patterns when exposed to high-calorie foods. To investigate the sensory basis underlying nutrient values, we developed novel engineering tools that quantify food textures on oral surfaces, using fresh pig tongues. Oral-texture (i.e., mouthfeel) parameters, including viscosity and sliding friction, were shown to mediate monkeys' preferences for high-fat foods. When translated to human subjects, this approach revealed a neural mechanism for preferring high-fat foods from oral texture in the orbitofrontal cortex (OFC)-a key reward system of the brain. Importantly, human OFC responses to oral sliding friction in individual subjects-measured in the MRI scanner-predicted subsequent fat intake in a naturalistic, life-like eating test. These findings suggest that a primate nutrient-reward paradigm offers a promising approach for investigating the behavioral and neural mechanisms for human-typical food reward and food choice, to advance understanding of human eating behavior, overeating, and obesity.

Keywords: Dieting; Food choice; Nonhuman primates; Nutrients; Obesity; Oral texture; Reinforcement learning.