Preferences for nutrients and sensory food qualities identify biological sources of economic values in monkeys

Fei-Yang Huang,Michael P F Sutcliffe,Fabian Grabenhorst

doi:10.1073/pnas.2101954118

Fei-Yang Huang, Michael P F Sutcliffe + Show 1 more

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https://doi.org/10.1073/pnas.2101954118

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Abstract

Value is a foundational concept in reinforcement learning and economic choice theory. In these frameworks, individuals choose by assigning values to objects and learn by updating values with experience. These theories have been instrumental for revealing influences of probability, risk, and delay on choices. However, they do not explain how values are shaped by intrinsic properties of the choice objects themselves. Here, we investigated how economic value derives from the biologically critical components of foods: their nutrients and sensory qualities. When monkeys chose nutrient-defined liquids, they consistently preferred fat and sugar to low-nutrient alternatives. Rather than maximizing energy indiscriminately, they seemed to assign subjective values to specific nutrients, flexibly trading them against offered reward amounts. Nutrient-value functions accurately modeled these preferences, predicted choices across contexts, and accounted for individual differences. The monkeys' preferences shifted their daily nutrient balance away from dietary reference points, contrary to ecological foraging models but resembling human suboptimal eating in free-choice situations. To identify the sensory basis of nutrient values, we developed engineering tools that measured food textures on biological surfaces, mimicking oral conditions. Subjective valuations of two key texture parameters-viscosity and sliding friction-explained the monkeys' fat preferences, suggesting a texture-sensing mechanism for nutrient values. Extended reinforcement learning and choice models identified candidate neuronal mechanisms for nutrient-sensitive decision-making. These findings indicate that nutrients and food textures constitute critical reward components that shape economic values. Our nutrient-choice paradigm represents a promising tool for studying food-reward mechanisms in primates to better understand human-like eating behavior and obesity.

Highlights

Value is a foundational concept in reinforcement learning and economic choice theory
Two liquids were pseudorandomly selected from a 2 × 2 factorial design with fat and sugar level as factors (Fig. 1B and SI Appendix, Table S1): the low-fat low-sugar liquid (LFLS), the high-fat low-sugar liquid (HFLS), the low-fat highsugar liquid (LFHS), and the high-fat high-sugar liquid (HFHS)
The LFLS liquid was lowest in energy content; the HFLS and LFHS liquids were matched in energy content at an intermediate level; and the HFHS liquid was highest in energy content

Summary

Introduction

Value is a foundational concept in reinforcement learning and economic choice theory. Values integrate past reward experiences to guide future behavior [3, 4] These theories have been critical for revealing how choices depend on factors such as probability, risk, and delay [2, 4, 5], they do not explain how values and preferences are shaped by particular properties of the choice objects themselves. Biology conceptualizes choice objects as rewards with well-defined components that benefit survival and reproductive success and endow rewards with value [4] We followed this approach to investigate how the biologically critical, intrinsic properties of foods—their nutrients and sensory qualities—influence values inferred from behavioral choices and help explain individual differences in preference. Previous studies in macaques uncovered key reward functions and their neuronal implementations, including the assignment of values to choice options [13, 18,19,20,21,22,23,24,25], reinforcement learning [4, 26]

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