Human chemosignals of disgust facilitate food judgment

Yan Zheng, Yuqi You, Ana R. Farias, Jessica Simon, Gün R. Semin, Monique A. Smeets, Wen Li
2018 Scientific Reports  
Choosing food is not a trivial decision that people need to make daily, which is often subject to social influences. Here, we studied a human homolog of social transmission of food preference (STFP) as observed in rodents and other animals via chemosignals of body secretions. Human social chemosignals (sweat) produced during a disgust or neutral state among a group of donors were presented to participants undergoing a 2-alternative-forced-choice food healthiness judgment task during functional
more » ... agnetic resonance imaging (fMRI). Response speed and two key signal detection indices-d' (discrimination sensitivity) and β (response bias)-converged to indicate that social chemosignals of disgust facilitated food healthiness decisions, in contrast to primary disgust elicitors (disgust odors) that impaired the judgment. fMRI analyses (disgust vs. neutral sweat) revealed that the fusiform face area (FFA), amygdala, and orbitofrontal cortex (OFC) were engaged in processing social chemosignals of disgust during food judgment. Importantly, a double contrast of social signaling across modalities (olfactory vs. visual-facial expressions) indicated that the FFA and OFC exhibited preferential response to social chemosignals of disgust. Together, our findings provide initial evidence for human STFP, where social chemosignals are incorporated into food decisions by engaging social and emotional areas of the brain. Every day, people make decisions about what to eat and what not to eat, exercising a keen effort on determining whether specific foods are healthy or not 1,2 . Through social media or personal conversations, food information is frequently offered and actively sought. In fact, social communication of food choices runs across the phylogeny. Non-primate animals use chemical secretions to communicate edibility and food choices among conspecifics 3-6 . In a well-established phenomenon of social transmission of food preference (STFP), mice would prefer a food consumed by other mice but only after smelling olfactory cues (e.g., carbon disulfide/CS 2 on the breath of the other mice) 7,8 . The olfactory system is intrinsically associated with feeding 9 and so it makes good sense that olfaction serves as an effective medium for food-related communication 8, 10 . Often deemed as a minor sensory system in comparison to other species, human olfaction nonetheless is documented behaviorally and neurally to possess extraordinary capacity for odor analysis 11-13 . For example, humans can potentially discriminate more than a trillion odors, way beyond their ability to discriminate colors (2.3-7.5 million) and tones (~340,000 11 ). Furthermore, while visual cues seem to dominate human interactions, it is also true that a certain degree of modality-selectivity exists in social communication such that some sensory channels are better suited for transmitting some messages than others 14-17 ). For example, touch predominantly communicates intimacy and complex emotions such as gratitude and sympathy while faces outperform in conveying basic emotions. We hypothesized that owing to its inherent association with feeding, the olfactory sense would be a privileged channel for food-related communication via human social chemosignals. Human body odor, extracted largely from sweat, is a primary form of human social chemosignal, which has been shown to carry a wide range of information (e.g., [18] [19] [20] [21] . The recently flourishing research field on the communicative function of chemosignals has revealed that after smelling another person's sweat produced during various behavioral and emotional states (e.g., anxious, fearful, or disgust), the receiver would display a simulacrum of the states and exhibit changes in cognition, affect, and behavior accordingly (e.g., 20, [22] [23] [24] [25] [26] [27] [28] [29] ). Among these emotions, disgust is a unique, ancient response to food, which is rooted in olfaction (and gustation), prompting an individual to avoid spoiled or poisonous food 30,31 . Therefore, sweat secreted in a disgust state could be a particularly useful social chemosignal for food and diet screening across people.
doi:10.1038/s41598-018-35132-w fatcat:3v2yrpbwwrdrdfkbrua3xeto24