Abstract
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 magnetic 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.
Highlights
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]
In a 2-by-2-by-2 factorial experimental design combined with functional magnetic resonance imaging, we tested the hypothesis that social signals would improve food healthiness judgement by recruiting key social and emotional areas in the brain
Based on the extant literature, we focused on a set of a priori Regions of interest (ROIs) implicated in social and emotion processing, including limbic/prelimbic areas and the fusiform face area (FFA)
Summary
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]. 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 (e.g.,20,22–29) 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]. Visual social transmission via facial expressions is known to involve limbic/ paralimbic structures, including the amygdala, the anterior cingulate cortex (ACC), and ventral medial prefrontal cortex/orbitofrontal cortex (vmPFC/OFC), and the face-perception network (e.g., the fusiform face area/FFA; cf.[32,33]). Neural evidence concerning olfactory signaling of emotion remains relatively scant, converging evidence has implicated similar key structures of the social and emotion networks, including limbic/prelimbic areas and the FFA26,29,37–40. In a 2-by-2-by-2 (emotion-by-source-by-modality) factorial experimental design combined with functional magnetic resonance imaging (fMRI), we tested the hypothesis that social signals (especially chemosignals) would improve food healthiness judgement by recruiting key social and emotional areas in the brain
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