A Causal Role for Gastric Rhythm in Human Disgust Avoidance

Abstract

Rotten food, maggots, bodily waste-all elicit disgust in humans. Disgust promotes survival by encouraging avoidance of disease vectors¹ but is also implicated in prejudice toward minority groups; avoidance of environmentally beneficial foods, such as insect protein; and maladaptive avoidance behavior in neuropsychiatric conditions.^2-5 Unlike fear, pathological disgust is not improved substantially by exposure therapy clinically,⁶ nor in experimental work does behavioral avoidance of disgusting images habituate following prolonged exposure.^7,8 Under normal physiological conditions, perception of disgusting stimuli disrupts myoelectrical rhythms in the stomach,^9-13 inducing gastric dysrhythmias that correlate with neural signatures of disgust.¹¹ However, the causal role of gastric rhythm in disgust avoidance is unknown. We manipulated gastric rhythm using domperidone, a peripheral dopamine D2/D3 antagonist and common anti-emetic, at a dose (10 mg) that acts to convert gastric dysrhythmias to normal rhythms.⁹ In a preregistered, randomized, double-blind, placebo-controlled crossover design in 25 healthy volunteers (aged 18-25), we measured the effects of domperidone on core disgust avoidance, using eye tracking to measure implicit (oculomotor) avoidance of disgusting images (feces) before and after an "exposure" intervention (monetary reinforcement for looking at disgusting images).^7,8 We find that domperidone significantly reduces oculomotor disgust avoidance following incentivized exposure. This suggests that domperidone may weaken the "immunity" of disgust to habituation, putatively by reducing gastric dysrhythmias during incentivized engagement with disgusting stimuli. This indicates a causal role for disgust-related visceral changes in disgust avoidance, supporting the hypothesis that physiological homeostasis contributes to emotional experience.

Keywords: avoidance; disgust; emotion; eye tracking; gastric; gut-brain interaction; interoception; nausea; somatic; visceral.

Figure 1

Experimental Procedure (Disgust Task) Participants visited twice, for domperidone and placebo administration, at least 7 days apart. At each session, we collected eye-tracking data over 24 trials (7 min) at baseline, 30 min after domperidone/placebo administration, and before and after incentivized exposure, when participants were reimbursed for ocular engagement with the disgusting stimulus. Histograms show horizontal eye gaze fixation positions (yellow histography on left indicates the disgusting stimulus; position was randomized in the experiment), weighted by fixation duration. Note that the original stimuli are not licensed for publication; these images are provided for illustration. Control (reward task) administration occurred after baseline measurement and again after post-incentive measurement (not pictured).

Figure 2

Average Dwell Time Proportions for the Disgusting (Yellow) and Neutral (Green) Stimuli and Non-stimulus Fixations (Gray) Shaded areas indicate the within-participant standard error of the mean. Colored boxes above the x axis indicate a significant difference in dwell time proportion between the disgusting and neutral stimuli time for each medication condition (blue, placebo; pink, domperidone; transparent for uncorrected α = 0.05; opaque after for Holm-Bonferroni correction). The subplots correspond to the task phases and histograms in Figure 1. The top-right panel shows the distribution of proportional dwell-time differences (averaged across trials within each block) for placebo (blue) and domperidone (pink). Notches in the boxplots indicate the within-participant 95% confidence interval around the median.