Emotional Appraisal Is Influenced by Cardiac Afferent Information

Marcus A. Gray, Felix D. Beacher, Ludovico Minati, Yoko Nagai, Andrew H. Kemp, Neil A. Harrison, Hugo D. Critchley

Influential models highlight the central integration of bodily arousal with emotion. Some emotions, notably disgust, are more closely coupled to visceral state than others. Cardiac baroreceptors, activated at systole within each cardiac cycle, provide short-term visceral feedback. Here we explored how phasic baroreceptor activation may alter the appraisal of brief emotional stimuli and consequent cardiovascular reactions. We used functional MRI (fMRI) to measure brain responses to emotional face stimuli presented before and during cardiac systole. We observed that the processing of emotional stimuli was altered by concurrent natural baroreceptor activation. Specifically, facial expressions of disgust were judged as more intense when presented at systole, and rebound heart rate increases were attenuated after expressions of disgust and happiness. Neural activity within prefrontal cortex correlated with emotionality ratings. Activity within periaqueductal gray matter reflected both emotional ratings and their interaction with cardiac timing. Activity within regions including prefrontal and visual cortices correlated with increases in heart rate evoked by the face stimuli, while orbitofrontal activity reflected both evoked heart rate change and its interaction with cardiac timing. Our findings demonstrate that momentary physiological fluctuations in cardiovascular afferent information (1) influence specific emotional judgments, mediated through regions including the periaqueductal gray matter, and (2) shape evoked autonomic responses through engagement of orbitofrontal cortex. Together these findings highlight the close coupling of visceral and emotional processes and identify neural regions mediating bodily state influences on affective judgment.