Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex

Carmelo M Vicario, Robert D Rafal, Sara Borgomaneri, Riccardo Paracampo, Ada Kritikos, Alessio Avenanti, Carmelo M Vicario, Robert D Rafal, Sara Borgomaneri, Riccardo Paracampo, Ada Kritikos, Alessio Avenanti

Abstract

The tongue holds a unique role in gustatory disgust. However, it is unclear whether the tongue representation in the motor cortex (tM1) is affected by the sight of distaste-related stimuli. Using transcranial magnetic stimulation (TMS) in healthy humans, we recorded tongue motor-evoked potentials (MEPs) as an index of tM1 cortico-hypoglossal excitability. MEPs were recorded while participants viewed pictures associated with gustatory disgust and revulsion (i.e. rotten foods and faces expressing distaste), non-oral-related disgusting stimuli (i.e. invertebrates like worms) and control stimuli. We found that oral-related disgust pictures suppressed tM1 cortico-hypoglossal output. This tM1 suppression was predicted by interindividual differences in disgust sensitivity. No similar suppression was found for disgusting invertebrates or when MEPs were recorded from a control muscle. These findings suggest that revulsion-eliciting food pictures trigger anticipatory inhibition mechanisms, possibly preventing toxin swallowing and contamination. A similar suppression is elicited when viewing distaste expressions, suggesting vicarious motor inhibition during social perception of disgust. Our study suggests an avoidant-defensive mechanism in human cortico-hypoglossal circuits and its 'resonant' activation in the vicarious experience of others' distaste. These findings support a role for the motor system in emotion-driven motor anticipation and social cognition.

Keywords: disgust; emotion recognition; motor-evoked potentials; tongue motor area; transcranial magnetic stimulation.

© The Author (2016). Published by Oxford University Press. For Permissions, please email: journals.permissions@oup.com.

Figures

Fig. 1.
Fig. 1.
Disgust-related and positive visual stimuli. The figure shows examples from the food, invertebrate and face categories that were presented in different blocks: ‘A’ disgusting food; ‘B’ positive food; ‘C’ disgusting invertebrate; ‘D’ positive invertebrate; ‘E’ disgusted expression; ‘F’ positive expression. In each food, invertebrate and face block, participants were also exposed to a fixation cross (neutral control).
Fig. 2.
Fig. 2.
MEP amplitudes recorded from the tongue (upper panel) and the ECR (lower panel). In the food block, tongue MEPs were reduced for disgusting foods relative to positive (pleasant food) and neutral (fixation cross) conditions. In the face block, tongue MEPs were reduced for faces expressing disgust relative to positive (happy expressions) and neutral (fixation) conditions. No difference in tongue MEPs was found in the invertebrate block. No difference in ECR MEPs was found for any of the three blocks. Error bars denote SEM. Asterisks (*) indicate P < 0.05.
Fig. 3.
Fig. 3.
Simple correlation between disgust sensitivity (measured by the DS-R score) and the magnitude of tM1 suppression detected when seeing pictures related to gustatory disgust (indexed by the mean MEP contrast for disgusting foods and facial expressions of distaste).

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