Disgust represents an evolutionary adaptive protective response and is present in many aspects of our daily life. For example, people may feel disgusted when they drink or eat something distasteful (‘distaste’), see poor hygiene or rotten food (‘core disgust’) or witness someone violating social and moral norms (‘socio-moral disgust’). Evolutionary and disgust appraisal models have long postulated an association between these processes and hypothesized that the subjective experience of core disgust has evolved from the basal distaste response and later been adopted into the social moral domain^1-3. However, a neural evaluation of this hypothesis was precluded by the lack of a precise neurobiological marker that tracks subjective disgust experience in humans.

The neural representation of disgust is inter-related with the brain basis of other defensive responses, for instance, fear⁴ or also general negative affect, however, the shared and separable neurofunctional representations underlying these negative emotions have not been systematically investigated.

We here capitalized on recent methodological advances in multivariate pattern analysis based neural decoding techniques and fMRI to develop an accurate and generalizable whole-brain signature predictive of momentary self-reported subjective disgust experience to address these questions.

A sensitive and comprehensive brain signature for subjective disgust experience

The experience of disgust was induced by visual core disgust stimuli with varying levels of subjective disgust induction e.g., by stimuli showing disgusting situations (Figure 1) while brain activity was recorded using fMRI. To facilitate robust results, we employed a discovery (n=78) and pre-registered validation (n=30) cohort design. Participants were instructed to react naturally to the stimuli and report their momentary level of disgust during each trial on a 5-point Likert scale ranging from 1 (neutral/slightest disgust) to 5 (very strong disgust).

Next, utilizing machine-learning-based neural decoding, we established and validated a comprehensive neurobiological model (visually induced disgust signature, VIDS) for subjective disgust experience. Specifically, the developed VIDS accurately predicted momentary self-reported subjective disgust across discovery and validation cohorts, both on the population-level and individual-level. Moreover, the VIDS robustly generalized across samples, study contexts and MRI systems with regard to accurately capturing disgust experience in response to core disgust stimuli (n=34 and n=26), oral distaste (n=30) and unfair offers in an ultimatum game task (socio-moral disgust; n=43), suggesting that the experience of disgust may extend from the gustatory over the subjective experience and into the socio-moral domain (see also evolutionary models proposed in ref.²).

Subjective disgust is associated with and predicted by distributed neural systems

Previous studies emphasized the contribution of specific brain regions, such as the insula^4,5, amygdala⁴, salience network⁶ and default mode network (DMN)⁷, to subjective disgust experience. Through a series of systematical analyses, we found that capturing disgust experience requires concerted engagement of brain-wide distributed cortical and subcortical systems, while no isolated region or network reached the predictive accuracy of the whole-brain model (i.e., VIDS).

The experience of disgust, fear and non-specific negative affect have shared yet distinguishable neurofunctional representations

In a series of analyses, we further demonstrated that subjective disgust experience showed shared yet separable neural representations with established predictive models for the subjective experience of non-specific negative affect (picture induced negative affect signature, PINES⁸) or fear (visually induced fear signature, VIFS⁹), such that all models engaged subcortical regions and regions implicated in emotional awareness and appraisal, whereas the neural signature of disgust robustly mediated the response of the other two models (PINES and VIFS) on subjective disgust ratings but not vice versa. Although the three neural signatures showed a certain extent of similarity in the range of intense emotional experiences (for a similar observation, see also ref.¹⁰), the signatures most accurately predicted the respective target experience.

Why is this study important?

We provide an accurate fMRI signature for disgust with a high potential to resolve ongoing evolutionary debates (Figure 2). This study adds to the understanding of the neurobiological underpinnings of subjective disgust experience. Disgust dysregulations play a role in a number of mental disorders^11-13, and the resulting subjective disgust marker can be potentially useful to examine novel treatments (for initial applications of MVPA-based decoders in treatment and intervention evaluation, see refs.^14,15).

References

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