Rotten to the core–a neural signature of subjective core disgust generalizes to sociomoral contexts

749 

Abstract Submission 

Xianyang Gan^1,2, Feng Zhou³, Ting Xu^1,2, Xiaobo Liu⁴, Ran Zhang^1,2, Zihao Zheng^1,2, Xi Yang⁵, Xinqi Zhou⁶, Fangwen Yu^1,2, Jialin Li⁷, Ruifang Cui^1,2, Lan Wang^1,2, Jiajin Yuan⁶, Dezhong Yao^1,2, Benjamin Becker^1,2,8,9

¹Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China, Chengdu, China, ²The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Chengdu, China, ³Faculty of Psychology, Southwest University, Chongqing, China, ⁴McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, Canada, ⁵Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, Netherlands, ⁶Institute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu, China, ⁷Max Planck School of Cognition, Leipzig , Germany, ⁸State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong, China, ⁹Department of Psychology, The University of Hong Kong, Hong Kong, China

Xianyang Gan  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Feng Zhou  
Faculty of Psychology, Southwest University
Chongqing, China

Ting Xu  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Xiaobo Liu  
McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University
Montreal, Canada

Ran Zhang  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Zihao Zheng  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Xi Yang  
Faculty of Health, Medicine and Life Sciences, Maastricht University
Maastricht, Netherlands

Xinqi Zhou  
Institute of Brain and Psychological Sciences, Sichuan Normal University
Chengdu, China

Fangwen Yu  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Jialin Li  
Max Planck School of Cognition
Leipzig , Germany

Ruifang Cui  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Lan Wang  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Jiajin Yuan  
Institute of Brain and Psychological Sciences, Sichuan Normal University
Chengdu, China

Dezhong Yao  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation
Chengdu, China|Chengdu, China

Benjamin Becker  
Sichuan Provincial People's Hospital, University of Electronic Science and Technology of China|The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation|State Key Laboratory for Brain and Cognitive Sciences, The University of Hong Kong|Department of Psychology, The University of Hong Kong
Chengdu, China|Chengdu, China|Hong Kong, China|Hong Kong, China

Recent affective and clinical neuroscience perspectives propose a paradigm shift towards subjective and conscious emotional experiences (Kyzar et al, 2023; LeDoux et al., 2017; Wager et al., 2018; Zhou et al., 2021). However, neurobiological models that accurately describe the respective neural representations are scarce. Disgust originates in the hard-wired mammalian distaste reflex, but in humans its conscious emotional experience is strongly shaped by subjective appraisal and may extend to sociomoral contexts. Here, we combined functional MRI with recent methodological advances in multivariate pattern analytic neural decoding techniques to develop an accurate and generalizable whole-brain signature predictive of momentary self-reported subjective disgust experience, and in turn utilize the neural disgust signature to test the evolutionary perspective on disgust.

First, consistent with methods evaluated in previous studies developing neuroaffective decoders (Chang et al., 2015; Zhou et al., 2021), we employed a linear support vector regression model to identify a whole-brain signature of fMRI activation predictive of self-reported disgust experience elicited by core disgust stimuli using data from a discovery cohort (n=78). The performance of the resultant visually induced disgust signature (VIDS) was then evaluated across multiple core disgust datasets: the discovery (10×10-fold cross-validation), validation (n=30), and generalization (n=26) cohorts. Next, we determined which brain regions and systems contribute to the whole-brain disgust prediction through a bootstrap test (Kohoutová et al., 2020) and the computation of model encoding maps (Haufe et al., 2014), and we further tested whether isolated regions or networks traditionally involved in disgust such as the insula or default mode network were sufficient to predict subjective disgust experience. Moreover, functional decoding analysis based on Neurosynth was also conducted to evaluate the neurobiological validity of the developed VIDS. We next systematically examined the functional specificity of the VIDS by conducting predictive comparisons with established decoders for subjective fear (VIFS; Zhou et al., 2021) and negative affect (PINES; Chang et al., 2015), respectively. Finally, we tested the evolutionary perspective on disgust by applying the decoders in fMRI experiments on gustatory distaste (n=30) and sociomoral disgust (fairness norm violations; n=43).

The results showed that the developed VIDS (Fig. 1a) accurately predicted momentary self-reported subjective disgust across three core disgust datasets (Fig. 1b,c,d), such that the averaged within-subject correlation between predicted and true disgust ratings was ≥0.88 in all cases and classification accuracies between different disgust levels were high (≥76%). The conscious experience of disgust is represented in distributed subcortical and cortical systems (Fig. 1e), and the contribution of insula (Fig. 1f) and large-scale networks (Fig. 1g) show lower predictive accuracy compared to the VIDS. More interestingly, the functional decoding analysis supported the disgust signature as a biologically plausible disgust model (Fig. 1h). The three affective decoders most accurately predicted the respective target experience, and the VIDS moreover outperformed the VIFS and PINES in predicting disgust experience in response to both gustatory distaste and sociomoral disgust (unfair offers) as revealed by both prediction accuracy and effect size (for more details see Gan et al., 2023).

The present study developed a sensitive neural signature for subjective disgust experience, which robustly generalizes across core disgust, gustatory distaste, and sociomoral contexts. The neural basis of subjective disgust is encoded in multiple distributed brain systems rather than isolated brain regions. We provide an accurate fMRI-signature for disgust with a high potential to resolve ongoing evolutionary debates.

Emotional Perception ¹

Activation (eg. BOLD task-fMRI)

Classification and Predictive Modeling ²

BOLD fMRI

Other - Disgust; unfairness; moral; gustatory distaste; neural decoding; fMRI; multivariate pattern analysis; emotion; subjective; neural signature