Somatosensory Evoked Potentials Reveal Reduced Embodiment of Emotions in Autism

Abstract

Consistent with current models of embodied emotions, this study investigates whether the somatosensory system shows reduced sensitivity to facial emotional expressions in autistic compared with neurotypical individuals, and whether these differences are independent from between-group differences in visual processing of facial stimuli. To investigate the dynamics of somatosensory activity over and above visual carryover effects, we recorded EEG activity from two groups of autism spectrum disorder (ASD) or typically developing (TD) humans (male and female), while they were performing a facial emotion discrimination task and a control gender task. To probe the state of the somatosensory system during face processing, in 50% of trials we evoked somatosensory activity by delivering task-irrelevant tactile taps on participants' index finger, 105 ms after visual stimulus onset. Importantly, we isolated somatosensory from concurrent visual activity by subtracting visual responses from activity evoked by somatosensory and visual stimuli. Results revealed significant task-dependent group differences in mid-latency components of somatosensory evoked potentials (SEPs). ASD participants showed a selective reduction of SEP amplitudes (P100) compared with TD during emotion task; and TD, but not ASD, showed increased somatosensory responses during emotion compared with gender discrimination. Interestingly, autistic traits, but not alexithymia, significantly predicted SEP amplitudes evoked during emotion, but not gender, task. Importantly, we did not observe the same pattern of group differences in visual responses. Our study provides direct evidence of reduced recruitment of the somatosensory system during emotion discrimination in ASD and suggests that this effect is not a byproduct of differences in visual processing.

SIGNIFICANCE STATEMENT The somatosensory system is involved in embodiment of visually presented facial expressions of emotion. Despite autism being characterized by difficulties in emotion-related processing, no studies have addressed whether this extends to embodied representations of others' emotions. By dissociating somatosensory activity from visual evoked potentials, we provide the first evidence of reduced recruitment of the somatosensory system during emotion discrimination in autistic participants, independently from differences in visual processing between typically developing and autism spectrum disorder participants. Our study uses a novel methodology to reveal the neural dynamics underlying difficulties in emotion recognition in autism spectrum disorder and provides direct evidence that embodied simulation of others' emotional expressions operates differently in autistic individuals.