Social touch observation in adults with autism: intact neural representations of affective meaning but lack of embodied resonance

Abstract

Humans can easily grasp the affective meaning of touch when observing social interactions.Several neural systems support this ability, including theory of mind (ToM) and somatosensory resonance systems, but it is unclear how these systems are affected in autism spectrum disorder (ASD). Individuals with ASD are characterized by impairments in social interaction and the use of (non)verbal communication such as social and reciprocal touch. The present study applies an ecologically valid stimulus set and multivoxel pattern fMRI neuroimaging to pinpoint atypicalities in the neural circuitry underlying socio-affective touch observation in adults with ASD as compared to matched neurotypical controls. The MVPA results reveal that the affective meaning of touch is well represented in the temporoparietal junction, a core ToM mentalizing area, in both groups. Conversely, only the neurotypical group hosts affective touch representations in the somatosensory cortex, not the ASD group, yielding a significant group difference. Lastly, individuals with a more positive attitude towards receiving, witnessing, and providing social touch and with a higher score on social responsivity, show more differentiated representations of the affective meaning of touch in these somatosensory areas. Together, our findings imply that individuals with ASD are able to cognitively represent the affective meaning of touch, but they lack the spontaneous embodied somatosensory resonance when observing social touch communications. Individual differences in this diminished resonance appear to be related to social touch avoidance and quantitative autism traits. Significance StatementAutism is characterized by socio-communicative impairments, including abnormal processing of interpersonal touch. Little is known about the neural basis of atypicalities in social touch processing in autism. Here, adults with and without autism watched video clips displaying social touch interactions and judged the affective valence of the touch. Subsequently, they underwent functional magnetic resonance imaging while watching the same videos. Brain activity patterns demonstrate that adults with autism show intact cognitive understanding (i.e. "knowing") of observed socio-affective touch experiences but lack of embodied emotional resonance (i.e. "feeling"). This lack of emotional resonance is linked to social touch avoidance and quantitative autism traits. These findings highlight that the depth of experiencing the state of others is shallower in people with autism.