Altered relationship between subjective perception and central representation of touch hedonics in adolescents with autism-spectrum disorder

Irene Perini,Johanna Molander,Håkan Olausson,Robin Kämpe,Per A Gustafsson,Maria Zetterqvist,Kajsa Igelström,Brigita Jasiunaite-Jokubaviciene,Leah M Mayo,Markus Heilig

doi:10.1038/s41398-021-01341-7

Irene Perini, Johanna Molander + Show 8 more

Open Access

https://doi.org/10.1038/s41398-021-01341-7

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Abstract

An impairment of social communication is a core symptom of autism-spectrum disorder (ASD). Affective touch is an important means of social interaction, and C-Tactile (CT) afferents are thought to play a key role in the peripheral detection and encoding of these stimuli. Exploring the neural and behavioral mechanisms for processing CT-optimal touch (~3 cm/s) may therefore provide useful insights into the pathophysiology of ASD. We examined the relationship between touch hedonics (i.e. the subjective pleasantness with which affective touch stimuli are perceived) and neural processing in the posterior superior temporal sulcus (pSTS). This region is less activated to affective touch in individuals with ASD, and, in typically developing individuals (TD), is correlated positively with touch pleasantness. TD and ASD participants received brushing stimuli at CT-optimal, and CT-non-optimal speeds during fMRI. Touch pleasantness and intensity ratings were collected, and affective touch awareness, a measure of general touch hedonics was calculated. As expected, slow touch was perceived as more pleasant and less intense than fast touch in both groups, whereas affective touch awareness was moderately higher in TD compared to ASD. There was a strong, positive correlation between right pSTS activation and affective touch awareness in TD, but not in ASD. Our findings suggest that altered neural coupling between right pSTS and touch hedonics in ASD may be associated with social touch avoidance in ASD.

Highlights

To appreciate a caress might feel like a simple, effortless ability, but extensive neural processing occurs before the caress is “labeled” as welcomed, pleasant, and caring
We demonstrate that autism-spectrum disorder (ASD) participants did not show a correlation between affective touch awareness and neural activity in right posterior superior temporal sulcus (pSTS), whereas this correlation was strong in typically developing control subjects (TD)
We have identified a robust correlation between affective touch awareness and neural activity in right pSTS in TD

Summary

Introduction

To appreciate a caress might feel like a simple, effortless ability, but extensive neural processing occurs before the caress is “labeled” as welcomed, pleasant, and caring. Myelinated Aß afferents promptly carry information about location, speed, and pressure of the caress while C-Tactile (CT) afferents convey speed-dependent information about the pleasantness of the touch. According to the Diagnostic and Statistical Manual of Mental Disorders (DSM-5), autism-spectrum disorder (ASD) encompasses difficulties with social interaction and “restricted, repetitive patterns of behavior, interests, or activities” which may take a form of “hyper- or hyporeactivity to sensory input, or unusual interest in sensory aspects of the environment”[3]. Altered sensory processing in individuals with ASD is observed across all sensory modalities, including tactile, visual, and auditory[4].

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