Relationship-specific Encoding of Social Touch in Somatosensory and Insular Cortices

Juulia T Suvilehto,Ville Renvall,Lauri Nummenmaa

doi:10.1016/j.neuroscience.2020.09.015

Juulia T Suvilehto, Ville Renvall + Show 1 more

Open Access

https://doi.org/10.1016/j.neuroscience.2020.09.015

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Abstract

Humans use touch to maintain their social relationships, and the emotional qualities of touch depend on who touches whom. However, it is not known how affective and social dimensions of touch are processed in the brain. We measured haemodynamic brain activity with functional magnetic resonance imaging (fMRI) from 19 subjects (10 males), while they were touched on their upper thigh by either their romantic partner, or an unfamiliar female or male confederate or saw the hand of one of these individuals near their upper thigh but were not touched. We used multi-voxel pattern analysis on pre-defined regions of interest to reveal areas that encode social touch in a relationship-specific manner. The accuracy of the machine learning classifier to identify actor for both feeling touch and seeing hand exceeded the chance level in the primary somatosensory cortex, while in the insular cortex accuracy was above chance level only for the touch condition. When classifying the relationship (partner or stranger), while keeping the toucher sex fixed, amygdala (AMYG), orbitofrontal cortex (OFC), and primary and secondary somatosensory cortices were able to discriminate toucher significantly above chance level.These results suggest that information on the social relationship of the toucher is processed consistently across several regions. More complex information about toucher identity is processed in the primary somatosensory and insular cortices, both of which can be considered early sensory areas.

Highlights

Touch is the most intimate form of interpersonal communication
We considered all regions of interest (ROI) used in one classification task to be a family of tests for the multiple comparison correction
Our main finding was that naturalistic social touch is coded in a relationship-specific manner in the primary somatosensory cortices as well as in the insular cortex

Summary

INTRODUCTION

Touch is the most intimate form of interpersonal communication. Both humans (Suvilehto et al, 2015) and nonhuman primates manage their social relations by means of mutual grooming or touching (Dunbar, 1991). Prior studies on neural processing of naturalistic social touch have manipulated the belief of the subjects regarding who is touching them, while in reality the toucher was always the same person They found that both experiencing and anticipating touch from a female experimenter modulated activity in the primary somatosensory cortex distinctly from when the subjects believed they were being touched or anticipated being touched by a male experimenter (Gazzola et al, 2012; Scheele et al, 2014). Intranasal oxytocin selectively enhances the neural response in the insular cortex, OFC and anterior cingulate cortex for female touch (Scheele et al, 2014) When subjects believed they were touched by their romantic partner or a stranger of the opposite sex (i.e. the same sex as their partner), relationship-specific responses to touch were observed in the orbitofrontal, posterior cingulate, and somatosensory cortices (Kreuder et al, 2017). We expected to replicate the earlier findings of differential cortical activation in the primary somatosensory cortex and orbitofrontal cortices for touch from male and female stranger, in line with Gazzola et al (2012), and for touch from partner and stranger, in line with Kreuder et al (2017) and extend these findings by differentiating between the effect of gender and the social relationship

Participants

RESULTS

DISCUSSION

Limitations and future directions