Autistic traits are associated with diminished neural response to affective touch

Abstract

'Social brain' circuitry has recently been implicated in processing slow, gentle touch targeting a class of slow-conducting, unmyelinated nerves, CT afferents, which are present only in the hairy skin of mammals. Given the importance of such 'affective touch' in social relationships, the current functional magnetic resonance imaging (fMRI) study aimed to replicate the finding of 'social brain' involvement in processing CT-targeted touch and to examine the relationship between the neural response and individuals' social abilities. During an fMRI scan, 19 healthy adults received alternating blocks of slow (CT-optimal) and fast (non-optimal) brushing to the forearm. Relative to fast touch, the slow touch activated contralateral insula, superior temporal sulcus (STS), medial prefrontal cortex (mPFC), orbitofrontal cortex (OFC) and amygdala. Connectivity analyses revealed co-activation of the mPFC, insula and amygdala during slow touch. Additionally, participants' autistic traits negatively correlated with the response to slow touch in the OFC and STS. The current study replicates and extends findings of the involvement of a network of 'social brain' regions in processing CT-targeted affective touch, emphasizing the multimodal nature of this system. Variability in the brain response to such touch illustrates a tight coupling of social behavior and social brain function in typical adults.

Affective and non-affective touch evoke differential brain responses in 2-month-old infants

“…The largest statistical difference between slow and fast stroking is located in the insula. The activated regions found in the present study coincide with areas that are activated by affective stroking touch in adults, such as S2, posterior insula and STS (Olausson et al, 2002;Gordon et al, 2013;Voos et al, 2013;Bennett et al, 2014;Kaiser et al, 2015). Interestingly, the cortical activation cluster found in the current study further overlaps with areas that process emotional speech in naturally sleeping 3-7 month old infants as shown in an fMRI study and with areas shown, using fNIRS, to process socially relevant visual stimuli at 5 months of age (Lloyd-Fox et al, 2009).…”

“…Brain regions involved in processing affective, slow stroking, touch in adults include the secondary somatosensory cortex (S2), insular cortex, insular operculum, temporoparietal junction, superior temporal sulcus (STS), amygdala, striatum, orbitofrontal cortex and pregenual anterior cingulate cortex (Olausson et al, 2002;Lindgren et al, 2012;Gordon et al, 2013;Voos et al, 2013;Bennett et al, 2014;Kaiser et al, 2015;Perini et al, 2015;Case et al, 2016). A recent meta-analysis further revealed that affective touch differs from discriminative touch processing with a higher likelihood of activation of the posterior insula and S2 (Morrison, 2016).…”

An Oxytocin-Induced Facilitation of Neural and Emotional Responses to Social Touch Correlates Inversely with Autism Traits

“…At the whole-brain level, under PLC treatment the caress touch stimulus, compared with the close physical proximity control condition, produced widespread activations in the social touch-processing network (Gazzola et al, 2012;Gordon et al, 2013;Lindgren et al, 2012;Lovero et al, 2009;McCabe et al, 2008;Morrison et al, 2011;Voos et al, 2013) including bilateral inferior parietal lobule, insula, somatosensory cortex, pACC, and OFC (Supplementary Tables S2 and S3). By contrast, and in line with previous research (Lovero et al, 2009), the paracentral lobule was significantly deactivated during touch.…”

“…The absence of comparable associations between AQ scores and OFC activation in the PLC session in the current study may reflect both methodological and subject differences. For example, Voos et al (2013) brushed the right forearm instead of both legs, they did not instruct their subjects to rate the pleasantness of each trial in the scanner and, perhaps most importantly, more than half of their subjects were female. Despite these differences, however, the same inclination for socially less competent individuals with higher AQ scores to exhibit a diminished response to pleasant touch occurred in both studies.…”

“…The neural underpinnings of human interpersonal touch are now attracting increasing interest, with recent functional magnetic resonance imaging (fMRI) studies (Gordon et al, 2013;Lindgren et al, 2012;Lovero et al, 2009;McCabe et al, 2008;Rolls et al, 2003;Voos et al, 2013) stressing the role of the pregenual anterior cingulate cortex (pACC) and orbitofrontal cortex (OFC) in coding its emotional value. Unmyelinated, C-tactile afferent fibers are sensitive to social touch (Loken et al, 2009) and project to the insula (Morrison et al, 2011), although recently the primary somatosensory cortex (SI) has also been shown to have an important role in the affective processing of touch (Gazzola et al, 2012).…”