Affective touch awareness in mental health and disease relates to autistic traits – An explorative neurophysiological investigation
Introduction
Interpersonal touch is highly important for human interaction and “provides the most emotional of our tactile experiences” (Gallace and Spence, 2010). Touch is sensed from the very first moments of life, when the newborn is comforted by the mother´s embrace and remains pivotal during the whole lifespan (Sehlstedt et al., 2015). Interpersonal touch is not only a powerful way to convey emotions between individuals (Hertenstein et al., 2006), but also decreases stress perception (Grewen et al., 2003) and stress related cortisol response (Ditzen et al., 2007). Moreover, even subtle interpersonal touch can have strong behavioral consequences: Waiters for instance receive higher tips when touching their customers (Crusco and Wetzel, 1984), basketball players perform better the more they touch each other at the beginning of the season (Kraus et al., 2010), and being touched by a nurse decreases levels of stress before surgery (Whitcher and Fisher, 1979). Taken together, interpersonal touch has a pronounced function in social behavior, such as the creation and strengthening of bonds (for review see (McGlone et al., 2014) and (Gallace and Spence, 2010)).
The ability to process and perceive the whole range of tactile stimulations may be a precondition for the creation of social bonds and in consequence for the maintenance of mental health. Indeed, a positive attitude towards interpersonal touch is negatively correlated to social reticence (Fromme et al., 1989) and socially high-anxious people experience interpersonal touch more aversive than low anxious ones (Wilhelm et al., 2001). Individuals with autism, a disorder involving the lack of functional social interaction, are known to dislike interpersonal touch and 70% of those also exhibit tactile sensory-perceptual abnormalities (Baranek et al., 2006). An interesting study on postnatal depression further showed, that such mothers have problems in creating a rewarding tactile interaction with their baby, which leads to decreased positive response in the babies (Malphurs et al., 1996).
Interestingly, research from the last decade opens new possibilities to examine the processing and perception of tactile stimulations. This research shows that there is a group of unmyelinated afferent nerve fibers, which are specialized in the detection of interpersonal touch. These so called C tactile afferents are located in the hairy skin of the body and respond to slowly moving, caressing types of touch (Löken et al., 2009). They respond optimally at a stimulus temperature of about 32 °C, i.e. similar to human skin temperature (Ackerley et al., 2014b). The C tactile fibers do not only have distinct response properties, but also project to distinct brain areas, mainly to the posterior insula cortex (Björnsdotter et al., 2009). Further, C tactile targeted stimuli activate regions known to be involved in reward processing such as the putamen and the orbitofrontal cortex (Sailer et al., 2016; Olausson et al., 2002), and regions implied in processing of social stimuli, such as the social superior temporal sulcus (Bennett et al., 2013, Voos et al., 2013a).
Microneurography recordings from nerves innervating the human forearm skin show that C tactile fibers respond optimally to stimulation with a velocity of 1–10 cm/s; stimulations performed with a velocity of 0.3 cm/s or slower or with a velocity of 30 cm/s or faster are less effective in activating C tactile fibers and especially fast stimulation does not excite those fibers (Ackerley et al., 2014b, Löken et al., 2009, Olausson et al., 2010). Accordingly, light, slow stroking stimulation performed with a velocity of about 1–10 cm/s is perceived more pleasant than stimulation with a fast velocity of 30 cm/s or with a superslow velocity of 0.1 or 0.3 cm/s. With those response characteristics, C tactile fibers are highly sensitive to human interpersonal stroking touch (Olausson et al., 2010). The velocity dependent pleasantness rating curve has been replicated several times - on different body parts (Ackerley et al., 2014a), with handheld as well as robot guided stroking stimulation (Triscoli et al., 2013), and for touch in various visual (Ellingsen et al., 2013) or olfactory conditions (Croy et al., 2014). However, there are individual differences, which suggest that several top-down modulatory processes play a substantial role in the subjective perception of the afferent information carried by C tactile fibers. While most people strongly prefer slow over fast stroking, some are rather indifferent. We hypothesize that any abnormalities in C tactile touch perception are likely seen in the domain of social behavior and mental health.
Although studies on touch in psychiatric disorders are rare, it has been reported that adults with autism are more sensitive than healthy controls to certain aspects of touch including vibration, texture perception and thermal pain (Cascio et al., 2008). There are a few published examinations on C tactile processing and autism. Those show that the perception and cortical processing of slow stroking, C tactile targeted stimuli is reduced in adults with high traits of autism compared to adults with low autistic scores (Voos et al., 2013), and in autistic compared to normally developed children (Kaiser et al., 2015). In line, recent findings point in the direction, that autism is related to small fiber loss - affecting C tactile fibers (Silva and Schalock, 2016). A study in mice further shows that experimental reduction of peripheral tactile sensitivity leads to enhanced anxiety behavior and reduced social interaction in mice (Orefice et al., 2016).
Here, we examined if C tactile perception is abnormal in a broader range of mental disorders and if such abnormality might provide a functional biomarker of mental disease. In order to capture the effect of a variety of mental disorders on affective touch perception, an explorative study was set up including patients with various diseases and symptom severity. As adverse childhood experience is related to mental disorders (Anda et al., 2006), childhood experience was further assessed in all participants.
Section snippets
Participants
Seventy patients presenting to outpatient psychotherapy (60 women, 10 men, aged 24–70 years, mean 46.0±12.0 years SD) were included in the study. The patients were recruited by four psychotherapists and diagnosed by their attending psychotherapist according to the international classification of mental and behavioral disorders, version 10 (Dilling et al., 1991). The sample was unbalanced in gender reflecting the distribution in outpatient psychotherapy. The majority of patients suffered from
Patients liked touch less, but there were no group differences in affective touch awareness or in hedonic perception of control pictures
There was a significant main effect of velocity (F[137,4]=72.9, p<0.001, ŋ2=0.35), with velocities in the intermediate range being rated as more pleasant compared to fast or very slow velocities (Fig. 1), and there was a significant quadratic fit of the pleasantness curve (F[138,1]=191.6, p<0.001, ŋ2=0.58). Ratings differed significantly between groups (F[138,1]=5.9, p=0.018, ŋ2=0.04), with patients rating touch less pleasant compared to controls. However, there was no significant interaction
Discussion
Both patients and healthy comparison subjects showed the expected velocity dependent pleasantness curve for brush stroking, indicating that C tactile targeted stroking velocities were preferred over slower and faster velocities (Löken et al., 2009). However, patients rated touch generally less pleasant than comparison subjects. This effect was especially pronounced in patients with disorders of personality. The attenuation of overall pleasantness of touch might be due to specific reductions of
Acknowledgements
This study was supported by a grant of the Marcus och Amalia Wallenbergs Minnesfond to IC (MAW 2014.000).
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