C-tactile fibers mediate Affective Touch: from childhood to individual differences to neural correlates

The emotional aspect of touch has been called ‘Affective Touch’ (AT), a term capturing tactile processing with a hedonic, motivational and social significance (e.g. affiliative behaviors or mother-infant bonding). AT is driven by C-Tactile (CT) fibers that are mainly present in hairy skin and respond specifically to slow, gentle touch. CT fibers project to a neural network including the insular cortex and other areas involved in the social domain. In this thesis, the reader will find three distinct studies that, however, follow a temporal progression that reflects both the way they have been carried out and the logical sequence of the rationale underpinning my doctoral project. In the first study, we studied the development of somatosensation and Affective Touch as central role throughout childhood. In adults, these functions are driven by different, neuroanatomically and functionally segregated fibers. To date, very little is known about the basic features of these fibers in childhood and this lack of knowledge is mirrored in the Affective Touch domain, where there are no studies on the main physiological features of the tactile processes linked to the stimulation of the hairy skin, namely the only body part that modulates Affective Touch. Thus, our study aims to analyse: tactile sensitivity and tactile acuity of children’s hairy forearms; a possible separation between somatosensation and the Affective Touch; and the presence/absence of a mature Affective Touch system already in childhood. To these aims, participants (160 children, aged 6 to 14 years), were administered with the Von Frey (tactile sensitivity) and the 2 Point Discrimination (tactile acuity) tests. Affective Touch was measured following the classic protocol and pleasantness ratings were recorded. Our findings showed a correlation between age and somatosensation, suggesting a progressive reduction of sensitivity and acuity as age grows. Further, there was no overlap between Affective Touch and somatosensation, suggesting a behavioral separation. Lastly, we found higher pleasantness ratings for Affective vs. Neutral stimulations at all ages and an enhanced preference for Affective as age grows. We concluded that both somatosensation and Affective Touch are already present as two separate components of touch in childhood and change as a function of age. In the second and third studies, I investigated the perception of AT on the basis of individual differences. The perception and the neural processing of AT appear to be modulated by psychological and psychopathological factors such as autistic traits, anorexia disorder and attachment patterns. Despite this, nothing is known about the Disorganized attachment pattern which is the one with the highest difficulty in regulating emotions and social skills that are central aspects of the AT network. Our studies aim to compare the perception and brain responses to AT in a sample of adults classified as having a Organized (OA) or a Disorganized attachment (DA). 46 OA and 17 DA individuals (as coded via Adult Attachment Interview) underwent a behavioral tactile procedure for basic somatosensation (comprising Von Frey Monofilaments, 2PD, and thermal sensitivity) and a psychological assessment (including SCL-90-R and PID-5). AT perception was measured applying Affective (AS) and Neutral Stimulations (NS) with a watercolor brush on the forearm, respectively at 3 or 30 cm/s; pleasantness ratings for AS and NS and a index of preference (AT index) were collected. A randomly selected subset of 12 OA and 8 DA underwent also a fMRI block design, during affective and neutral tactile stimulations (four run of 5 repetitions of AS and 5 repetitions of NS each), in addition of two resting-state sessions for a functional connectivity analysis (fc-fMRI). No differences emerged for somatosensation and psychological scales. A MANOVA on AS and NS ratings showed that DA vs OA reported lower ratings for AS and no difference for NS. A t-test on AT index showed that DA vs OA preferred NS. A fMRI F omnibus contrast revealed the involvement of posterior insula (PI), somatosensory primary cortex (S1), supramarginal gyrus (SMG) and amygdala during AS and NS. A 2 (OA vs DA) x 2 (AS vs NS) mixed factorial ANOVA on hemodynamic responses showed an effect of stimulation, with higher activation for NS in PI, S1 and amygdala, and an effect of group, with DA showing higher activation in amygdala. An interaction in amygdala showed higher activation for NS vs AS in DA, but not in OA. fc-fMRI showed connectivity between PI and SMG and PI and S1. Results showed that DA perceived AT as less pleasant and preferred NS compared to OA, suggesting that adults who experience difficulties in the ways to relate to others in the affectivity domain, and, in particular, referring to attachment history, are specifically impaired in AT perception, but not in other basic functions of somatosensation. Altered AT perception appeared to be also mirrored by differences in brain mechanism for processing AT. In fact, we found a higher activation in amygdala for AS and NS in DA compared to OA, suggesting different mechanisms for coding motivational and hedonic aspect of AT. Further studies are needed to understand whether this atypical response to AT refers to attribution of a negative or positive value to these stimuli. The results from my three experiments have shown that it is worth investigating this construct in the future. From a personal point of view, it seems to me that this set of three experiments is a trait d'union between neurosciences, which we all know and fascinate us because of their ability to measure very complex phenomena, and other constructs associated with a more clinical perspective such as attachment. I therefore hope that my doctoral thesis will be a humble contribution to a wider view of clinical and neuroscientific phenomena.