Expressions of nurturing socio-affiliative behaviors, such as love and affection, are a cornerstone in the development of attachment. Specifically, animal research emphasizes the life-long effects of physical maternal care, including licking and grooming, on nervous system maturation and behavior (Weaver et al., 2004). Indeed, interpersonal touch plays a particularly important role in brain development across a range of species (Ardiel and Rankin, 2010), and is a primary channel mediating social bonding and secure attachment in primates across the lifespan (Harlow, 1958; Dunbar, 2010; Walker and McGlone, 2013).

The temporal lobes contain key nodes of the circuitry supporting social cognition, essential for accurate perception of social cues and healthy development of attachment (Adolphs, 2009; Vrticka and Vuilleumier, 2012; Nolte et al., 2013). The posterior superior temporal sulcus (pSTS) has been identified as particularly sensitive to visually presented social information (Yang et al., 2015). A growing number of studies suggest that the pSTS may also contain multisensory circuits (Beauchamp, 2010), including areas responding to tactile stimulation (Beauchamp et al., 2008). Given the profound role interpersonal touch plays in social interactions and attachment (McGlone et al., 2014), it seems likely that the pSTS may be selectively sensitive to socially relevant tactile information. Indeed, recent studies show that caress-like gentle skin stroking of the forearm activates the right pSTS (Gordon et al., 2013; Voos et al., 2013; Björnsdotter et al., 2014). Moreover, pSTS responses to skin stroking show sex-specific developmental effects (Björnsdotter et al., 2014), correlate inversely with autistic traits (Voos et al., 2013) and are reduced in individuals diagnosed with autism spectrum disorder (Kaiser et al., 2015). Taken together, these findings demonstrate a role of the pSTS in tactile processing, but also link temporal lobe functionality to individual variability in social behavior.

Already at the level of the skin, specific peripheral nerves in the form of small-diameter, unmyelinated C tactile (CT) afferents signal socio-affective dimensions of touch (Löken et al., 2009; Björnsdotter et al., 2010; Morrison, 2012; Ackerley et al., 2014). Contrary to large-diameter myelinated mechanoreceptive (Aβ) afferents, CT nerve fibers respond particularly well to gentle, caress-like slow skin stroking (Löken et al., 2009; Ackerley et al., 2014) but poorly to rapid skin deformation such as vibrotactile stimuli (Bessou et al., 1971; Olausson et al., 2002). Physical touch mediates social bonding and attachment in primates (Harlow, 1958; Dunbar, 2010), and the CT system is posited to play a particularly important role in the development of attachment (McGlone et al., 2014). Moreover, pure CT stimulation evokes a vaguely pleasant percept (Olausson et al., 2002), and CT afferent firing frequency correlates with perceived pleasantness of skin stroking (Löken et al., 2009; Ackerley et al., 2014).

Consistent with a socio-affective role of the CT system, previous studies suggest that posterior temporal lobe regions responsive to touch may be selective to the type of skin stroking that vigorously activates CT afferents. Stroking of the hairy skin of the arm elicits more activity than that of the glabrous skin of the palm (Gordon et al., 2013; Björnsdotter et al., 2014) which is not innervated by CT afferents (Björnsdotter et al., 2010). Also, the STS is more responsive to slow than fast skin strokes (Voos et al., 2013). However, the extent to which the STS is selective to CT targeted stimulation is unclear; specifically, the STS is known to respond to skin vibration (Beauchamp et al., 2008), which poorly activates CT afferents (Bessou et al., 1971; Olausson et al., 2002). In the current study, we therefore used functional magnetic resonance imaging (fMRI) to contrast brain responses to skin stroking and vibration in healthy participants.

In addition to having dissimilar effects on Aβ and CT afferents, skin vibration is an artificial type of touch that is not associated with social processes. The right pSTS is selectively responsive to point-light displays of biological motion, including depictions of human movements compared to randomly moving dots (Grossman and Blake, 2002). Similar to such displays, purposeful gentle skin stroking is an inherently social stimulus, in contrast to vibration, which can be considered an unnatural, non-social type of touch. Consistent with previous studies showing selective activations of the posterior temporal lobe to socially relevant touch (Gordon et al., 2013; Voos et al., 2013; Björnsdotter et al., 2014), we hypothesized that the pSTS would respond more to skin stroking than to skin vibration. Superior temporal cortex activity is also modulated by a wide array of factors related to individual variability, such as social impairment (Kaiser et al., 2010), autism diagnosis (Björnsdotter et al., 2016), perceived level of animacy (Kuzmanovic et al., 2014), and plasma oxytocin (Lancaster et al., 2015). Specifically, temporal responses to skin stroking are affected by age and gender (Björnsdotter et al., 2014), autistic traits (Voos et al., 2013), and autism diagnosis (Kaiser et al., 2015). Here, we asked whether pSTS activity may also be modulated by individual percepts of the affective quality of tactile stimulation. In line with previous studies of the CT system (Olausson et al., 2002; Löken et al., 2009; Ackerley et al., 2014), we therefore asked the participants to rate the perceived pleasantness of the tactile stimuli. Consistent with the role of the pSTS in processing socially relevant touch (Gordon et al., 2013; Voos et al., 2013; Björnsdotter et al., 2014), we hypothesized that pleasantness ratings of skin stroking, but not vibration, would correlate with pSTS responses.

We examined the extent to which posterior temporal lobe responses are selective to socio-affective touch by comparing activity elicited by skin stroking and skin vibration. Contrary to our hypothesis, we found no significant differences between skin stroking and vibration. However, right pSTS responses correlated significantly with participants’ perceived pleasantness of skin stroking, but not vibration. These results suggest that right pSTS responses may indeed be selective to skin stroking, but also that pSTS activity is modulated by individual variability in perceived affective quality of touch.

Our study did not replicate previous findings of significant group level pSTS responses to skin stroking, and skin stroking did not elicit significantly more temporal lobe activity than vibration on the group level. However, the finding of a positive correlation between pleasantness ratings and pSTS responses to skin stroking, but not vibration, suggests that the lacking group level effects may be partially due to statistical issues. Specifically, we applied voxelwise correction for multiple comparisons, which was recently demonstrated to be substantially more conservative than clusterwise correction (Eklund et al., 2016) used in previous studies (Gordon et al., 2013; Voos et al., 2013; Björnsdotter et al., 2014). As such, there may have been STS effects that would have survived a less stringent initial threshold (of e.g., p < 0.005) with clusterwise correction for multiple comparisons, but that did not pass our least stringent voxelwise threshold (p < 0.001). In the current study, we did not assess the effects using less stringent criteria due to the high risk of obtaining type I errors (Eklund et al., 2016). The experimental design, in which stroking and vibration stimuli were interleaved with no interstimulus interval, is less likely to have caused the lacking effect: this design was successfully applied in a similar previous study (Morrison et al., 2011), albeit using a larger number of stimuli repetitions but also substantially fewer participants, and we identified condition differences across a large number of other brain regions previously associated with tactile stimulation at the highly conservative threshold of whole-brain pFWE < 0.05.

In light of potential statistical processing differences, our finding that pSTS responses to skin stroking, but not to vibration, correlate with pleasantness ratings is highly consistent with previous findings of a selective role of the right pSTS in processing socially relevant tactile cues (Gordon et al., 2013; Voos et al., 2013; Björnsdotter et al., 2014). Although vibrotactile stimulation may be linked to social processing – the vibration probe was manually applied by the experimenter, and vibration is becoming increasingly associated with communication through cell phones (Drouin et al., 2012) – our data did not reveal any significant effects in relation to skin vibration. However, since vibrotactile stimuli is known to activate the temporal lobe (Beauchamp et al., 2008), we speculate that paradigms specifically interrogating social processes linked to vibration, such as the behavioral response to the regular repeated buzz of a cell phone call, may detect such effects. Similarly, the current study did not attempt to dissociate social and CT-mediated touch processing, as gentle skin stroking is both the preferred CT stimulus and an inherently social type of touch. Instead, future studies using factorial designs including social/non-social and CT/non-CT mediated touch are required to establish whether the observed effects are related to the social component of touch or to the CT system.

The finding of a correlation between brain responses to skin stroking and pleasantness ratings supports the previously demonstrated link between variability in pSTS processing and social behavior. The superior temporal cortex is modulated by an astonishing variety of individual parameters, including task performance (Herrington et al., 2011), cognitive ability (Rutherford and Troje, 2012), social impairment (Kaiser et al., 2010), perceived animacy (Kuzmanovic et al., 2014), motor skills (Freitag et al., 2008), serotonin transporter genotype (Fisher et al., 2015), and plasma oxytocin (Lancaster et al., 2015). In line with these findings, we speculate that the demonstrated correlation may reflect a range of individual factors related to socio-affective sensory dimensions, rather than varying levels of peripheral input or low-level processing. For instance, early experiences such as frequency of maternal touch (Brauer et al., 2016), attachment-related stress (Nolte et al., 2013), and a range of other attachment-related processes (Vrticka and Vuilleumier, 2012) influence the functioning of social brain regions such as the STS. Since we did not assess these measures in the current study, future studies are needed to disentangle the relative contributions of such factors, as well as to identify additional brain circuits that may contribute to the coding of affective aspects of touch.

Conforming to previous research on the CT system (Löken et al., 2009; Morrison et al., 2011), we asked participants to rate the tactile experience in terms of pleasantness. The term ‘pleasant’ is not sufficiently concise to allow a precise interpretation, however; for example, interpersonal touch may feel pleasant in terms of sensory hedonics (such as ‘softness’) but unpleasant in terms of social aspects (such as ‘unfamiliarity’) (Gentsch et al., 2015). Hence, it is not clear whether the demonstrated correlation reflects a sensory-hedonic or social-affective dimension of the tactile sensation. Since the pSTS is robustly linked to social (Adolphs, 2009), rather than emotional or hedonic processing, we speculate that the observed correlation is primarily governed by a social-affective dimension.

Given the role of the pSTS in integrating sensory and social information (Yang et al., 2015), we further propose that the pSTS may play a role in the translation of neutral tactile stimuli into positively valenced, socially relevant touch. As such, this system may be affected in psychiatric conditions associated with altered social behavior and impaired attachment, including autism spectrum disorder (ASD). Consistent with this notion, just-published findings show reduced right pSTS responses to skin stroking in children with ASD (Kaiser et al., 2015). Socially relevant tactile behaviors extend well beyond skin stroking and caressing, however, including hugging, kissing, tickling, and so on; further studies are required to elucidate any generalized role of the temporal lobes across such behaviors.

Our results support a role for the posterior temporal lobe in processing socio-affective dimensions of touch. Specifically, our study supports the notion that socio-affective touch may be selectively processed in the temporal lobe; however, our results also suggest that any selectivity is contingent on top-down effects related to subjectively perceived qualities of the tactile stimulation.

MD and EJ designed the study and collected data. MD and MB performed the analyses. All authors participated in the interpretation of the data. MD an MB drafted the article. All authors contributed to the final revision of the article.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.