Discussion
In the present study we examined neural correlates to gentle skin stroking of hairy skin in early infancy. We found neural activity patterns similar to Tuulari et al (2019) and different brain responses between males and females. Specifically, compared to males, females exhibited stronger neural activation in bilateral OFC, right ventral striatum and bilateral inferior striatum, pons and cerebellum. Moreover, exploratory PPI analysis revealed differences in males and females in task-dependent functional connectivity considering left-OFC as seed region. Between-group comparisons revealed that females had stronger functional connectivity between the left-OFC and the bilateral somatosensory cortex, cingulate cortex and precuneus. Our findings highlight a sexually dimorphic development of neural processing of affective touch.
In the sexual differentiation of the human brain, different factors (e.g., genetic, hormonal, environment) interact to each other resulting in a variety of anatomical and functional brain differences between the two sexes (Proverbio, 2021). Pre an postnatal differences in testosterone concentration between males and females, for example, have been found to affect brain physiology also modulating dendritic growth, brain receptors, neurogenesis and gliogenesis (McCarthy et al., 2012). As a result, differences in brain activity and functional connectivity patterns could be explained as a result of sexual dimorphic development.
In this regard, our results shown that, while gentle brush stimulation evokes the activation of different brain areas known to be related to neural processing of affective touch, gender differentiation addresses different brain regions. Specifically, in the whole sample (N = 18) and in the smaller one (N = 13), gentle brushing evoked the activation of somatosensory and insular cortices, the two brain regions known as main targets of CT-fibers and a stronger neural activation in bilateral OFC in females (Björnsdotter et al., 2009, 2014; Tuulari et al., 2019b). A significant activation of OFC is corroborated by several previous studies which outlined that gentle touch activates this region in addition to posterior insular and somatosensory cortices (Lamm et al., 2015; McGlone et al., 2012). Moreover, in adults the activation of OFC correlates with the subjective pleasantness of touch as well as with rewarding stimuli from different modalities (Rolls et al., 2003). We also found a stronger activation in ventral striatum cortices that has already been found in response to gentle touch in adolescents (May et al., 2014). OFC and ventral striatum cortices are key components of the brain’s reward circuit. As CT-fibres encode the reward value associated with close physical contact, one could speculate that affective touch could be a more rewarding stimulus for females and that this result could be related to the stronger “social attitude” often linked to the female sex since early infancy (Connellan et al., 2000; Leeb & Rejskind, 2004; McClure, 2000; Mutlu et al., 2013).
Concerning PPI analysis, we revealed in females a widespread functional connectivity between the left-OFC and the bilateral somatosensory cortex, cingulate cortex and precuneus. The components of the human posterior medial cortex, the posterior cingulate cortex (PCC) and precuneus have been implicated in different tasks such as attention, memory, emotion, self-relevance detection and reward evaluation, and are considered key hubs of the default-mode-network (DMN). Interestingly, while the DMN in adults consists in two major rich-club hubs such as the medial-PFC and the PCC, previous studies with infants have outlined that posterior regions of the default-mode-network (i.e. the PCC) are predominant at early stages of life (Xiao et al., 2016). Thus, our results are in line with previous studies highlighting connectivity patterns related to the PCC and precuneus in infancy (Xiao et al., 2016) but also link those to OFC activation.
Finally, the left OFC has been identified as a key hub in sensory integration. Neurophysiological recordings in non-human primate and neuroimaging studies in humans have found that the OFC is activated by auditory, gustatory, olfactory, somatosensory and visual inputs. As already mentioned, gentle skin stroking also activates Aβ fibers which target contralateral primary (SI) and bilateral secondary (SII) somatosensory cortices (McGlone et al., 2014). It would be tempting to conclude that the synchronous activation of the left OFC and somatosensory cortices are implicated in encoding the sensory value of affective touch. However, in the early stages of life, brain networks likely have different functions as compared to the corresponding networks in older infants or adults, which complicates the interpretation (Power et al., 2010).
Before concluding, the present findings have to be considered in light of the following limitation: first, despite previous studies have shown detectable responses to a range of sensory stimuli in sleeping infants (Graham et al., 2015; Williams et al., 2015), it is unclear if and how sleep affects brain processing of tactile stimuli. Second, the sample size of the present study was relatively small, although within the range of previously published fMRI activation studies (Graham et al., 2015). Third, despite manual application dominates fMRI studies of affective touch in adults (Björnsdotter et al., 2009, 2014; Gordon et al., 2013; Morrison et al., 2011; Olausson et al., 2008), it added a source of uncontrolled variability within and between participants. Fourth, we used an echo time of 30 ms, whereas recent research in infant neuroimaging shows that longer echo times (∼50 ms) substantially improve sensitivity (Gursul et al., 2018). Fifth, given the highly limited fMRI time allowed by the Ethics Committee (6 min) in combination with the high risk of data loss due to motion, we opted for collection of robust main effect of slow skin stroking with no control condition. Future studies are encouraged to include a control condition (e.g., fast stroking) to determine whether the observed effects are selective to slow skin stroking. Finally, the current sample is cross-sectional and does not address brain developmental trajectories; future follow-up studies within the FinnBrain Birth Cohort Study may allow for clarification of the maturation of sensory processing in further detail, as well as its practical implications for child development.