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.