1. Introduction
In the beginning of life, mother-infant interactions are characterized
by nonverbal communication. Especially during the first year of life,
one key nonverbal channel through which mothers communicate affection to
their infants is touch (Field et al., 2007). It plays a key role in
early affective mother-infant exchanges and lays the foundation of
lifelong socio-emotional wellbeing (Cekaite, 2016; Yoshida & Funato,
2021). Several studies have shown the importance of early physical
contact highlighting different positive neurodevelopmental outcomes such
as heart rate stabilization and arousal regulation, decreased risk of
infections, improved regulatory as well as social learning abilities
(Björnsdotter et al., 2009; Croy, Drechsler, et al., 2016; Feldman et
al., 2010; Mariani Wigley, 2021; Tuulari et al., 2019c; Van Puyvelde et
al., 2019, 2021).
Studies on adults highlighted that skin stroking activates low-threshold
mechanoreceptors and myelinated fast-conducting Aβ fibers. These fibers
innervate the entire body, including both glabrous and hairy skin, and
play a critical role in coding discriminative properties of touch, such
as thermal, nociceptive, chemical and pruritic stimuli. Aβ fibers target
contralateral primary (SI) and bilateral secondary (SII) somatosensory
cortices (McGlone et al., 2014). Even if these fibers are not fully
mature in infancy, they are capable of conveying tactile stimulation at
early stages of life (Williams et al., 2015). In preterm and term-born
infants, for example, a palm stimulation activates infants’ postcentral
gyrus (Arichi et al., 2012) while the stimulation of the plantar surface
of the foot yields activations in primary sensory areas in two-week-old
infants (Williams et al., 2015).
In addition, gentle skin stoking activates a particular group of
mechanosensitive neurons, the so called C-tactile (CT) fibres, which
innervate exclusively hairy skin (McGlone et al., 2014). CT afferents
are unmyelinated, slow-conducting, and tuned to respond to specific
thermo-mechanical properties of a tactile stimulation that resembles a
caress-like touch, typically made by a human hand (i.e., velocities
between 1−10 cm/s and temperatures of 32° C). As a result, it has been
hypothesized that CT-fibres encode socio-affective dimensions of touch.
In the mature nervous system, gentle skin stroking evokes the activation
of posterior insular cortex, the primary target of CT-fibres (Olausson
et al., 2002). More recently, insular sensitivity to gentle skin
stroking has been detected also in full-term infants of 2-5 weeks of
age, suggesting that CT system functions early in infancy (Tuulari et
al., 2019a). However, while neural correlates of affective touch in
early infancy have already been investigated (Jonsson et al., 2018;
Tuulari et al., 2019a), the potential effect of infants sex on brain
activation remains unexplored.
Sexual dimorphism is known to affect several aspects of brain
development and the maturation of the social brain. Female neonates make
more eye contact (Leeb & Rejskind, 2004), are more likely to orient to
faces and human voices (Connellan et al., 2000) and exhibit a better
discrimination of emotional expression than males (McClure, 2000).
Although some sex differences have been detected also in relation to
affective touch (Björnsdotter et al., 2014; Schirmer & McGlone, 2019)
(e.g., females often perceive affective touch as more pleasant compared
to males), the role of sex in brain processing of caress-like touch
remains poorly understood, and regarding neonates, unknown. Early
differences in the neural processing of a social cue, such as affective
touch, may explain later-life differentiations in cognitive and social
development and therefore call for investigation.
In the light of this evidence, it emerges that caress-related neural
activity plays an important role in shaping social functioning and
stress regulation from the earliest moments of life. In this regard,
although we have already shown that the infant’s brain is responsive to
affective touch soon after birth and highlighted the activation of brain
regions related to CT-fibers and affective touch processing (posterior
insular and somatosensory cortices) (Tuulari et al., 2019c), it remains
crucial to further characterize brain mechanisms related to affective
touch in early infancy (Björnsdotter et al., 2014).
In the present study, we therefore extended our previous work with
infants (Tuulari et al., 2019c) by exploring whether sex could affect
neural responses to affective touch using fMRI in order to capture also
subcortical activations otherwise impossible to catch with surface-based
neuroimaging techniques. Specifically, like in previous studies, we
examined caress-like, gentle skin stroking, a type of tactile
stimulation intimately associated with social interaction and
affectionate touch (Croy, Geide, et al., 2016). Moreover, we conducted a
psychophysiological interactions (PPI) and a seed-based connectivity
(SCA) analysis in order to investigate connectivity networks related to
gentle brushing.