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.