The Dual Nature of Early-Life Experience on Somatosensory Processing in the Human Infant Brain

Abstract

Every year, 15 million preterm infants are born, and most spend their first weeks in neonatal intensive care units (NICUs) [1]. Although essential for the support and survival of these infants, NICU sensory environments are dramatically different from those in which full-term infants mature and thus likely impact the development of functional brain organization [2]. Yet the integrity of sensory systems determines effective perception and behavior [3, 4]. In neonates, touch is a cornerstone of interpersonal interactions and sensory-cognitive development [5-7]. NICU treatments used to improve neurodevelopmental outcomes rely heavily on touch [8]. However, we understand little of how brain maturation at birth (i.e., prematurity) and quality of early-life experiences (e.g., supportive versus painful touch) interact to shape the development of the somatosensory system [9]. Here, we identified the spatial, temporal, and amplitude characteristics of cortical responses to light touch that differentiate them from sham stimuli in full-term infants. We then utilized this data-driven analytical framework to show that the degree of prematurity at birth determines the extent to which brain responses to light touch (but not sham) are attenuated at the time of discharge from the hospital. Building on these results, we showed that, when controlling for prematurity and analgesics, supportive experiences (e.g., breastfeeding, skin-to-skin care) are associated with stronger brain responses, whereas painful experiences (e.g., skin punctures, tube insertions) are associated with reduced brain responses to the same touch stimuli. Our results shed crucial insights into the mechanisms through which common early perinatal experiences may shape the somatosensory scaffolding of later perceptual, cognitive, and social development.

Keywords: development; infant; pain; parent; preterm; sensory; tactile; touch.

Figure 1

Normative analysis of ERPs from full-term infants. A. Photos of a full-term infant undergoing EEG recording (left) and the tubing and nozzle for delivering calibrated light touch to the hand (right). B. Superimposed ERPs to touch and sham stimuli (black and red traces, respectively). C. Significant ERP differences began at 184ms post-stimulus onset (percentage of significant electrodes across time shown). D. Hierarchical topographic clustering identified a series of touch-related ERP components (shaded boxes); the earliest, 171–240ms, was the focus of the present analyses. e. 24 bilateral electrodes were at the maxima/minima of the blue ERP topography, and measures from these were used in subsequent analyses. For term patient characteristics see Table S1.

Figure 2

Impaired ERP responses to light touch in preterm infants. A. Group-averaged ERPs from full-term and preterm infants (black and red traces, respectively; s.e.m. shown) at a left frontal scalp site. B. Overlay of ERPs from the entire electrode montage. Insets show mean ERP topographies over the 171–240ms period (top view) when significant differences were observed (Table 1). C. The orange curve displays the spatial correlation between ERPs from full-term vs. preterm infants. The blue area displays statistically significant differences in ERP topography, indicative of differences in the active brain circuits in responses from full-term vs. preterm infants. Corresponding data and analyses in response to sham stimuli are shown in d–f. No statistically reliable differences were observed. For preterm patient characteristics see Table S1.