The maturation of cortical circuits is coordinated by genetic and experience-dependent mechanisms [29]. The susceptibility of developing cortical circuits to environmental factors begins in the womb [30] and this is underscored the capacity of human newborns to immediately interact with their caregivers [7,31,32].
The last trimester of gestation is marked by rapid cortical growth [33,34]. While the premature exposure to the extrauterine environment during this period may interfere with the maturation of association areas and increase the risk of neurodevelopmental impairment [35], the rate of cortical maturation is not synchronous across cortical regions [4,36]. In the primary auditory cortex, for instance, developmental changes in cortical microstructure have largely occurred by 28 weeks of gestation [4]. This differential pattern of cortical maturation might explain why non-primary areas are more vulnerable to disruption due to premature exposure to the extrauterine environment [37,38] while primary areas may experience an acceleration in maturation [9,10]. According to our findings (see Figure 1B), the earlier exposure to extrauterine sound stimulation in late-preterm infants probably speeds up the maturation of auditory cortical circuits and improves the efficiency of auditory input processing in this population during the first months of postnatal life [39].
An earlier study [40] had already reported that P1 latency was similar in one-month-old terms and preterms. However, our study is the first to show that P1 latency in a group of three months old infants is shorter in moderate-to-late preterms (see Figure 1B). Previous works had shown that P1 latency steadily decreases from around 250 ms in one-month-old infants towards 100 ms in adults [41,42]. The smaller P1 latency of preterms in the three-month CA group probably reflects the accelerating maturational effects of early exposure to the extrauterine environment, which usually includes speech stimulation [43].
Other studies had already investigated the effect of preterm birth on the maturation of auditory cortical pathways in pre-schoolers using P1 as a biomarker [44-47]. However, the preterms in those studies were classified as extreme/very-preterm and the poor results they observed in comparison to controls may have been influenced by concurrent clinical conditions associated with extreme prematurity [47].
The neural mechanisms associated with the accelerating effects of preterm birth on the maturation of cortical pathways remain to be determined. One possibility is an increase in the effectiveness of thalamocortical connectivity with the primary auditory cortex [1] due to precocious exposure to the external social environment. A similar effect was reported previously in the primary somatosensory cortex of very preterm infants (GA<33 weeks) following the premature exposure to activities such as breastfeeding and bottle-feeding [10].
A previous study [48] had shown that the latencies of components N1 and P2 are shorter in term than in preterm infants at three months of GA. While this result is the opposite we observed in the present work, we suppose this difference stems from the choice of auditory stimuli and the biomarker for physiological maturation. In that study [48], the stimulus was a click while we used speech stimuli (the phoneme /da/). Also, we used the latency of the P1 component as a biomarker, the gold standard for evaluating the maturation of cortical auditory pathways [17,21,23-25,49-55].
Our results are corroborated by other studies that show the advantages of prematurity in auditory recognition memory [56], binocular vision [9], and language comprehension [57]. Thus, even though preterm birth is associated with many neurodevelopmental risks, especially in small for gestational age (SGA) infants [34], the early exposure to socially relevant stimuli can enhance the maturation of sensory pathways [58]. Though our results differ from studies using visual evoked potentials (VEP) that show that preterm birth negatively affects the development of visual pathways [59, 60], the preterm group in those studies was composed of very preterm infants, which may have been SGA at birth.