Reduced neural sensitivity to emotional faces and voices in preterm five-year-olds: a comparative study.

Abstract

Background: Accurate emotion processing is crucial for social development. Preterm birth is associated with neurodevelopmental alterations and increased vulnerability to subtle socio-emotional difficulties, often described within the preterm behavioral phenotype. Previous studies have reported impaired emotion recognition in preterm populations, but have largely relied on behavioral tasks and primarily focused on facial expressions. Because explicit emotion recognition is still developing in early childhood, objective neural markers of implicit emotion discrimination may be particularly informative for early detection.

Methods: We administered a series of frequency-tagging electroencephalography (EEG) paradigms to investigate neural sensitivity to brief changes in emotional expressions in a cohort of five-year-old preterm children (N = 66), and age-matched full-term peers (N = 32). Frequency-tagging EEG utilizes fast periodic stimulation to elicit synchronized brain responses measurable in the frequency domain. Neural sensitivity to changes in emotional expressions was examined in both the visual and auditory modality, using oddball paradigms with neutral faces or voices presented at base frequency and emotional expressions (either fearful or happy) presented as periodic oddballs. Linear mixed models were used to investigate the effects of group, emotion, and prematurity severity.

Results: All children showed implicit neural discrimination between neutral and emotional expressions. Compared to full-term peers, children born before 32 weeks of gestation, but not those born between 33 and 36 weeks of gestation, showed reduced neural sensitivity to facial emotional expression changes. In contrast, all preterm children (< 37 weeks of gestation) showed reduced neural sensitivity to vocal emotional expression changes. Across modalities, reduced neural sensitivity to happy emotional expressions was associated with higher parent-reported social difficulties.

Conclusions: Five-year-old children born preterm show reduced neural sensitivity to brief changes in facial and vocal emotional expressions compared with full-term peers. Strikingly, the impact of prematurity severity differed between the visual and auditory modalities, indicating differential maturation of higher-level visual and auditory processing following preterm birth. These findings contribute to a more detailed understanding of socio-emotional development after preterm birth and highlight the importance of early, modality-sensitive monitoring of socio-emotional development across the entire preterm population.