Caregiver-infant interactions selectively shape emerging functional connectivity in the neonatal brain

Abstract

From birth, human infants engage in multi-modal social exchanges with caregivers that involve the coordination of gaze and touch to guide attention and support neurodevelopment. However, little is known about the association between these first interactive experiences and the functional organization of the developing brain during the first postnatal month, a window of remarkable brain growth in humans. We address this gap by combining microanalytic coding of caregiver- infant interactions with task-free functional connectivity (FC), measured using high-density diffuse optical tomography (HD-DOT) in infants homes during the first postnatal month. Task-free FC measures the intrinsic functional organization of the developing brain, shedding light on the early development of neural systems supporting perception, regulation, and social interactions. Infants were assessed up to three times (1 week, 2 weeks, 1 month), enabling characterization of both early FC and its rapid developmental change. Caregiver-infant interactions were associated with both concurrent organization and rapid longitudinal change in FC. Dyadic engagement in the context of face-to-face interaction was associated with the refinement of short-range connectivity and the integration of long-range connectivity particularly between social brain regions, while affectionate touch was associated with general increases in long-distance connectivity. These results demonstrate that caregiving experiences influence the development of the brains functional architecture in the first postnatal month, highlighting a critical window for shaping infant brain function. Significance StatementThe first postnatal weeks are a period of rapid brain development, when the brain may be especially sensitive to experience. A key early experience is social interaction between infants and their caregivers, yet it remains unknown if these interactions influence neonate brain function. By combining observations of caregiver-infant interactions at one month with repeated home-based brain imaging, we show that variations in dyadic engagement and affectionate touch influence how infant brain functional connectivity is organized and develops. These findings highlight the importance of supporting perinatal life and early interactions for infant brain development.