Infant EEG microstate dynamics relate to fine-grained patterns of infant attention during naturalistic play with caregivers

Abstract

As infants grow, they develop greater attentional control during interactions with others, shifting from patterns of attention primarily driven by caregivers (exogenous) to those that are also self-directed (endogenous). The ability to endogenously control attention during infancy is thought to reflect ongoing brain development and is influenced by patterns of joint attention between infant and caregiver. However, whether measures of infant attentional control and caregiver behavior during infant-caregiver interactions relate to patterns of infant brain activity is unknown and key for informing developmental models of attentional control. Using data from 43 infant-caregiver dyads, we quantified patterns of visual attention with dyadic, head-mounted eye tracking during infant-caregiver play and associated them with the duration of infant EEG microstate D/4 measured during rest. Importantly, microstate D/4 is a scalp potential topography thought to reflect the organization and function of attention-related brain networks. We found that microstate D/4 associated positively with infant-led joint attention rate but did not associate with caregiver-led joint attention rate, suggesting that infants initiatives in joint attention during play may be critical for the neurobiological development of attentional control. Further, we found that microstate D/4 associated negatively with infant attention shifts rate and positively with infant sustained attention duration, suggesting that increased stability of microstate D/4 may reflect maturation of attentional control and its underlying neural substrates. Together, our findings provide novel insights into how infant attentional control abilities and infant-caregiver visual behavior during play are associated with the spatial and temporal dynamics of infant brain activity. Significance StatementThe ability to control attention endogenously during infancy has been associated with individual differences in future language skills and executive and self-regulatory functions. However, how the infant brain supports the development of attentional control is unknown. Using dyadic, head-mounted eye tracking during infant-caregiver play with toys and microstate analysis of infant EEG during resting state, we found associations between measures of attentional control and brain activity underlying attention-related brain networks. Specifically, our findings suggest that longer durations of EEG microstate D/4 may reflect the maturation of attention-related brain networks that support the development of infant attentional control. This is the first study to provide insight into the functional significance of microstate D/4 in relation to real-world behavior during infancy.