Functional networks in the infant brain during sleep and wake states

Abstract

Functional brain networks are assessed differently early in development than at maturity: infants are almost universally scanned during sleep, whereas adults are typically scanned awake while resting or performing tasks. Observed differences between infant and adult functional networks may thus reflect these differing states of consciousness rather than or in addition to developmental changes. We explore this question by comparing functional networks in fMRI scans acquired from infants during natural sleep and awake movie-watching. As a reference, we also acquired fMRI scans in adults during awake rest and awake movie-watching. Whole-brain functional connectivity was more similar within-state (sleep-sleep, wake-wake) than across-state (sleep-wake) in infants, demonstrating that movies elicit a different network configuration than typical sleep acquisitions. Indeed, a classifier trained on patterns of functional connectivity during infant sleep versus wake robustly decoded the state of additional infants and even generalized to decode rest versus movie in adults; interestingly, a classifier trained on rest versus movie in adults did not generalize nearly as well to sleep versus wake in infants. Moreover, the overall level of similarity between infant and adult functional connectivity was modulated by adult state (stronger for movie than rest) but not infant state (equivalent for sleep and wake). Nevertheless, the network connections that drove similarity between infants and adults, particularly in frontoparietal network, were modulated by infant state. In sum, infant functional connectivity can differ between sleep and wake states, highlighting the potential value of awake data for studying the early development of functional brain networks. Significance statementFunctional networks in the infant brain provide a foundation for early cognitive abilities and act as a marker of brain maturation and developmental disorders. What we know about these networks comes from fMRI data acquired during sleep, given the challenges of awake infant fMRI. This contrasts with the dominant approach in older populations of assessing networks during awake rest or tasks. These differing levels of consciousness cloud the interpretation of developmental changes. Here we show that whole-brain functional connectivity differs between sleeping and awake infants, and that the similarity of these infant states to adults loads on dissociable network connections. This research suggests that a full understanding of early functional brain networks will benefit from complementary insights in awake infants.