Local Gradients of Functional Connectivity Enable Precise Fingerprinting of Infant Brains During Dynamic Development

Brain functional connectivity patterns exhibit distinctive, individualized characteristics capable of distinguishing one individual from others, like fingerprint. Accurate and reliable depiction of individualized functional connectivity patterns during infancy is crucial for advancing our understanding of individual uniqueness and variability of the intrinsic functional architecture during dynamic early brain development, as well as its role in neurodevelopmental disorders. However, the highly dynamic and rapidly developing nature of the infant brain presents significant challenges in capturing robust and stable functional fingerprint, resulting in low accuracy in individual identification over ages during infancy using functional connectivity. Conventional methods rely on brain parcellations for computing inter-regional functional connections, which are sensitive to the chosen parcellation scheme and completely ignore important fine-grained, spatially detailed patterns in functional connectivity that encodes developmentally-invariant, subject-specific features critical for functional fingerprinting. To solve these issues, for the first time, we propose a novel method to leverage the high-resolution, vertex-level local gradient map of functional connectivity from resting-state functional MRI, which captures sharp changes and subject-specific rich information of functional connectivity patterns, to explore infant functional fingerprint. Leveraging a longitudinal dataset comprising 591 high-resolution resting-state functional MRI scans from 103 infants, our method demonstrates superior performance in infant individual identification across ages. Our method has unprecedentedly achieved 99% individual identification rates across three age-varied sub-datasets, with consistent and robust identification rates across different phase encoding directions, significantly outperforming atlas-based approaches with only around 70% accuracy. Further vertex-wise uniqueness and differential power analyses highlighted the discriminative identifiability of higher-order functional networks. Additionally, the local gradient-based functional fingerprints demonstrated reliable predictive capabilities for cognitive performance during infancy. These findings suggest the existence of unique individualized functional fingerprints during infancy and underscore the potential of local gradients of functional connectivity in capturing neurobiologically meaningful and fine-grained features of individualized characteristics for advancing normal and abnormal early brain development.