Developmental and Aging Changes in Brain Network Switching Dynamics Revealed by EEG Phase Synchronization

Abstract

Adaptive behavior depends on the brains capacity to vary its activity across multiple spatial and temporal scales. Yet, how distinct facets of this variability evolve from childhood to older adulthood remains poorly understood, limiting mechanistic models of neurocognitive aging. Here, we characterize lifespan neural variability using an integrated empirical-computational approach. We analyzed high-density EEG cohort data spanning 111 healthy individuals aged 9-75 years, recorded at rest and during passive and attended auditory oddball stimulation task. We extracted scale-dependent measures of EEG fluctuations amplitude and entropy, together with millisecond-resolved phase-synchrony networks in the 2-20 Hz range. Multi-condition partial least squares decomposition analysis revealed two independent lifespan trajectories. First, slow-frequency power, variance and complexity at longer timescales declined monotonically with age, indicating a progressive dampening of low-frequency fluctuations and large-scale coherence. Second, the temporal organization of phase-synchrony reconfigurations followed an inverted U-trend: young adults exhibited the slowest yet most diverse switching--characterized by low mean but high variance and low kurtosis of jump lengths at 2-6 Hz and the opposite pattern at 8-20 Hz--whereas children and older adults showed faster, more stereotyped dynamics. To mechanistically account for these patterns, we fitted a ten-node phase-oscillator model constrained by the human structural connectome. Only an intermediate, metastable coupling regime reproduced the empirical combination of reduced low-frequency variability and maximally heterogeneous synchrony dynamics observed in young adults, while deviations toward weaker or stronger coupling mimicked the childrens and older adults profiles. Our results demonstrate that development and aging entail changes in the switching dynamics of EEG phase synchronization, by differentially sculpting stationary and transient aspects of neural variability. This establishes time-resolved phase-synchrony metrics as sensitive, mechanistically grounded markers of neurocognitive status across the lifespan. Author summaryBrain activations fluctuate and synchronize according to functionally relevant patterns, both at rest and during task performance. Here we investigated how these fluctuations change from childhood to older adulthood and what do these changes reveal about healthy development and aging. Using electrophysiological brain activity recordings from 111 participants aged 9 to 75 years during rest and a cognitive task, we discovered two key developmental trajectories. First, a linear trend reflecting mainly a gradual weakening of slower brain rhythms with age. Second, an inverted U-shaped trend suggesting that neural flexibility peaks in young adults, who switch between neural synchronization states in a uniquely diverse yet controlled ways, whereas children and older adults showed more rigid and predictable patterns. To explain this, we developed a computational model. The simulated data confirmed that young adults operate in a "sweet spot" of connectivity--balanced enough to support dynamic coordination without becoming unstable or overly rigid--unlike in childhood and older age, where connectivity becomes either too weak or too strong. Our work shows that age fundamentally reshapes how flexibly brain regions communicate. This gives us sensitive markers for tracking brain health across life.