Dynamic fluctuations of intrinsic brain activity are associated with consistent topological patterns in puberty and are biomarkers of neural maturation

Intrinsic brain dynamics play a fundamental role in cognitive function, but their development is incompletely understood. We investigated pubertal changes in temporal fluctuations of intrinsic network topologies (focusing on the strongest connections and coordination patterns) and signals, in an early longitudinal sample from the Adolescent Brain Cognitive Development (ABCD) study, with resting-state fMRI (<i>n</i> = 4,099 at baseline; <i>n</i> = 3,376 at follow-up [median age = 10.0 (1.1) and 12.0 (1.1) years; <i>n</i> = 2,116 with both assessments]). Reproducible, inverse associations between low-frequency signal and topological fluctuations were estimated (<i>p</i> < 0.05, <i>β</i> = -0.20 to -0.02, 95% confidence interval (CI) = [-0.23, -0.001]). Signal (but not topological) fluctuations increased in somatomotor and prefrontal areas with pubertal stage (<i>p</i> < 0.03, <i>β</i> = 0.06-0.07, 95% CI = [0.03, 0.11]), but decreased in orbitofrontal, insular, and cingulate cortices, as well as cerebellum, hippocampus, amygdala, and thalamus (<i>p</i> < 0.05, <i>β</i> = -0.09 to -0.03, 95% CI = [-0.15, -0.001]). Higher temporal signal and topological variability in spatially distributed regions were estimated in girls. In racial/ethnic minorities, several associations between signal and topological fluctuations were in the opposite direction of those in the entire sample, suggesting potential racial differences. Our findings indicate that during puberty, intrinsic signal dynamics change significantly in developed and developing brain regions, but their strongest coordination patterns may already be sufficiently developed and remain temporally consistent.