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 (n = 4,099 at baseline; n = 3,376 at follow-up [median age = 10.0 (1.1) and 12.0 (1.1) years; n = 2,116 with both assessments]). Reproducible, inverse associations between low-frequency signal and topological fluctuations were estimated (p < 0.05, β = −0.20 to −0.02, 95% CI = [−0.23, −0.001]). Signal (but not topological) fluctuations increased in somatomotor and prefrontal areas with pubertal stage (p < 0.03, β = 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 (p < 0.05, β = −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.

We have investigated pubertal changes in intrinsic signal and network dynamics, estimated from resting-state fMRI in a sample of youth from the Adolescent Brain Cognitive Development (ABCD) study. We have identified reproducible, inverse associations between low-frequency signal and topological fluctuations, as well as pubertal changes in intrinsic signal dynamics but not topological patterns of strongly connected networks. We have also identified sex differences in these dynamics and negative associations with BMI. Several associations between signal and topological fluctuations were in the opposite direction in racial/ethnic minorities compared with those in the entire sample. Our findings indicate that intrinsic signal dynamics change significantly in developed and developing brain regions during puberty, but their strongest synchronization patterns may already be sufficiently developed prior to puberty and are dynamically reproducible.