Developmental relationships between the human alpha rhythm and intrinsic neural timescales are dependent on neural hierarchy

Maturation of human brain structure has been well-studied, but developmental changes to brain physiology are not as well understood. One consistent finding is that the peak alpha rhythm frequency (PAF) increases throughout childhood. Another is that resting-state functional connectivity shifts from sensorimotor regions in children to association regions in adolescents, a reorganization along a hierarchy called the sensorimotor-to-association (S-A) axis. In mature brains, the S-A axis has been parcellated physiologically using the duration of persistent neural activity, known as the intrinsic neural timescale (INT), which increases along the hierarchy. Here, we studied the development of PAF and INT in a cohort of patients with epilepsy 3-33 yr of age undergoing intracranial electrocorticographic (ECoG) monitoring. Given the well-known developmental trajectory of PAF, and the ability to delineate hierarchy using INT, we hypothesized that changes to PAF and INT would correlate across development, but that their relationship may be influenced by hierarchy. Consequently, we predicted that age-dependent PAF increases would accompany INT decreases, and we tested whether their relationship varied between sensorimotor and association regions. We found that PAF increased significantly with age in both sensorimotor and association regions, whereas age-dependent INT decreases were only significant in association regions. Supporting this finding, we found a significant negative relationship between PAF and INT in association regions, but not sensorimotor regions. Together, our results provide further evidence that developmental divisions across the S-A axis manifest in the relationships between neurophysiological measures.<b>NEW & NOTEWORTHY</b> We report a novel developmental relationship between the human resting-state alpha rhythm frequency and the duration of intrinsic neural timescales. Using resting-state electrocorticography, we found that alpha frequency increased with age at either end of the sensorimotor-to-association cortical hierarchy, whereas intrinsic neural timescales only decreased with age in association regions. This negative correlation between alpha frequency and intrinsic timescale was only evident in association regions, further linking functional maturation and cortical hierarchy.