Navigating pubertal goldilocks: the optimal pace for hierarchical brain organization

Szakács, Hanna; Mutlu, Murat Can; Balestrieri, Giulio; Gombos, Ferenc; Braun, Jochen; Kringelbach, Morten L.; Deco, Gustavo; Kovács, Ilona

doi:http://dx.doi.org/10.1002/advs.202308364

Navigating pubertal goldilocks: the optimal pace for hierarchical brain organization

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Szakács H, Mutlu MC, Balestrieri G, Gombos F, Braun J, Deco G, et al. Navigating pubertal goldilocks: the optimal pace for hierarchical brain organization. Adv Sci. 2024 Jun 5;11(21):2308364. DOI: 10.1002/advs.202308364

Abstract

Adolescence is a timed process with an onset, tempo, and duration. Nevertheless, the temporal dimension, especially the pace of maturation, remains an insufficiently studied aspect of developmental progression. The primary objective is to estimate the precise influence of pubertal maturational tempo on the configuration of associative brain regions. To this end, the connection between maturational stages and the level of hierarchical organization of large-scale brain networks in 12-13-year-old females is analyzed. Skeletal maturity is used as a proxy for pubertal progress. The degree of maturity is defined by the difference between bone age and chronological age. To assess the level of hierarchical organization in the brain, the temporal dynamic of closed eye resting state high-density electroencephalography (EEG) in the alpha frequency range is analyzed. Different levels of hierarchical order are captured by the measured asymmetry in the directionality of information flow between different regions. The calculated EEG-based entropy production of participant groups is then compared with accelerated, average, and decelerated maturity. Results indicate that an average maturational trajectory optimally aligns with cerebral hierarchical order, and both accelerated and decelerated timelines result in diminished cortical organization. This suggests that a “Goldilocks rule” of brain development is favoring a particular maturational tempo.