open access publication

Article, 2024

Navigating Pubertal Goldilocks: The Optimal Pace for Hierarchical Brain Organization

Advanced Science, ISSN 2198-3844, Volume 11, 21, Page 2308364, 10.1002/advs.202308364

Contributors

Szakács, Hanna 0000-0001-5081-7535 [1] [2] Mutlu, Murat Can 0000-0003-2933-6985 [3] [4] Balestrieri, Giulio [5] Gombos, Ferenc 0000-0001-6000-1820 [2] [6] Braun, Jochen 0000-0002-8886-078X [3] [4] Kringelbach, Morten Lindtner 0000-0002-3908-6898 [7] [8] Deco, Gustavo 0000-0002-8995-7583 [5] [9] Kovács, Ilona 0000-0002-1772-2697 (Corresponding author) [6] [10]

Affiliations

  1. [1] Semmelweis University
  2. [NORA names: Hungary; Europe, EU; OECD];
  3. [2] Pázmány Péter Catholic University
  4. [NORA names: Hungary; Europe, EU; OECD];
  5. [3] Center for Behavioral Brain Sciences
  6. [NORA names: Germany; Europe, EU; OECD];
  7. [4] Otto-von-Guericke University Magdeburg
  8. [NORA names: Germany; Europe, EU; OECD];
  9. [5] Pompeu Fabra University
  10. [NORA names: Spain; Europe, EU; OECD];

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.

Keywords

adolescents, age, alpha, alpha frequency range, associative brain regions, asymmetry, bone, bone age, brain, brain development, brain networks, brain organization, brain regions, chronological age, configuration, connection, cortical organization, decelerated maturation, degree, degree of maturity, development, developmental progression, dimensions, direction, direction of information flow, duration, electroencephalography, females, flow, frequency range, group, hierarchical brain organization, hierarchical order, hierarchical organization, hierarchically, high-density electroencephalography, influence, information flow, levels, levels of hierarchical organization, maturation, maturational tempo, maturational trajectories, mature stage, measured asymmetry, network, objective, optimal pace, order, organization, pacing, participant groups, process, progression, pubertal progression, range, region, results, skeletal maturity, stage, tempo, temporal dimension, temporal dynamics, time processing, timeline, trajectory

Funders

  • National Research, Development and Innovation Office

Data Provider: Digital Science