Optimization of energy state transition trajectory supports the development of executive function during youth
- University of Pennsylvania, United States
- Indiana University, United States
- University of Electronic Science and Technology, China
- University of California, Riverside, United States
Abstract
Executive function develops during adolescence, yet it remains unknown how structural brain networks mature to facilitate activation of the fronto-parietal system, which is critical for executive function. In a sample of 946 human youths (ages 8-23y) who completed diffusion imaging, we capitalized upon recent advances in linear dynamical network control theory to calculate the energetic cost necessary to activate the fronto-parietal system through the control of multiple brain regions given existing structural network topology. We found that the energy required to activate the fronto-parietal system declined with development, and the pattern of regional energetic cost predicts unseen individuals' brain maturity. Finally, energetic requirements of the cingulate cortex were negatively correlated with executive performance, and partially mediated the development of executive performance with age. Our results reveal a mechanism by which structural networks develop during adolescence to reduce the theoretical energetic costs of transitions to activation states necessary for executive function.
Data availability
The PNC data is publicly available in the Database of Genotypes and Phenotypes: accession number: phs000607.v3.p2; https://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/study.cgi?study_id=phs000607.v3.p2. All analysis code is available here: https://github.com/ZaixuCui/pncControlEnergy, with detailed explanation in https://github.com/ZaixuCui/pncControlEnergy/wiki.
Article and author information
Author details
Danielle S Bassett
Theodore D Satterthwaite
Funding
National Institute of Mental Health (R21MH106799)
- Danielle S Bassett
National Institute of Mental Health (R01MH113550)
- Theodore D Satterthwaite
National Institute of Mental Health (R01MH107703)
- Theodore D Satterthwaite
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Thomas Yeo, National University of Singapore, Singapore
Ethics
Human subjects: All subjects or their parent/guardian provided informed consent, and minors provided assent. The Institutional Review Boards of both Penn and CHOP approved study procedures (IRB-approved protocol number 810336).
Version history
- Received: October 25, 2019
- Accepted: March 26, 2020
- Accepted Manuscript published: March 27, 2020 (version 1)
- Version of Record published: April 16, 2020 (version 2)
Copyright
© 2020, Cui et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Optimization of energy state transition trajectory supports the development of executive function during youth
eLife 9:e53060.
https://doi.org/10.7554/eLife.53060
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