Optimization of energy state transition trajectory supports the development of executive function during youth

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.

The following previously published data sets were used

Article and author information

Author details

  1. Zaixu Cui

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  2. Jennifer Stiso

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3295-586X
  3. Graham L Baum

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  4. Jason Z Kim

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  5. David R Roalf

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  6. Richard F Betzel

    Psychological and Brain Sciences, Indiana University, Bloomington, United States
    Competing interests
    No competing interests declared.
  7. Shi Gu

    Computer Science, University of Electronic Science and Technology, Chengdu, China
    Competing interests
    No competing interests declared.
  8. Zhixin Lu

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  9. Cedric H Xia

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  10. Xiaosong He

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  11. Rastko Ciric

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  12. Desmond J Oathes

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7346-2669
  13. Tyler M Moore

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  14. Russell T Shinohara

    Epidemiology and Informatics, University of Pennsylvania, Philadelphia, United States
    Competing interests
    Russell T Shinohara, has received legal consulting and advisory board income from Genentech/Roche..
  15. Kosha Ruparel

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  16. Christos Davatzikos

    Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  17. Fabio Pasqualetti

    Mechanical Engineering, University of California, Riverside, Riverside, United States
    Competing interests
    No competing interests declared.
  18. Raquel E Gur

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
  19. Ruben C Gur

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9657-1996
  20. Danielle S Bassett

    Department of Bioengineering, University of Pennsylvania, Philadelphia, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6183-4493
  21. Theodore D Satterthwaite

    Psychiatry, University of Pennsylvania, Philadelphia, United States
    For correspondence
    sattertt@pennmedicine.upenn.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7072-9399

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.

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).

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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  1. Zaixu Cui
  2. Jennifer Stiso
  3. Graham L Baum
  4. Jason Z Kim
  5. David R Roalf
  6. Richard F Betzel
  7. Shi Gu
  8. Zhixin Lu
  9. Cedric H Xia
  10. Xiaosong He
  11. Rastko Ciric
  12. Desmond J Oathes
  13. Tyler M Moore
  14. Russell T Shinohara
  15. Kosha Ruparel
  16. Christos Davatzikos
  17. Fabio Pasqualetti
  18. Raquel E Gur
  19. Ruben C Gur
  20. Danielle S Bassett
  21. Theodore D Satterthwaite
(2020)
Optimization of energy state transition trajectory supports the development of executive function during youth
eLife 9:e53060.
https://doi.org/10.7554/eLife.53060

Share this article

https://doi.org/10.7554/eLife.53060

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