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Effects of age, sex, and puberty on neural efficiency of cognitive and motor control in adolescents

  • Tilman SchulteEmail author
  • Jui-Yang Hong
  • Edith V. Sullivan
  • Adolf Pfefferbaum
  • Fiona C. Baker
  • Weiwei Chu
  • Devin Prouty
  • Dongjin Kwon
  • Mary J. Meloy
  • Ty Brumback
  • Susan F. Tapert
  • Ian M. Colrain
  • Eva M. Müller-Oehring
ORIGINAL RESEARCH

Abstract

Critical changes in adolescence involve brain cognitive maturation of inhibitory control processes that are essential for a myriad of adult functions. Cognitive control advances into adulthood as there is more flexible integration of component processes, including inhibitory control of conflicting information, overwriting inappropriate response tendencies, and amplifying relevant responses for accurate execution. Using a modified Stroop task with fMRI, we investigated the effects of age, sex, and puberty on brain functional correlates of cognitive and motor control in 87 boys and 91 girls across the adolescent age range. Results revealed dissociable brain systems for cognitive and motor control processes, whereby adolescents flexibly adapted neural responses to control demands. Specifically, when response repetitions facilitated planning-based action selection, frontoparietal-insular regions associated with cognitive control operations were less activated, whereas cortical-pallidal-cerebellar motor regions associated with motor skill acquisition, were more activated. Attenuated middle cingulate cortex activation occurred with older adolescent age for both motor control and cognitive control with automaticity from repetition learning. Sexual dimorphism for control operations occurred in extrastriate cortices involved in visuo-attentional selection: While boys enhanced extrastriate selection processes for motor control, girls activated these regions more for cognitive control. These sex differences were attenuated with more advanced pubertal stage. Together, our findings show that brain cognitive and motor control processes are segregated, demand-specific, more efficient in older adolescents, and differ between sexes relative to pubertal development. Our findings advance our understanding of how distributed brain activity and the neurodevelopment of automaticity enhances cognitive and motor control ability in adolescence.

Keywords

Functional MRI Executive control Age and gender Puberty Automaticity of behavior 

Notes

Acknowledgements

This work was supported by the U.S. National Institute on Alcohol Abuse and Alcoholism with co-funding from the National Institute on Drug Abuse, the National Institute of Mental Health, the National Institute of Health Office of the Director, the National Institute of Child Health and Human Development, and the Office of the Director, National Institutes of Health [NCANDA grant numbers: AA021696 (IMC + FCB), AA021695 (SAB + SFT), AA021692 (SFT), AA021697 (AP + KMP)]. Additional funding was provided by NIAAA grant number AA010723 (EVS).

Compliance with ethical standards

Conflict of interest

None of the authors have conflicts of interest with the reported data or their interpretation.

Supplementary material

11682_2019_75_MOESM1_ESM.docx (393 kb)
ESM 1 (DOCX 393 kb)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Tilman Schulte
    • 1
    • 2
    Email author
  • Jui-Yang Hong
    • 1
  • Edith V. Sullivan
    • 3
  • Adolf Pfefferbaum
    • 1
    • 3
  • Fiona C. Baker
    • 1
  • Weiwei Chu
    • 1
  • Devin Prouty
    • 1
  • Dongjin Kwon
    • 1
    • 3
  • Mary J. Meloy
    • 4
  • Ty Brumback
    • 4
  • Susan F. Tapert
    • 4
  • Ian M. Colrain
    • 1
  • Eva M. Müller-Oehring
    • 1
    • 3
  1. 1.Center for Health Sciences, Neuroscience Program, Biosciences DivisionSRI InternationalMenlo ParkUSA
  2. 2.Pacific Graduate School of Clinical PsychologyPalo Alto UniversityPalo AltoUSA
  3. 3.Department of Psychiatry & Behavioral SciencesStanford University School of MedicineStanfordUSA
  4. 4.Department of PsychiatryUniversity of CaliforniaLa JollaUSA

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