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The age of reason: Functional brain network development during childhood

View ORCID ProfileUrsula A. Tooley, Anne T. Park, Julia A. Leonard, Austin L. Boroshok, Cassidy L. McDermott, View ORCID ProfileM. Dylan Tisdall, View ORCID ProfileDani S. Bassett, Allyson P. Mackey
doi: https://doi.org/10.1101/2022.07.07.499176
Ursula A. Tooley
1Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
2Neuroscience Graduate Group, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
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Anne T. Park
1Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
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Julia A. Leonard
3Department of Psychology, Yale University, New Haven, CT 06520, USA
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Austin L. Boroshok
1Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
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Cassidy L. McDermott
1Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
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M. Dylan Tisdall
4Department of Radiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104
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Dani S. Bassett
5Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
6Department of Electrical & Systems Engineering, School of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA
7Department of Physics & Astronomy, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
8Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
9Department of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
10Santa Fe Institute, Santa Fe, NM 87501 USA
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Allyson P. Mackey
1Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
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  • For correspondence: mackeya@upenn.edu
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Abstract

Human childhood is characterized by dramatic changes in the mind and brain. However, little is known about the large-scale intrinsic cortical network changes that occur during childhood due to methodological challenges in scanning young children. Here, we overcome this barrier by using sophisticated acquisition and analysis tools to investigate functional network development in children between the ages of 4 and 10 years (n = 92). At multiple spatial scales, age is positively associated with brain network segregation. At the system level, age was associated with segregation of systems involved in attention from those involved in abstract cognition, and with integration among attentional and perceptual systems. Associations between age and functional connectivity are most pronounced in visual and medial prefrontal cortex, the two ends of a gradient from perceptual, externally oriented cortex to abstract, internally oriented cortex. These findings suggest that both ends of the sensory-association gradient may develop early, in contrast to the classical theories that cortical maturation proceeds from back to front, with sensory areas developing first and association areas developing last. More mature patterns of brain network architecture, controlling for age, were associated with better visuospatial reasoning abilities. Our results suggest that as cortical architecture becomes more specialized, children become more able to reason about the world and their place in it.

Significance Anthropologists have called the transition from early to middle childhood the “age of reason”, when children across cultures become more independent. We employ cutting-edge neuroimaging acquisition and analysis approaches to investigate associations between age and functional brain architecture in childhood. Age was positively associated with segregation between cortical systems that process the external world, and those that process abstract phenomena like the past, future, and minds of others. Surprisingly, we observed pronounced development at both ends of the sensory-association gradient, challenging the theory that sensory areas develop first and association areas develop last. Our results open new directions for research into how brains reorganize to support rapid gains in cognitive and socioemotional skills as children reach the age of reason.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/utooley/Tooley_2022_childhood_functional_network_dev

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 09, 2022.
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The age of reason: Functional brain network development during childhood
Ursula A. Tooley, Anne T. Park, Julia A. Leonard, Austin L. Boroshok, Cassidy L. McDermott, M. Dylan Tisdall, Dani S. Bassett, Allyson P. Mackey
bioRxiv 2022.07.07.499176; doi: https://doi.org/10.1101/2022.07.07.499176
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The age of reason: Functional brain network development during childhood
Ursula A. Tooley, Anne T. Park, Julia A. Leonard, Austin L. Boroshok, Cassidy L. McDermott, M. Dylan Tisdall, Dani S. Bassett, Allyson P. Mackey
bioRxiv 2022.07.07.499176; doi: https://doi.org/10.1101/2022.07.07.499176

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