
==== Front
bioRxiv
BIORXIV
bioRxiv
2692-8205
Cold Spring Harbor Laboratory

10.1101/2024.08.23.608315
preprint
2
Article
Brain structure and activity predicting cognitive maturation in adolescence
Zhu Junda http://orcid.org/0000-0002-0221-5289

Garin Clément M http://orcid.org/0000-0003-0712-7330

Qi Xue-Lian
Machado Anna
Wang Zhengyang
Ben Hamed Suliann http://orcid.org/0000-0003-1510-7284

Stanford Terrence R
Salinas Emilio http://orcid.org/0000-0001-7411-5693

Whitlow Christopher T
Anderson Adam W
Zhou Xin Maizie http://orcid.org/0000-0003-4015-4787

Calabro Finnegan J http://orcid.org/0000-0002-8092-3942

Luna Beatriz http://orcid.org/0000-0002-9929-2458

Constantinidis Christos http://orcid.org/0000-0001-7441-022X

02 9 2024
2024.08.23.608315https://creativecommons.org/licenses/by-nd/4.0/ This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License, which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
http://biorxiv.org/lookup/doi/10.1101/2024.08.23.608315
nihpp-2024.08.23.608315.pdf
Cognitive abilities of primates, including humans, continue to improve through adolescence. While a range of changes in brain structure and connectivity have been documented, how they affect neuronal activity that ultimately determines performance of cognitive functions remains unknown. Here, we conducted a multilevel longitudinal study of monkey adolescent neurocognitive development. The developmental trajectory of neural activity in the prefrontal cortex accounted remarkably well for working memory improvements. While complex aspects of activity changed progressively during adolescence, such as the rotation of stimulus representation in multidimensional neuronal space, which has been implicated in cognitive flexibility, even simpler attributes, such as the baseline firing rate in the period preceding a stimulus appearance had predictive power over behavior. Unexpectedly, decreases in brain volume and thickness, which are widely thought to underlie cognitive changes in humans 5 did not predict well the trajectory of neural activity or cognitive performance changes. Whole brain cortical volume in particular, exhibited an increase and reached a local maximum in late adolescence, at a time of rapid behavioral improvement. Maturation of long-distance white matter tracts linking the frontal lobe with areas of the association cortex and subcortical regions best predicted changes in neuronal activity and behavior. Our results provide evidence that optimization of neural activity depending on widely distributed circuitry effects cognitive development in adolescence.
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pmc
