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Morphometric brain organization across the human lifespan reveals increased dispersion linked to cognitive performance

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  • Jiao Li
  • Chao Zhang
  • Yao Meng
  • Siqi Yang
  • Jie Xia
  • Huafu Chen
  • Wei Liao

Abstract

The human brain is organized as segregation and integration units and follows complex developmental trajectories throughout life. The cortical manifold provides a new means of studying the brain’s organization in a multidimensional connectivity gradient space. However, how the brain’s morphometric organization changes across the human lifespan remains unclear. Here, leveraging structural magnetic resonance imaging scans from 1,790 healthy individuals aged 8 to 89 years, we investigated age-related global, within- and between-network dispersions to reveal the segregation and integration of brain networks from 3D manifolds based on morphometric similarity network (MSN), combining multiple features conceptualized as a “fingerprint” of an individual’s brain. Developmental trajectories of global dispersion unfolded along patterns of molecular brain organization, such as acetylcholine receptor. Communities were increasingly dispersed with age, reflecting more disassortative morphometric similarity profiles within a community. Increasing within-network dispersion of primary motor and association cortices mediated the influence of age on the cognitive flexibility of executive functions. We also found that the secondary sensory cortices were decreasingly dispersed with the rest of the cortices during aging, possibly indicating a shift of secondary sensory cortices across the human lifespan from an extreme to a more central position in 3D manifolds. Together, our results reveal the age-related segregation and integration of MSN from the perspective of a multidimensional gradient space, providing new insights into lifespan changes in multiple morphometric features of the brain, as well as the influence of such changes on cognitive performance.There is much interest in how the brain’s morphometric organization changes throughout the human lifespan to support cognition. By analyzing structural MRI data from subjects aged 8-89, this study reveals that networks within the brain become more dispersed with age, and that these effects may underlie age-related changes in cognitive flexibility and executive function.

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  • Jiao Li & Chao Zhang & Yao Meng & Siqi Yang & Jie Xia & Huafu Chen & Wei Liao, 2024. "Morphometric brain organization across the human lifespan reveals increased dispersion linked to cognitive performance," PLOS Biology, Public Library of Science, vol. 22(6), pages 1-24, June.
    • Handle: RePEc:plo:pbio00:3002647
    DOI: 10.1371/journal.pbio.3002647
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    1. Seok-Jun Hong & Reinder Vos de Wael & Richard A. I. Bethlehem & Sara Lariviere & Casey Paquola & Sofie L. Valk & Michael P. Milham & Adriana Di Martino & Daniel S. Margulies & Jonathan Smallwood & Bor, 2019. "Atypical functional connectome hierarchy in autism," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Hilary Richardson & Grace Lisandrelli & Alexa Riobueno-Naylor & Rebecca Saxe, 2018. "Development of the social brain from age three to twelve years," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Jakob Seidlitz & Ajay Nadig & Siyuan Liu & Richard A. I. Bethlehem & Petra E. Vértes & Sarah E. Morgan & František Váša & Rafael Romero-Garcia & François M. Lalonde & Liv S. Clasen & Jonathan D. Blume, 2020. "Author Correction: Transcriptomic and cellular decoding of regional brain vulnerability to neurogenetic disorders," Nature Communications, Nature, vol. 11(1), pages 1-6, December.
    4. Jakob Seidlitz & Ajay Nadig & Siyuan Liu & Richard A. I. Bethlehem & Petra E. Vértes & Sarah E. Morgan & František Váša & Rafael Romero-Garcia & François M. Lalonde & Liv S. Clasen & Jonathan D. Blume, 2020. "Transcriptomic and cellular decoding of regional brain vulnerability to neurogenetic disorders," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. R. A. Rigby & D. M. Stasinopoulos, 2005. "Generalized additive models for location, scale and shape," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 54(3), pages 507-554, June.
    6. Jiao Li & Jakob Seidlitz & John Suckling & Feiyang Fan & Gong-Jun Ji & Yao Meng & Siqi Yang & Kai Wang & Jiang Qiu & Huafu Chen & Wei Liao, 2021. "Cortical structural differences in major depressive disorder correlate with cell type-specific transcriptional signatures," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
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    1. Jiao Li & Zhiliang Long & Gong-Jun Ji & Shaoqiang Han & Yuan Chen & Guanqun Yao & Yong Xu & Kerang Zhang & Yong Zhang & Jingliang Cheng & Kai Wang & Huafu Chen & Wei Liao, 2025. "Major depressive disorder on a neuromorphic continuum," Nature Communications, Nature, vol. 16(1), pages 1-13, December.

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