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

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101183755 Publication Model: eCollection Cited Medium: Internet ISSN: 1545-7885 (Electronic) Linking ISSN: 15449173 NLM ISO Abbreviation: PLoS Biol Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, [2003]-

Cognition*/physiology ; Magnetic Resonance Imaging*/methods ; Brain*/diagnostic imaging ; Brain*/physiology ; Brain*/growth & development ; Longevity*/physiology ; Aging*/physiology; Humans ; Adult ; Aged ; Adolescent ; Middle Aged ; Male ; Female ; Aged, 80 and over ; Child ; Young Adult ; Nerve Net/physiology ; Nerve Net/diagnostic imaging ; Executive Function/physiology

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.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Comment in: PLoS Biol. 2024 Jun 21;22(6):e3002669. doi: 10.1371/journal.pbio.3002669. (PMID: 38905164)

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U01 AG052564 United States AG NIA NIH HHS; U01 MH109589 United States MH NIMH NIH HHS; U54 MH091657 United States MH NIMH NIH HHS

Date Created: 20240620 Date Completed: 20240620 Latest Revision: 20240623

20240623

PMC11189252

10.1371/journal.pbio.3002647

38900742