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

• Published in: PLoS biology Vol. 22; no. 6; p. e3002647
• Main Authors: Li, Jiao, Zhang, Chao, Meng, Yao, Yang, Siqi, Xia, Jie, Chen, Huafu, Liao, Wei
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 20.06.2024; Public Library of Science (PLoS)
• Subjects: Acetylcholine receptors; Adolescent; Adult; Age; Aged; Aged, 80 and over; Aging; Aging - physiology; Biology and Life Sciences; Brain; Brain - diagnostic imaging; Brain - growth & development; Brain - physiology; Brain architecture; Brain research; Child; Child development; Cognition; Cognition - physiology; Cognitive ability; Cognitive tasks; Computer and Information Sciences; Executive Function - physiology; Female; Grants; Health aspects; Human performance; Humans; Life span; Longevity - physiology; Magnetic resonance imaging; Magnetic Resonance Imaging - methods; Male; Manifolds; Medical imaging; Medicine and Health Sciences; Middle Aged; Nerve Net - diagnostic imaging; Nerve Net - physiology; Neural networks; Neuroimaging; Neurosciences; Physical Sciences; Position sensing; Research and Analysis Methods; Sensory integration; Similarity; Social Sciences; Young Adult; Young adults; China
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3002647

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.