title: Age-related changes in the topological organization of the white matter structural connectome across the human lifespan.
abstract: Lifespan is a dynamic process with remarkable changes in brain structure and function. Previous neuroimaging studies have indicated age-related microstructural changes in specific white matter tracts during development and aging. However, the age-related alterations in the topological architecture of the white matter structural connectome across the human lifespan remain largely unknown. Here, a cohort of 113 healthy individuals (ages 9-85) with both diffusion and structural MRI acquisitions were examined. For each participant, the high-resolution white matter structural networks were constructed by deterministic fiber tractography among 1024 parcellation units and were quantified with graph theoretical analyses. The global network properties, including network strength, cost, topological efficiency, and robustness, followed an inverted U-shaped trajectory with a peak age around the third decade. The brain areas with the most significantly nonlinear changes were located in the prefrontal and temporal cortices. Different brain regions exhibited heterogeneous trajectories: the posterior cingulate and lateral temporal cortices displayed prolonged maturation/degeneration compared with the prefrontal cortices. Rich-club organization was evident across the lifespan, whereas hub integration decreased linearly with age, especially accompanied by the loss of frontal hubs and their connections. Additionally, age-related changes in structural connections were predominantly located within and between the prefrontal and temporal modules. Finally, based on the graph metrics of structural connectome, accurate predictions of individual age were obtained (r = 0.77). Together, the data indicated a dynamic topological organization of the brain structural connectome across human lifespan, which may provide possible structural substrates underlying functional and cognitive changes with age.
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Tengda
authors.initials: T
authors.lastname: Zhao
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Miao
authors.initials: M
authors.lastname: Cao
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Haijing
authors.initials: H
authors.lastname: Niu
authors.affiliation: Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.|Key Laboratory of Behavioral Science, Institute of Psychology Chinese Academy of Sciences, Beijing, 100101, China.|Laboratory for Functional Connectome and Development, Institute of Psychology Chinese Academy of Sciences, Beijing, 100101, China.|Magnetic Resonance Imaging Research Center, Institute of Psychology Chinese Academy of Sciences, Beijing, 100101, China.
authors.forename: Xi-Nian
authors.identifier: http://orcid.org/0000-0001-9110-585X
authors.initials: XN
authors.lastname: Zuo
authors.affiliation: McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, Quebec, H3A 2B4, Canada.
authors.forename: Alan
authors.initials: A
authors.lastname: Evans
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Yong
authors.initials: Y
authors.lastname: He
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Qi
authors.initials: Q
authors.lastname: Dong
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.|Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing, 100875, China.
authors.forename: Ni
authors.initials: N
authors.lastname: Shu
mesh_terms: D000293:Adolescent; D000328:Adult; D000368:Aged; D000369:Aged, 80 and over; D000375:Aging / Q000502:physiology*; D000465:Algorithms; D001921:Brain / Q000033:anatomy & histology / Q000254:growth & development*; D002648:Child; D063132:Connectome / Q000379:methods*; D056324:Diffusion Tensor Imaging; D005260:Female; D006179:Gyrus Cinguli / Q000033:anatomy & histology / Q000254:growth & development; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009412:Nerve Fibers; D009434:Neural Pathways / Q000033:anatomy & histology / Q000254:growth & development*; D017397:Prefrontal Cortex / Q000033:anatomy & histology / Q000254:growth & development; D015203:Reproducibility of Results; D012727:Sex Characteristics; D013702:Temporal Lobe / Q000033:anatomy & histology / Q000254:growth & development; D066127:White Matter / Q000033:anatomy & histology / Q000254:growth & development*; D055815:Young Adult
keywords: brain network; diffusion MRI; fiber tractography; graph theory; lifespan; white matter