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Hub architecture of the human structural connectome: Links to aging and processing speed
Aging Research Center, Karolinska Institute and Stockholm University, Stockholm, Sweden.
Umeå University, Faculty of Medicine, Umeå Centre for Functional Brain Imaging (UFBI). Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM). Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Aging Research Center, Karolinska Institute and Stockholm University, Stockholm, Sweden.
Aging Research Center, Karolinska Institute and Stockholm University, Stockholm, Sweden; Center for Lifespan Developmental Research (LEADER), School of Behavioral, Social and Legal Sciences, Örebro University, Örebro, Sweden.
2023 (English)In: NeuroImage, ISSN 1053-8119, E-ISSN 1095-9572, Vol. 278, article id 120270Article in journal (Refereed) Published
Abstract [en]

The human structural brain network, or connectome, has a rich-club organization with a small number of brain regions showing high network connectivity, called hubs. Hubs are centrally located in the network, energy costly, and critical for human cognition. Aging has been associated with changes in brain structure, function, and cognitive decline, such as processing speed. At a molecular level, the aging process is a progressive accumulation of oxidative damage, which leads to subsequent energy depletion in the neuron and causes cell death. However, it is still unclear how age affects hub connections in the human connectome. The current study aims to address this research gap by constructing structural connectome using fiber bundle capacity (FBC). FBC is derived from Constrained Spherical Deconvolution (CSD) modeling of white-matter fiber bundles, which represents the capacity of a fiber bundle to transfer information. Compared to the raw number of streamlines, FBC is less bias for quantifying connection strength within biological pathways. We found that hubs exhibit longer-distance connections and higher metabolic rates compared to peripheral brain regions, suggesting that hubs are biologically costly. Although the landscape of structural hubs was relatively age-invariant, there were wide-spread age effects on FBC in the connectome. Critically, these age effects were larger in connections within hub compared to peripheral brain connections. These findings were supported by both a cross-sectional sample with wide age-range (N = 137) and a longitudinal sample across 5 years (N = 83). Moreover, our results demonstrated that associations between FBC and processing speed were more concentrated in hub connections than chance level, and FBC in hub connections mediated the age-effects on processing speed. Overall, our findings indicate that structural connections of hubs, which demonstrate greater energy demands, are particular vulnerable to aging. The vulnerability may contribute to age-related impairments in processing speed among older adults.

Place, publisher, year, edition, pages
Elsevier, 2023. Vol. 278, article id 120270
Keywords [en]
Aging, Connectome, Diffusion-weighted imaging, Fiber bundle capacity, Processing speed
National Category
Neurosciences
Identifiers
URN: urn:nbn:se:umu:diva-212415DOI: 10.1016/j.neuroimage.2023.120270PubMedID: 37423273Scopus ID: 2-s2.0-85165230998OAI: oai:DiVA.org:umu-212415DiVA, id: diva2:1784634
Funder
Swedish Research Council, 421-2013-1039Swedish Research Council, F02014-0224Available from: 2023-07-28 Created: 2023-07-28 Last updated: 2023-07-28Bibliographically approved

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Salami, Alireza

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Umeå Centre for Functional Brain Imaging (UFBI)Wallenberg Centre for Molecular Medicine at Umeå University (WCMM)Department of Integrative Medical Biology (IMB)
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