open access publication

Article, 2021

Reorganization of brain structural networks in aging: A longitudinal study

Journal of Neuroscience Research, ISSN 0360-4012, 1097-4547, Volume 99, 5, Pages 1354-1376, 10.1002/jnr.24795

Contributors

Coelho, Ana 0000-0001-8489-5750 [1] [2] Fernandes, Henrique Miguel 0000-0003-1245-0474 [3] [4] Magalhães, Ricardo José Da Silva 0000-0001-6279-2195 [1] [2] Moreira, Pedro Silva 0000-0002-2800-3903 [1] [2] Marques, Paulo César Gonçalves 0000-0002-6304-4989 [1] [2] Soares, José Miguel Montenegro 0000-0001-6558-4973 [1] [2] Amorim, Liliana 0000-0002-5105-7045 [1] [2] Portugal-Nunes, Carlos 0000-0001-8398-1366 [1] [2] Castanho, Teresa Costa 0000-0002-4162-0359 [1] [2] Santos, Nadine Correia 0000-0001-8110-7173 [1] [2] Sousa, Nuno Jorge Carvalho 0000-0002-8755-5126 (Corresponding author) [1] [2]

Affiliations

  1. [1] Clinical Academic Center of Braga
  2. [NORA names: Portugal; Europe, EU; OECD];
  3. [2] University of Minho
  4. [NORA names: Portugal; Europe, EU; OECD];
  5. [3] Aarhus University
  6. [NORA names: AU Aarhus University; University; Denmark; Europe, EU; Nordic; OECD];
  7. [4] University of Oxford
  8. [NORA names: United Kingdom; Europe, Non-EU; OECD]

Abstract

Normal aging is characterized by structural and functional changes in the brain contributing to cognitive decline. Structural connectivity (SC) describes the anatomical backbone linking distinct functional subunits of the brain and disruption of this communication is thought to be one of the potential contributors for the age-related deterioration observed in cognition. Several studies already explored brain network's reorganization during aging, but most focused on average connectivity of the whole-brain or in specific networks, such as the resting-state networks. Here, we aimed to characterize longitudinal changes of white matter (WM) structural brain networks, through the identification of sub-networks with significantly altered connectivity along time. Then, we tested associations between longitudinal changes in network connectivity and cognition. We also assessed longitudinal changes in topological properties of the networks. For this, older adults were evaluated at two timepoints, with a mean interval time of 52.8 months (SD = 7.24). WM structural networks were derived from diffusion magnetic resonance imaging, and cognitive status from neurocognitive testing. Our results show age-related changes in brain SC, characterized by both decreases and increases in connectivity weight. Interestingly, decreases occur in intra-hemispheric connections formed mainly by association fibers, while increases occur mostly in inter-hemispheric connections and involve association, commissural, and projection fibers, supporting the last-in-first-out hypothesis. Regarding topology, two hubs were lost, alongside with a decrease in connector-hub inter-modular connectivity, reflecting reduced integration. Simultaneously, there was an increase in the number of provincial hubs, suggesting increased segregation. Overall, these results confirm that aging triggers a reorganization of the brain structural network.

Keywords

WM structural networks, adults, age, age-related changes, age-related deterioration, anatomical backbone, assessed longitudinal changes, association, association fibers, average connectivity, backbone, brain, brain network reorganization, brain structural networks, changes, cognition, cognitive decline, cognitive status, communication, connection, connection weights, contributors, decline, decrease, deterioration, diffusion, diffusion magnetic resonance imaging, disruption, fibers, functional changes, functional subunits, hub, hypothesis, identification, identification of sub-networks, images, increase, increased segregation, integration, inter-hemispheric connectivity, inter-modular connections, interval time, intra-hemispheric connectivity, longitudinal changes, longitudinal study, magnetic resonance imaging, matter, mean interval time, months, network, network connectivity, network reorganization, neurocognitive tests, normal aging, older adults, potential contributors, project, projection fibers, properties, provincial hubs, reduced integration, reorganization, resonance imaging, resting-state networks, results, segregation, status, structural connectivity, structural network, study, sub-networks, subunit, test, test associations, time, timepoints, topological properties, topology, weight, white matter, whole-brain

Funders

  • Fundação para a Ciência e Tecnologia
  • European Commission

Data Provider: Digital Science