Age-related changes in topological organization of structural brain networks in healthy individuals - PubMed (original) (raw)

Kai Wu et al. Hum Brain Mapp. 2012 Mar.

Abstract

The aim of this study was to examine structural brain networks using regional gray matter volume, as well as to investigate changes in small-world and modular organization with normal aging. We constructed structural brain networks composed of 90 regions in young, middle, and old age groups. We randomly selected 350 healthy subjects for each group from a Japanese magnetic resonance image database. Structural brain networks in three age groups showed economical small-world properties, providing high global and local efficiency for parallel information processing at low connection cost. The small-world efficiency and node betweenness varied significantly and revealed a U- or inverted U-curve model tendency among three age groups. Results also demonstrated that structural brain networks exhibited a modular organization in which the connections between regions are much denser within modules than between them. The modular organization of structural brain networks was similar between the young and middle age groups, but quite different from the old group. In particular, the old group showed a notable decrease in the connector ratio and the intermodule connections. Combining the results of small-world efficiency, node betweenness and modular organization, we concluded that the brain network changed slightly, developing into a more distributed organization from young to middle age. The organization eventually altered greatly, shifting to a more localized organization in old age. Our findings provided quantitative insights into topological principles of structural brain networks and changes related to normal aging.

Copyright © 2011 Wiley Periodicals, Inc.

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Figures

Figure 1

Figure 1

Economical small‐world properties and age‐related changes. Left: The local and global efficiency of brain networks as a function of cost threshold. Right: The trend for the integrated efficiency metrics in age‐specific groups. A: Local efficiency calculated under the cost threshold range of 0.11–0.25. B: Global efficiency calculated under the cost threshold range of 0.11–0.25. Significant differences between age groups were tested by permutation test under uncorrected conditions (P < 0.05). ▴; Y vs. M, ×; Y vs. M, ♦; Y vs. O. C: Integrated local efficiency. D: Integrated global efficiency. Three comparisons were performed as follows: Z I (Young vs. Middle), Z II (Middle vs. Old), and Z III (Young vs. Old).

Figure 2

Figure 2

Surface representations for global hubs and the significant age‐related changes in node betweenness. Top: The global hubs in the young group. Middle: The global hubs in the middle group and the significant age‐related changes in node betweenness from young to middle age. Bottom: The global hubs in the old group and the significant age‐related changes in node betweenness from middle to old age. The global hubs and non‐hubs are indicated by spheres in big and small size, respectively. The nodes with significant decreased and increased age‐related changes are indicated by green and red spheres, respectively. The nodes without significant age‐related change are indicated by blue spheres.

Figure 3

Figure 3

Surface representations for modules in structural brain networks. All of 90 brain regions are plotted by different colored spheres (different colors represent distinct network modules) and further mapped onto the cortical surfaces at the lateral and medial views, respectively.

Figure 4

Figure 4

Modular organization of structural brain networks. Left: The modular organization of young (A), middle (B), and old (C) brain networks visualized by minimizing free energy using a Kamada‐Kawaki layout algorithm. The global hubs and non‐hubs are represented by the bigger and smaller circles, respectively. The regions are represented by the module color. The intramodule and intermodule connections are represented by the light gray and black lines, respectively. Right: The regional node roles in brain modules for young (D), middle (E), and old (F) brain networks, with connector nodes located in a central ring to highlight intermodule connections. The intramodule and intermodule connections are shown in colored and black lines, respectively.

Figure 5

Figure 5

The ratio of intermodule connections.

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