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Connectomic Insights into Topologically Centralized Network Edges and Relevant Motifs in the Human Brain.

Xia M, Lin Q, Bi Y, He Y - Front Hum Neurosci (2016)

Bottom Line: We found that the pivotal WM connections with highly topological-edge centrality were primarily distributed in several long-range cortico-cortical connections (including the corpus callosum, cingulum and inferior fronto-occipital fasciculus) and some projection tracts linking subcortical regions.Computational simulation models indicated the sharp decrease of global network integrity when attacking these highly centralized edges.Together, our results demonstrated high building-cost consumption and substantial communication capacity contributions for pivotal WM connections, which deepens our understanding of the topological mechanisms that govern the organization of human connectomes.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University Beijing, China.

ABSTRACT
White matter (WM) tracts serve as important material substrates for information transfer across brain regions. However, the topological roles of WM tracts in global brain communications and their underlying microstructural basis remain poorly understood. Here, we employed diffusion magnetic resonance imaging and graph-theoretical approaches to identify the pivotal WM connections in human whole-brain networks and further investigated their wiring substrates (including WM microstructural organization and physical consumption) and topological contributions to the brain's network backbone. We found that the pivotal WM connections with highly topological-edge centrality were primarily distributed in several long-range cortico-cortical connections (including the corpus callosum, cingulum and inferior fronto-occipital fasciculus) and some projection tracts linking subcortical regions. These pivotal WM connections exhibited high levels of microstructural organization indicated by diffusion measures (the fractional anisotropy, the mean diffusivity and the axial diffusivity) and greater physical consumption indicated by streamline lengths, and contributed significantly to the brain's hubs and the rich-club structure. Network motif analysis further revealed their heavy participations in the organization of communication blocks, especially in routes involving inter-hemispheric heterotopic and extremely remote intra-hemispheric systems. Computational simulation models indicated the sharp decrease of global network integrity when attacking these highly centralized edges. Together, our results demonstrated high building-cost consumption and substantial communication capacity contributions for pivotal WM connections, which deepens our understanding of the topological mechanisms that govern the organization of human connectomes.

No MeSH data available.


Vulnerability of the pivotal edges and lesion simulation. (A) The pivotal edges showed significant greater vulnerability than the non-pivotal ones. The error bars represent the standard deviation. (B) The global efficiency and (C) the size of largest connected component slowly declined in the random failure. When facing the targeted attacks, these network properties decreased rapidly (over 40%) after the top 20% edges were removed.
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Figure 6: Vulnerability of the pivotal edges and lesion simulation. (A) The pivotal edges showed significant greater vulnerability than the non-pivotal ones. The error bars represent the standard deviation. (B) The global efficiency and (C) the size of largest connected component slowly declined in the random failure. When facing the targeted attacks, these network properties decreased rapidly (over 40%) after the top 20% edges were removed.

Mentions: Two simulation strategies were used to evaluate how a “lesion” of the pivotal WM edges influenced brain network performance. First, we calculated the vulnerability of each edge in the WM network, which was defined as the change in the global efficiency of the network after eliminating this edge from the whole-brain network (Costa et al., 2007). Not surprisingly, the pivotal edges showed significantly greater vulnerability than the non-pivotal ones (p < 0.0001, permutation tests) (Figure 6A), especially the precuneus-related fiber tracts (Table 1). Second, we evaluated the topological robustness of the brain networks against random failure and targeted attacks of WM edges (Kaiser et al., 2007; He et al., 2008). Both the global efficiency and the size of the largest-connected component slowly declined in response to the random failure; In contrast, these network properties decreased rapidly in response to a targeted attack, with an over 40% reduction when 20% of the most centralized edges were attacked (Figures 6B,C). These simulation analyses highlight the topological significance of the pivotal WM edges in the global integrity of brain networks.


Connectomic Insights into Topologically Centralized Network Edges and Relevant Motifs in the Human Brain.

Xia M, Lin Q, Bi Y, He Y - Front Hum Neurosci (2016)

Vulnerability of the pivotal edges and lesion simulation. (A) The pivotal edges showed significant greater vulnerability than the non-pivotal ones. The error bars represent the standard deviation. (B) The global efficiency and (C) the size of largest connected component slowly declined in the random failure. When facing the targeted attacks, these network properties decreased rapidly (over 40%) after the top 20% edges were removed.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835491&req=5

Figure 6: Vulnerability of the pivotal edges and lesion simulation. (A) The pivotal edges showed significant greater vulnerability than the non-pivotal ones. The error bars represent the standard deviation. (B) The global efficiency and (C) the size of largest connected component slowly declined in the random failure. When facing the targeted attacks, these network properties decreased rapidly (over 40%) after the top 20% edges were removed.
Mentions: Two simulation strategies were used to evaluate how a “lesion” of the pivotal WM edges influenced brain network performance. First, we calculated the vulnerability of each edge in the WM network, which was defined as the change in the global efficiency of the network after eliminating this edge from the whole-brain network (Costa et al., 2007). Not surprisingly, the pivotal edges showed significantly greater vulnerability than the non-pivotal ones (p < 0.0001, permutation tests) (Figure 6A), especially the precuneus-related fiber tracts (Table 1). Second, we evaluated the topological robustness of the brain networks against random failure and targeted attacks of WM edges (Kaiser et al., 2007; He et al., 2008). Both the global efficiency and the size of the largest-connected component slowly declined in response to the random failure; In contrast, these network properties decreased rapidly in response to a targeted attack, with an over 40% reduction when 20% of the most centralized edges were attacked (Figures 6B,C). These simulation analyses highlight the topological significance of the pivotal WM edges in the global integrity of brain networks.

Bottom Line: We found that the pivotal WM connections with highly topological-edge centrality were primarily distributed in several long-range cortico-cortical connections (including the corpus callosum, cingulum and inferior fronto-occipital fasciculus) and some projection tracts linking subcortical regions.Computational simulation models indicated the sharp decrease of global network integrity when attacking these highly centralized edges.Together, our results demonstrated high building-cost consumption and substantial communication capacity contributions for pivotal WM connections, which deepens our understanding of the topological mechanisms that govern the organization of human connectomes.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University Beijing, China.

ABSTRACT
White matter (WM) tracts serve as important material substrates for information transfer across brain regions. However, the topological roles of WM tracts in global brain communications and their underlying microstructural basis remain poorly understood. Here, we employed diffusion magnetic resonance imaging and graph-theoretical approaches to identify the pivotal WM connections in human whole-brain networks and further investigated their wiring substrates (including WM microstructural organization and physical consumption) and topological contributions to the brain's network backbone. We found that the pivotal WM connections with highly topological-edge centrality were primarily distributed in several long-range cortico-cortical connections (including the corpus callosum, cingulum and inferior fronto-occipital fasciculus) and some projection tracts linking subcortical regions. These pivotal WM connections exhibited high levels of microstructural organization indicated by diffusion measures (the fractional anisotropy, the mean diffusivity and the axial diffusivity) and greater physical consumption indicated by streamline lengths, and contributed significantly to the brain's hubs and the rich-club structure. Network motif analysis further revealed their heavy participations in the organization of communication blocks, especially in routes involving inter-hemispheric heterotopic and extremely remote intra-hemispheric systems. Computational simulation models indicated the sharp decrease of global network integrity when attacking these highly centralized edges. Together, our results demonstrated high building-cost consumption and substantial communication capacity contributions for pivotal WM connections, which deepens our understanding of the topological mechanisms that govern the organization of human connectomes.

No MeSH data available.