Specificity and robustness of long-distance connections in weighted, interareal connectomes.
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ABSTRACT: Brain areas' functional repertoires are shaped by their incoming and outgoing structural connections. In empirically measured networks, most connections are short, reflecting spatial and energetic constraints. Nonetheless, a small number of connections span long distances, consistent with the notion that the functionality of these connections must outweigh their cost. While the precise function of long-distance connections is unknown, the leading hypothesis is that they act to reduce the topological distance between brain areas and increase the efficiency of interareal communication. However, this hypothesis implies a nonspecificity of long-distance connections that we contend is unlikely. Instead, we propose that long-distance connections serve to diversify brain areas' inputs and outputs, thereby promoting complex dynamics. Through analysis of five weighted interareal network datasets, we show that long-distance connections play only minor roles in reducing average interareal topological distance. In contrast, areas' long-distance and short-range neighbors exhibit marked differences in their connectivity profiles, suggesting that long-distance connections enhance dissimilarity between areal inputs and outputs. Next, we show that-in isolation-areas' long-distance connectivity profiles exhibit nonrandom levels of similarity, suggesting that the communication pathways formed by long connections exhibit redundancies that may serve to promote robustness. Finally, we use a linearization of Wilson-Cowan dynamics to simulate the covariance structure of neural activity and show that in the absence of long-distance connections a common measure of functional diversity decreases. Collectively, our findings suggest that long-distance connections are necessary for supporting diverse and complex brain dynamics.
SUBMITTER: Betzel RF
PROVIDER: S-EPMC6003515 | biostudies-literature | 2018 May
REPOSITORIES: biostudies-literature
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