Dataset Information

Wiring cost and topological participation of the mouse brain connectome.

ABSTRACT: Brain connectomes are topologically complex systems, anatomically embedded in 3D space. Anatomical conservation of "wiring cost" explains many but not all aspects of these networks. Here, we examined the relationship between topology and wiring cost in the mouse connectome by using data from 461 systematically acquired anterograde-tracer injections into the right cortical and subcortical regions of the mouse brain. We estimated brain-wide weights, distances, and wiring costs of axonal projections and performed a multiscale topological and spatial analysis of the resulting weighted and directed mouse brain connectome. Our analysis showed that the mouse connectome has small-world properties, a hierarchical modular structure, and greater-than-minimal wiring costs. High-participation hubs of this connectome mediated communication between functionally specialized and anatomically localized modules, had especially high wiring costs, and closely corresponded to regions of the default mode network. Analyses of independently acquired histological and gene-expression data showed that nodal participation colocalized with low neuronal density and high expression of genes enriched for cognition, learning and memory, and behavior. The mouse connectome contains high-participation hubs, which are not explained by wiring-cost minimization but instead reflect competitive selection pressures for integrated network topology as a basis for higher cognitive and behavioral functions.

SUBMITTER: Rubinov M

PROVIDER: S-EPMC4538676 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Wiring cost and topological participation of the mouse brain connectome.

Rubinov Mikail M Ypma Rolf J F RJ Watson Charles C Bullmore Edward T ET

Proceedings of the National Academy of Sciences of the United States of America 20150727 32

Brain connectomes are topologically complex systems, anatomically embedded in 3D space. Anatomical conservation of "wiring cost" explains many but not all aspects of these networks. Here, we examined the relationship between topology and wiring cost in the mouse connectome by using data from 461 systematically acquired anterograde-tracer injections into the right cortical and subcortical regions of the mouse brain. We estimated brain-wide weights, distances, and wiring costs of axonal projection ...[more]

PMID: 26216962

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Project description:The primate connectome, possessing a characteristic global topology and specific regional connectivity profiles, is well organized to support both segregated and integrated brain function. However, the organization mechanisms shaping the characteristic connectivity and its relationship to functional requirements remain unclear. The primate brain connectome is shaped by metabolic economy as well as functional values. Here, we explored the influence of two competing factors and additional advanced functional requirements on the primate connectome employing an optimal trade-off model between neural wiring cost and the representative functional requirement of processing efficiency. Moreover, we compared this model with a generative model combining spatial distance and topological similarity, with the objective of statistically reproducing multiple topological features of the network. The primate connectome indeed displays a cost-efficiency trade-off and that up to 67% of the connections were recovered by optimal combination of the two basic factors of wiring economy and processing efficiency, clearly higher than the proportion of connections (56%) explained by the generative model. While not explicitly aimed for, the trade-off model captured several key topological features of the real connectome as the generative model, yet better explained the connectivity of most regions. The majority of the remaining 33% of connections unexplained by the best trade-off model were long-distance links, which are concentrated on few cortical areas, termed long-distance connectors (LDCs). The LDCs are mainly non-hubs, but form a densely connected group overlapping on spatially segregated functional modalities. LDCs are crucial for both functional segregation and integration across different scales. These organization features revealed by the optimization analysis provide evidence that the demands of advanced functional segregation and integration among spatially distributed regions may play a significant role in shaping the cortical connectome, in addition to the basic cost-efficiency trade-off. These findings also shed light on inherent vulnerabilities of brain networks in diseases.

Dataset Information

Wiring cost and topological participation of the mouse brain connectome.

Publications

Wiring cost and topological participation of the mouse brain connectome.

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