Abstract

Interareal connectomes are whole-brain wiring diagrams of white-matter pathways. Recent studies have identified modules, hubs, module hierarchies and rich clubs as structural hallmarks of these wiring diagrams. An influential current theory postulates that connectome modules are adequately explained by evolutionary pressures for wiring economy, but that the other hallmarks are not explained by such pressures and are therefore less trivial. Here, we use constraint network models to test these postulates in current gold-standard vertebrate and invertebrate interareal-connectome reconstructions. We show that empirical wiring-cost constraints inadequately explain connectome module organization, and that simultaneous module and hub constraints induce the structural byproducts of hierarchies and rich clubs. These byproducts, known as spandrels in evolutionary biology, include the structural substrate of the default-mode network. Our results imply that currently standard connectome characterizations are based on circular analyses or double dipping, and we emphasize an integrative approach to future connectome analyses for avoiding such pitfalls.

Highlights

  • Interareal connectomes are whole-brain wiring diagrams of white-matter pathways

  • Such understanding requires the simultaneous reconstruction of accurate whole-brain wiring diagrams, the reduction of these diagrams to informative features, such as anatomical maps of sensory, association and motor systems, and the description of biologically valid mechanisms underlying the organization of these features

  • We evaluated the accuracy of module hierarchies with the normalized mutual information (NMI) between high- and low-resolution module and connectome partitions

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Summary

Introduction

Interareal connectomes are whole-brain wiring diagrams of white-matter pathways. Recent studies have identified modules, hubs, module hierarchies and rich clubs as structural hallmarks of these wiring diagrams. Two recent reconstructions of interareal connectomes, based on data generated by the Allen Institute mouse brain initiative[4,8] and the FlyCircuit Drosophila brain initiative[9,10], have an unmatched combination of brain-wide coverage (compared with more spatially limited imaging studies3,11,12), single-site acquisition (compared with meta-analyses of heterogeneous studies5,13) and high-resolution light-microscopy imaging (compared with lower quality diffusion MRI14,15). By virtue of this combination, these data sets represent the current gold-standard interareal connectome reconstructions of model vertebrate and invertebrate organisms. Studies reported the simultaneous presence of modules and hubs as a ‘small-world’ network organization[20]

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