Abstract

The connectome provides the structural substrate facilitating communication between brain regions. We aimed to establish whether accounting for polysynaptic communication in structural connectomes would improve prediction of interindividual variation in behavior as well as increase structure-function coupling strength. Connectomes were mapped for 889 healthy adults participating in the Human Connectome Project. To account for polysynaptic signaling, connectomes were transformed into communication matrices for each of 15 different network communication models. Communication matrices were (a) used to perform predictions of five data-driven behavioral dimensions and (b) correlated to resting-state functional connectivity (FC). While FC was the most accurate predictor of behavior, communication models, in particular communicability and navigation, improved the performance of structural connectomes. Communication also strengthened structure-function coupling, with the navigation and shortest paths models leading to 35–65% increases in association strength with FC. We combined behavioral and functional results into a single ranking that provides insight into which communication models may more faithfully recapitulate underlying neural signaling patterns. Comparing results across multiple connectome mapping pipelines suggested that modeling polysynaptic communication is particularly beneficial in sparse high-resolution connectomes. We conclude that network communication models can augment the functional and behavioral predictive utility of the human structural connectome.

Highlights

  • The structural connectome is a complex network that describes anatomical connections between neural elements (Bassett & Sporns, 2017; Fornito, Zalesky, & Bullmore, 2016)

  • Brain network communication models aim to describe the patterns of large-scale neural signaling that facilitate functional interactions between brain regions

  • We investigated a number of candidate models of connectome communication and found that they improved structure-function coupling and the extent to which structural connectomes can predict interindividual variation in behavior

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Summary

Introduction

The structural connectome is a complex network that describes anatomical connections between neural elements (Bassett & Sporns, 2017; Fornito, Zalesky, & Bullmore, 2016). Numerous studies have demonstrated that the macroscale human connectome is characterized by several nonrandom topological properties, including a smallworld and modular architecture (Bassett & Bullmore, 2006; Sporns & Betzel, 2016), heterogeneous degree distribution (Bullmore & Sporns, 2009), and a core of densely connected hubs (van den Heuvel & Sporns, 2011). This complex anatomical scaffold both facilitates and constrains neural signaling between brain regions. Understanding the dynamics of polysynaptic communication in large-scale brain networks is a key open challenge in neuroscience (Avena-Koenigsberger, Mišic, & Sporns, 2018)

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