Abstract

Hierarchical counterstream via feedforward and feedback interactions is a major organizing principle of the cerebral cortex. The counterstream, as a topological feature of the network of cortical areas, is captured by the convergence and divergence of paths through directed links. So defined, the convergence degree (CD) reveals the reciprocal nature of forward and backward connections, and also hierarchically relevant integrative properties of areas through their inward and outward connections. We asked if topology shapes large-scale cortical functioning by studying the role of CD in network resilience and Granger causal coupling in a model of hierarchical network dynamics. Our results indicate that topological synchronizability is highly vulnerable to attacking edges based on CD, while global network efficiency depends mostly on edge betweenness, a measure of the connectedness of a link. Furthermore, similar to anatomical hierarchy determined by the laminar distribution of connections, CD highly correlated with causal coupling in feedforward gamma, and feedback alpha-beta band synchronizations in a well-studied subnetwork, including low-level visual cortical areas. In contrast, causal coupling did not correlate with edge betweenness. Considering the entire network, the CD-based hierarchy correlated well with both the anatomical and functional hierarchy for low-level areas that are far apart in the hierarchy. Conversely, in a large part of the anatomical network where hierarchical distances are small between the areas, the correlations were not significant. These findings suggest that CD-based and functional hierarchies are interrelated in low-level processing in the visual cortex. Our results are consistent with the idea that the interplay of multiple hierarchical features forms the basis of flexible functional cortical interactions.

Highlights

  • Cognition emerges as the result of dynamics on the large-scale network of the cerebral cortex

  • Large-scale cortical dynamics are rooted in the anatomical network formed by axonal connections between neuronal structures, the relationship of network architecture and function represented by coordinated network dynamics is far from clear

  • It is thought that modularity, Path Convergence Shapes Cortical Dynamics core-periphery, and hierarchy are fundamental organizing principles of the anatomical network that constrain functioning

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Summary

Introduction

Cognition emerges as the result of dynamics on the large-scale network of the cerebral cortex. A central question in understanding how network structure gives birth to the rich dynamics of cortical functioning is the role of topological features in identifying network paths of communication dynamics (Avena-Koenigsberger et al, 2018). Shortest paths play a significant role in determining the integrative and coordinative capacities at the level of network elements. It was shown e.g., that in a functional brain network the closeness centrality of an area (how easy it is to reach a node via the shortest paths) influences the path length of anatomical connections between active loci, resulting in a small but not negligible elongation (∼10%) compared to the shortest path length (Csoma et al, 2017)

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