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Task-related effective connectivity reveals that the cortical rich club gates cortex-wide communication.

ABSTRACT: Higher cognition may require the globally coordinated integration of specialized brain regions into functional networks. A collection of structural cortical hubs-referred to as the rich club-has been hypothesized to support task-specific functional integration. In the present paper, we use a whole-cortex model to estimate directed interactions between 68 cortical regions from functional magnetic resonance imaging activity for four different tasks (reflecting different cognitive domains) and resting state. We analyze the state-dependent input and output effective connectivity (EC) of the structural rich club and relate these to whole-cortex dynamics and network reconfigurations. We find that the cortical rich club exhibits an increase in outgoing EC during task performance as compared with rest while incoming connectivity remains constant. Increased outgoing connectivity targets a sparse set of peripheral regions with specific regions strongly overlapping between tasks. At the same time, community detection analyses reveal massive reorganizations of interactions among peripheral regions, including those serving as target of increased rich club output. This suggests that while peripheral regions may play a role in several tasks, their concrete interplay might nonetheless be task-specific. Furthermore, we observe that whole-cortex dynamics are faster during task as compared with rest. The decoupling effects usually accompanying faster dynamics appear to be counteracted by the increased rich club outgoing EC. Together our findings speak to a gating mechanism of the rich club that supports fast-paced information exchange among relevant peripheral regions in a task-specific and goal-directed fashion, while constantly listening to the whole network.

SUBMITTER: Senden M

PROVIDER: S-EPMC6866345 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Task-related effective connectivity reveals that the cortical rich club gates cortex-wide communication.

Senden Mario M Reuter Niels N van den Heuvel Martijn P MP Goebel Rainer R Deco Gustavo G Gilson Matthieu M

Human brain mapping 20171208 3

Higher cognition may require the globally coordinated integration of specialized brain regions into functional networks. A collection of structural cortical hubs-referred to as the rich club-has been hypothesized to support task-specific functional integration. In the present paper, we use a whole-cortex model to estimate directed interactions between 68 cortical regions from functional magnetic resonance imaging activity for four different tasks (reflecting different cognitive domains) and rest ...[more]

PMID: 29222818

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Project description:Graph-theoretical analysis of brain connectivity data has revealed significant features of brain network organization across a range of species. Consistently, large-scale anatomical networks exhibit highly nonrandom attributes including an efficient small world modular architecture, with distinct network communities that are interlinked by hub regions. The functional importance of hubs motivates a closer examination of their mutual interconnections, specifically to examine the hypothesis that hub regions are more densely linked than expected based on their degree alone, i.e. forming a central rich club. Extending recent findings of rich club topology in the cat and human brain, this report presents evidence for the existence of rich club organization in the cerebral cortex of a non-human primate, the macaque monkey, based on a connectivity data set representing a collation of numerous tract tracing studies. Rich club regions comprise portions of prefrontal, parietal, temporal and insular cortex and are widely distributed across network communities. An analysis of network motifs reveals that rich club regions tend to form star-like configurations, indicative of their central embedding within sets of nodes. In addition, rich club nodes and edges participate in a large number of short paths across the network, and thus contribute disproportionately to global communication. As rich club regions tend to attract and disperse communication paths, many of the paths follow a characteristic pattern of first increasing and then decreasing node degree. Finally, the existence of non-reciprocal projections imposes a net directional flow of paths into and out of the rich club, with some regions preferentially attracting and others dispersing signals. Overall, the demonstration of rich club organization in a non-human primate contributes to our understanding of the network principles underlying neural connectivity in the mammalian brain, and further supports the hypothesis that rich club regions and connections have a central role in global brain communication.

Dataset Information

Task-related effective connectivity reveals that the cortical rich club gates cortex-wide communication.

Publications

Task-related effective connectivity reveals that the cortical rich club gates cortex-wide communication.

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