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Research Article

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

Mario Senden

Corresponding Author

E-mail address: mario.senden@maastrichtuniversity.nl

Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6201BC Maastricht, The Netherlands

Maastricht Brain Imaging Centre, Faculty of Psychology and Neuroscience, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands

Mario Senden and Niels Reuter contributed equally to this study.

Correspondence Mario Senden, Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, P.O. Box 616, Oxfordlaan 55, 6200 MD Maastricht, The Netherlands. Email:

mario.senden@maastrichtuniversity.nl

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Niels Reuter

Institute of Systems Neuroscience and Institute of Clinical Neuroscience & Medical Psychology, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany

Institute of Neuroscience and Medicine (INM‐1, INM‐7), Research Centre Jülich, Jülich, Germany

Mario Senden and Niels Reuter contributed equally to this study.

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Martijn P. van den Heuvel

Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, Brain Center Rudolf Magnus, 3508 GA Utrecht, The Netherlands

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Rainer Goebel

Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6201BC Maastricht, The Netherlands

Maastricht Brain Imaging Centre, Faculty of Psychology and Neuroscience, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands

Department of Neuroimaging and Neuromodeling, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences (KNAW), 1105BA Amsterdam, The Netherlands

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Gustavo Deco

Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Roc Boronat 138, Barcelona 08018, Spain

Institució Catalana de la Recerca i Estudis Avançats (ICREA), Universitat Pompeu Fabra, Passeig Lluís Companys 23, Barcelona 08010, Spain

Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany

School of Psychological Sciences, Monash University, Melbourne, Clayton VIC 3800, Australia

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Matthieu Gilson

Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Roc Boronat 138, Barcelona 08018, Spain

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First published: 08 December 2017
Cited by: 1

Funding information: European Research Council under the European Union's Seventh Framework Program (ERC‐2010‐AdG, ERC), Grant/Award Number: 269853; European Union's Horizon 2020 research and innovation program, Grant/Award Number: 720270 (HBP SGA1); ERC Advanced Grant: DYSTRUCTURE, Grant/Award Number: 295129; Spanish Research Project PSI2016‐75688‐P (AEI/FEDER), and by the European Union's Horizon 2020 research and innovation program, Grant/Award Number: 720270 (HBP SGA1); Marie Sklodowska‐Curie Action grant, Grant/Award Number: H2020‐MSCA‐656547; European Research Council Advanced Grant DYSTRUCTURE, Grant/Award Number: 295129; Human Brain Project, Grant/Award Number: FP7‐FET‐ICT‐604102; VIDI grant of The Netherlands Organization for Scientific Research, Grant/Award Number: NWO 452‐16‐015; NWO ALW open (ALWOP.179).

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.

Number of times cited according to CrossRef: 1

  • , A generative model of whole-brain effective connectivity, NeuroImage, 10.1016/j.neuroimage.2018.05.058, 179, (505-529), (2018).