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      The significance of structural rich club hubs for the processing of hierarchical stimuli

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          Abstract

          The brain's structural network follows a hierarchy that is described as rich club (RC) organization, with RC hubs forming the well‐interconnected top of this hierarchy. In this study, we tested whether RC hubs are involved in the processing of hierarchically higher structures in stimulus sequences. Moreover, we explored the role of previously suggested cortical gradients along anterior‐posterior and medial‐lateral axes throughout the frontal cortex. To this end, we conducted a functional magnetic resonance imaging (fMRI) experiment and presented participants with blocks of digit sequences that were structured on different hierarchically nested levels. We additionally collected diffusion weighted imaging data of the same subjects to identify RC hubs. This classification then served as the basis for a region of interest analysis of the fMRI data. Moreover, we determined structural network centrality measures in areas that were found as activation clusters in the whole‐brain fMRI analysis. Our findings support the previously found anterior and medial shift for processing hierarchically higher structures of stimuli. Additionally, we found that the processing of hierarchically higher structures of the stimulus structure engages RC hubs more than for lower levels. Areas involved in the functional processing of hierarchically higher structures were also more likely to be part of the structural RC and were furthermore more central to the structural network. In summary, our results highlight the potential role of the structural RC organization in shaping the cortical processing hierarchy.

          Abstract

          We collected functional magnetic resonance imaging data during presentation of hierarchically structured stimuli, and diffusion weighted imaging data to identify the hierarchical rich club architecture in the same subjects. Integrating functional and structural data revealed an anterior‐medial frontal shift and engagement of rich club hubs for processing hierarchically higher stimulus structures.

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              A Mathematical Theory of Communication

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                Author and article information

                Contributors
                f_meck01@uni-muenster.de
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                08 December 2023
                March 2024
                : 45
                : 4 ( doiID: 10.1002/hbm.v45.4 )
                : e26543
                Affiliations
                [ 1 ] Department of Psychology, Biological Psychology University of Münster Münster Germany
                [ 2 ] Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience University of Münster Münster Germany
                [ 3 ] Institute for Translational Psychiatry University of Münster Münster Germany
                [ 4 ] Department for Psychiatry, Psychosomatic Medicine and Psychotherapy University Hospital Frankfurt, Goethe University Frankfurt Germany
                [ 5 ] Institute for Computational and Applied Mathematics University of Münster Münster Germany
                Author notes
                [*] [* ] Correspondence

                Falko Mecklenbrauck, Department of Psychology, Biological Psychology, University of Münster, Münster, Germany.

                Email: f_meck01@ 123456uni-muenster.de

                Author information
                https://orcid.org/0000-0002-8187-6826
                https://orcid.org/0000-0002-6094-9950
                https://orcid.org/0000-0002-6365-3055
                https://orcid.org/0000-0002-5532-3910
                https://orcid.org/0000-0001-8718-0128
                https://orcid.org/0000-0003-2968-4795
                https://orcid.org/0000-0002-0623-3759
                https://orcid.org/0000-0001-5802-6869
                Article
                HBM26543
                10.1002/hbm.26543
                10915744
                38069537
                2e318f08-b3c9-4502-b31c-16d023767919
                © 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 17 October 2023
                : 09 June 2023
                : 09 November 2023
                Page count
                Figures: 11, Tables: 5, Pages: 28, Words: 24728
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                March 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.9 mode:remove_FC converted:06.03.2024

                Neurology
                cortical hierarchies,dwi,fmri,nested hierarchies,rich club,structural connectivity
                Neurology
                cortical hierarchies, dwi, fmri, nested hierarchies, rich club, structural connectivity

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