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      Semantic Integration Demands Modulate Large‐Scale Network Interactions in the Brain

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          ABSTRACT

          The ability to integrate semantic information into the context of a sentence is essential for human communication. Several studies have shown that the predictability of a final keyword based on the sentence context influences semantic integration on the behavioral, neurophysiological, and neural level. However, the architecture of the underlying network interactions for semantic integration across the lifespan remains unclear. In this study, 32 healthy participants (30–75 years) performed an auditory cloze probability task during functional magnetic resonance imaging (fMRI), requiring lexical decisions on the sentence's final words. Semantic integration demands were implicitly modulated by presenting sentences with expected, unexpected, anomalous, or pseudoword endings. To elucidate network interactions supporting semantic integration, we combined univariate task‐based fMRI analyses with seed‐based connectivity and between‐network connectivity analyses. Behavioral data revealed typical semantic integration effects, with increased integration demands being associated with longer response latencies and reduced accuracy. Univariate results demonstrated increased left frontal and temporal brain activity for sentences with higher integration demands. Between‐network interactions highlighted the role of task‐positive and default mode networks for sentence processing with increased semantic integration demands. Furthermore, increasing integration demands led to a higher number of behaviorally relevant network interactions, suggesting that the increased between‐network coupling becomes more relevant for successful task performance as integration demands increase. Our findings elucidate the complex network interactions underlying semantic integration across the aging continuum. Stronger interactions between various task‐positive and default mode networks correlated with more efficient processing of sentences with increased semantic integration demands. These results may inform future studies with healthy old and clinical populations.

          Abstract

          This study elucidates the complex within‐ and between‐network interactions underlying semantic integration. Increased semantic integration demands are mainly reflected by activity in frontal control regions as well as stronger interactions between task‐positive and default mode networks.

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          The assessment and analysis of handedness: The Edinburgh inventory

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            “Mini-mental state”

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              The organization of the human cerebral cortex estimated by intrinsic functional connectivity.

              Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.
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                Author and article information

                Contributors
                nieberlein@cbs.mpg.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
                26 December 2024
                15 December 2024
                : 45
                : 18 ( doiID: 10.1002/hbm.v45.18 )
                : e70113
                Affiliations
                [ 1 ] Research Group Cognition and Plasticity Max Planck Institute for Human Cognitive and Brain Sciences Leipzig Germany
                [ 2 ] Wilhelm Wundt Institute for Psychology Leipzig University Leipzig Germany
                [ 3 ] Martin Luther University Halle‐Wittenberg Halle (Saale) Germany
                [ 4 ] University Clinic and Outpatient Clinic for Radiology University Hospital Halle (Saale) Halle Germany
                [ 5 ] Halle MR Imaging Core Facility (HMRICF) Halle (Saale) Germany
                [ 6 ] Department of Neurosurgery University Hospital Halle (Saale) Halle Germany
                [ 7 ] Department of Neurosurgery University Hospital Erlangen Erlangen Germany
                Author notes
                [*] [* ] Correspondence:

                Laura Nieberlein ( nieberlein@ 123456cbs.mpg.de )

                Author information
                https://orcid.org/0000-0002-7934-8194
                Article
                HBM70113 HBM-24-0632.R1
                10.1002/hbm.70113
                11669845
                39723465
                05b817a7-b453-4a20-8fdc-abc7b86bbb7d
                © 2024 The Author(s). 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/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 19 November 2024
                : 25 June 2024
                : 09 December 2024
                Page count
                Figures: 8, Tables: 0, Pages: 19, Words: 14500
                Funding
                Funded by: Lise Meitner Excellence funding from the Max Planck Society
                Funded by: Deutsche Forschungsgemeinschaft , doi 10.13039/501100001659;
                Award ID: HA 6314/3‐1
                Award ID: HA 6314/4‐2
                Award ID: HA 6314/9‐1
                Funded by: European Research Council , doi 10.13039/501100000781;
                Award ID: ERC‐2021‐COG 101043747
                Categories
                Research Article
                Research Article
                Custom metadata
                2.0
                December 15, 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.5.1 mode:remove_FC converted:26.12.2024

                Neurology
                cloze probability,fmri,functional connectivity,language network,network interactions
                Neurology
                cloze probability, fmri, functional connectivity, language network, network interactions

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