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The organization of individually mapped structural and functional semantic networks in aging adults

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Abstract

Language function in the brain, once thought to be highly localized, is now appreciated as relying on a connected but distributed network. The semantic system is of particular interest in the language domain because of its hypothesized integration of information across multiple cortical regions. Previous work in healthy individuals has focused on group-level functional connectivity (FC) analyses of the semantic system, which may obscure interindividual differences driving variance in performance. These studies also overlook the contributions of white matter networks to semantic function. Here, we identified semantic network nodes at the individual level with a semantic decision fMRI task in 53 typically aging adults, characterized network organization using structural connectivity (SC), and quantified the segregation and integration of the network using FC. Hub regions were identified in left inferior frontal gyrus. The individualized semantic network was composed of three interacting modules: (1) default-mode module characterized by bilateral medial prefrontal and posterior cingulate regions and also including right-hemisphere homotopes of language regions; (2) left frontal module extending dorsally from inferior frontal gyrus to pre-motor area; and (3) left temporoparietal module extending from temporal pole to inferior parietal lobule. FC within Module3 and integration of the entire network related to a semantic verbal fluency task, but not a matched phonological task. These results support and extend the tri-network semantic model (Xu in Front Psychol 8: 1538 1538, 2017) and the controlled semantic cognition model (Chiou in Cortex 103: 100 116, 2018) of semantic function.

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Data availability

The datasets analyzed during the current study are not presently publicly available as data collection is still ongoing. The data used for this study are available from the corresponding author on reasonable request.

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Funding

This work was supported by NIH/NIDCD R01DC014960 to PET and K99DC018828 to AD.

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Contributions

The conception and design of this study was developed by authors WTK, AD, and PET. Data collection was performed by authors SP and CV. Author WTK was responsible for material preparation, data analysis, and original manuscript writing. All authors contributed to revision and finalization of the manuscript and have approved the final version.

Corresponding author

Correspondence to W. Tyler Ketchabaw.

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The authors have no relevant financial or non-financial interests to disclose.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki, and all study procedures were approved by the Georgetown Institutional Review Board.

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Written informed consent was obtained from all participants included in this study.

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Ketchabaw, W.T., DeMarco, A.T., Paul, S. et al. The organization of individually mapped structural and functional semantic networks in aging adults. Brain Struct Funct 227, 2513–2527 (2022). https://doi.org/10.1007/s00429-022-02544-4

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  • DOI: https://doi.org/10.1007/s00429-022-02544-4

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