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Age differences in the functional architecture of the human brain

View ORCID ProfileRoni Setton, View ORCID ProfileLaetitia Mwilambwe-Tshilobo, View ORCID ProfileManesh Girn, Amber W. Lockrow, View ORCID ProfileGiulia Baracchini, View ORCID ProfileColleen Hughes, Alexander J. Lowe, Benjamin N. Cassidy, View ORCID ProfileJian Li, Wen-Ming Luh, View ORCID ProfileDanilo Bzdok, View ORCID ProfileRichard M. Leahy, View ORCID ProfileTian Ge, View ORCID ProfileDaniel S. Margulies, View ORCID ProfileBratislav Misic, View ORCID ProfileBoris C. Bernhardt, W. Dale Stevens, View ORCID ProfileFelipe De Brigard, View ORCID ProfilePrantik Kundu, View ORCID ProfileGary R. Turner, View ORCID ProfileR. Nathan Spreng
doi: https://doi.org/10.1101/2021.03.31.437922
Roni Setton
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Laetitia Mwilambwe-Tshilobo
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Manesh Girn
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Amber W. Lockrow
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Giulia Baracchini
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Colleen Hughes
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
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Alexander J. Lowe
2Institute of Neurology, University College London
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Benjamin N. Cassidy
3Department of Psychiatry, University of Toronto, Toronto, ON, Canada
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Jian Li
4Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA, USA
5Department of Neurology, Massachusetts General Hospital, Boston, MA, USA
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Wen-Ming Luh
6National Institutes of Health, National Institute on Aging, Baltimore, MD, USA
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Danilo Bzdok
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
7Department of Biomedical Engineering, McGill University, Montreal, QC, Canada
8McConnell Brain Imaging Centre, McGill University, Montreal, QC, Canada
9School of Computer Science, McGill University, Montreal, QC, Canada
10Mila – Quebec Artificial Intelligence Institute, Montreal, QC, Canada
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Richard M. Leahy
11Department of Electrical Engineering-Systems, University of Southern California, Los Angeles, CA, USA
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Tian Ge
12Psychiatric and Neurodevelopmental Genetics Unit, Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA
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Daniel S. Margulies
13Integrative Neuroscience and Cognition Center (UMR 8002), Centre National de la Recherche Scientifique (CNRS) and Université de Paris, Paris, France
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Bratislav Misic
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
8McConnell Brain Imaging Centre, McGill University, Montreal, QC, Canada
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Boris C. Bernhardt
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
8McConnell Brain Imaging Centre, McGill University, Montreal, QC, Canada
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W. Dale Stevens
14Department of Psychology, York University, Toronto, ON, Canada
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Felipe De Brigard
15Department of Philosophy, Duke University, Durham, NC, USA
16Department of Psychology and Neuroscience, Durham, NC, USA
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Prantik Kundu
17Icahn School of Medicine at Mount Sinai, New York, NY, USA
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Gary R. Turner
14Department of Psychology, York University, Toronto, ON, Canada
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R. Nathan Spreng
1Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada
8McConnell Brain Imaging Centre, McGill University, Montreal, QC, Canada
18Departments of Psychiatry and Psychology, McGill University, Montreal, QC, Canada
19Douglas Mental Health University Institute, Verdun, QC, Canada
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  • For correspondence: nathan.spreng@gmail.com
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Abstract

The intrinsic functional organization of the brain changes into older adulthood. Age differences are observed at multiple spatial scales, from global reductions in modularity and segregation of distributed brain systems, to network-specific patterns of dedifferentiation. Whether dedifferentiation reflects an inevitable, global shift in brain function with age, circumscribed, experience dependent changes, or both, is uncertain. We employed a multi-method strategy to interrogate dedifferentiation at multiple spatial scales. Multi-echo (ME) resting-state fMRI was collected in younger (n=181) and older (n=120) healthy adults. Cortical parcellation sensitive to individual variation was implemented for precision functional mapping of each participant, while preserving group-level parcel and network labels. ME-fMRI processing and gradient mapping identified global and macroscale network differences. Multivariate functional connectivity methods tested for microscale, edge-level differences. Older adults had lower BOLD signal dimensionality, consistent with global network dedifferentiation. Gradients were largely age-invariant. Edge-level analyses revealed discrete, network-specific dedifferentiation patterns in older adults. Visual and somatosensory regions were more integrated within the functional connectome; default and frontoparietal control network regions showed greater connectivity; and the dorsal attention network was more integrated with heteromodal regions. These findings highlight the importance of multi-scale, multi-method approaches to characterize the architecture of functional brain aging.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 05, 2022.
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Age differences in the functional architecture of the human brain
Roni Setton, Laetitia Mwilambwe-Tshilobo, Manesh Girn, Amber W. Lockrow, Giulia Baracchini, Colleen Hughes, Alexander J. Lowe, Benjamin N. Cassidy, Jian Li, Wen-Ming Luh, Danilo Bzdok, Richard M. Leahy, Tian Ge, Daniel S. Margulies, Bratislav Misic, Boris C. Bernhardt, W. Dale Stevens, Felipe De Brigard, Prantik Kundu, Gary R. Turner, R. Nathan Spreng
bioRxiv 2021.03.31.437922; doi: https://doi.org/10.1101/2021.03.31.437922
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Age differences in the functional architecture of the human brain
Roni Setton, Laetitia Mwilambwe-Tshilobo, Manesh Girn, Amber W. Lockrow, Giulia Baracchini, Colleen Hughes, Alexander J. Lowe, Benjamin N. Cassidy, Jian Li, Wen-Ming Luh, Danilo Bzdok, Richard M. Leahy, Tian Ge, Daniel S. Margulies, Bratislav Misic, Boris C. Bernhardt, W. Dale Stevens, Felipe De Brigard, Prantik Kundu, Gary R. Turner, R. Nathan Spreng
bioRxiv 2021.03.31.437922; doi: https://doi.org/10.1101/2021.03.31.437922

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