Structural damage-driven brain compensation among near-centenarians and centenarians without dementia

Compensation has been proposed as a mechanism to explain how individuals in very old age remain able to maintain normal cognitive functioning. Previous studies have provided evidence on the role of increasing functional connectivity as a compensatory mechanism for age-related white matter damage. Ho...

Full description

Saved in:
Bibliographic Details
Main Authors: Hui Tang, Haichao Zhao, Hao Liu, Jiyang Jiang, Nicole Kochan, Jing Jing, Henry Brodaty, Wei Wen, Perminder S. Sachdev, Tao Liu
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811925000679
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832573254236110848
author Hui Tang
Haichao Zhao
Hao Liu
Jiyang Jiang
Nicole Kochan
Jing Jing
Henry Brodaty
Wei Wen
Perminder S. Sachdev
Tao Liu
author_facet Hui Tang
Haichao Zhao
Hao Liu
Jiyang Jiang
Nicole Kochan
Jing Jing
Henry Brodaty
Wei Wen
Perminder S. Sachdev
Tao Liu
author_sort Hui Tang
collection DOAJ
description Compensation has been proposed as a mechanism to explain how individuals in very old age remain able to maintain normal cognitive functioning. Previous studies have provided evidence on the role of increasing functional connectivity as a compensatory mechanism for age-related white matter damage. However, we lack direct investigation into how these mechanisms contribute to the preservation of cognition in the very old population. We examined a cohort of near-centenarians and centenarians without dementia (aged 95-103 years, n=44). We constructed a structural disconnection matrix based on the disruption of white matter pathways caused by white matter hyperintensities (WMHs), aiming to explore the relationship between functional connections, cognitive preservation and white matter damage. Our results revealed that structural damage can reliably explain the variations of functional connections or cognitive maintenance. Notably, we found significant correlations between the weights in the functional connectivity model and the weights in the cognition model. We observed positive correlations between models for brain disconnections and cognitive function in near-centenarians and centenarians. The strongest effects were found between attention and somatomotor network (SMN) (r=0.397, p<0.001), memory and SMN (r=0.333 p<0.001), fluency and visual network (VIS) - control network (CN) (r=0.406, p<0.001), language and VIS (r=0.309, p<0.001), visuospatial ability and VIS-default mode network (DMN) (r=0.464, p<0.001), as well as global cognition and VIS-DMN (r=0.335, p<0.001). These findings suggest that enhancement of functional connectivity may serve as a compensatory mechanism, such that it mitigates the effects of white matter damage and contributes to preserved cognitive performance in very old age.
format Article
id doaj-art-e62ac8fe27ac46628efe32d4b59e72e8
institution Kabale University
issn 1095-9572
language English
publishDate 2025-03-01
publisher Elsevier
record_format Article
series NeuroImage
spelling doaj-art-e62ac8fe27ac46628efe32d4b59e72e82025-02-02T05:26:51ZengElsevierNeuroImage1095-95722025-03-01308121065Structural damage-driven brain compensation among near-centenarians and centenarians without dementiaHui Tang0Haichao Zhao1Hao Liu2Jiyang Jiang3Nicole Kochan4Jing Jing5Henry Brodaty6Wei Wen7Perminder S. Sachdev8Tao Liu9Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, International Research Institute for Multidisciplinary Science, Beihang University, Beijing 100191, ChinaBeijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, International Research Institute for Multidisciplinary Science, Beihang University, Beijing 100191, China; Faculty of Psychology, MOE Key Laboratory of Cognition and Personality, Southwest University, Chongqing, ChinaBeijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, International Research Institute for Multidisciplinary Science, Beihang University, Beijing 100191, ChinaCentre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, AustraliaCentre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, Australia; Neuropsychiatric Institute, Prince of Wales Hospital, Sydney, NSW, AustraliaChina National Clinical Research Center for Neurological Diseases, Beijing, China; Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, ChinaCentre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, AustraliaCentre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, Australia; Neuropsychiatric Institute, Prince of Wales Hospital, Sydney, NSW, AustraliaCentre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, Australia; Neuropsychiatric Institute, Prince of Wales Hospital, Sydney, NSW, Australia; Corresponding author at: Centre for Healthy Brain Ageing (CHeBA), School of Psychiatry, University of New South Wales, Prince of Wales Hospital, Barker Street, Randwick, NSW 2031, AustraliaBeijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, International Research Institute for Multidisciplinary Science, Beihang University, Beijing 100191, China; Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Beijing, China; Corresponding author at: Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, International Research Institute for Multidisciplinary Science, Beihang University, Beijing 100191, China.Compensation has been proposed as a mechanism to explain how individuals in very old age remain able to maintain normal cognitive functioning. Previous studies have provided evidence on the role of increasing functional connectivity as a compensatory mechanism for age-related white matter damage. However, we lack direct investigation into how these mechanisms contribute to the preservation of cognition in the very old population. We examined a cohort of near-centenarians and centenarians without dementia (aged 95-103 years, n=44). We constructed a structural disconnection matrix based on the disruption of white matter pathways caused by white matter hyperintensities (WMHs), aiming to explore the relationship between functional connections, cognitive preservation and white matter damage. Our results revealed that structural damage can reliably explain the variations of functional connections or cognitive maintenance. Notably, we found significant correlations between the weights in the functional connectivity model and the weights in the cognition model. We observed positive correlations between models for brain disconnections and cognitive function in near-centenarians and centenarians. The strongest effects were found between attention and somatomotor network (SMN) (r=0.397, p<0.001), memory and SMN (r=0.333 p<0.001), fluency and visual network (VIS) - control network (CN) (r=0.406, p<0.001), language and VIS (r=0.309, p<0.001), visuospatial ability and VIS-default mode network (DMN) (r=0.464, p<0.001), as well as global cognition and VIS-DMN (r=0.335, p<0.001). These findings suggest that enhancement of functional connectivity may serve as a compensatory mechanism, such that it mitigates the effects of white matter damage and contributes to preserved cognitive performance in very old age.http://www.sciencedirect.com/science/article/pii/S1053811925000679(Near-)centenariansWhite matter hyperintensitiesCompensatory mechanismFunctional connectionsCognition
spellingShingle Hui Tang
Haichao Zhao
Hao Liu
Jiyang Jiang
Nicole Kochan
Jing Jing
Henry Brodaty
Wei Wen
Perminder S. Sachdev
Tao Liu
Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
NeuroImage
(Near-)centenarians
White matter hyperintensities
Compensatory mechanism
Functional connections
Cognition
title Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
title_full Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
title_fullStr Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
title_full_unstemmed Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
title_short Structural damage-driven brain compensation among near-centenarians and centenarians without dementia
title_sort structural damage driven brain compensation among near centenarians and centenarians without dementia
topic (Near-)centenarians
White matter hyperintensities
Compensatory mechanism
Functional connections
Cognition
url http://www.sciencedirect.com/science/article/pii/S1053811925000679
work_keys_str_mv AT huitang structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT haichaozhao structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT haoliu structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT jiyangjiang structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT nicolekochan structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT jingjing structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT henrybrodaty structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT weiwen structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT perminderssachdev structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia
AT taoliu structuraldamagedrivenbraincompensationamongnearcentenariansandcentenarianswithoutdementia