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...
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Elsevier
2025-03-01
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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 |
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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. |
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language | English |
publishDate | 2025-03-01 |
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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 |
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