Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology
Studying older adults with excellent cognitive capacities (Supernormals) provides a unique opportunity for identifying factors related to cognitive success – a critical topic across lifespan. There is a limited understanding of Supernormals’ neural substrates, especially whether any of them attends...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2020-01-01
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| Series: | NeuroImage: Clinical |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158220302503 |
| _version_ | 1818390190279884800 |
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| author | Quanjing Chen Timothy M. Baran Brian Rooks M. Kerry O'Banion Mark Mapstone Zhengwu Zhang Feng Lin |
| author_facet | Quanjing Chen Timothy M. Baran Brian Rooks M. Kerry O'Banion Mark Mapstone Zhengwu Zhang Feng Lin |
| author_sort | Quanjing Chen |
| collection | DOAJ |
| description | Studying older adults with excellent cognitive capacities (Supernormals) provides a unique opportunity for identifying factors related to cognitive success – a critical topic across lifespan. There is a limited understanding of Supernormals’ neural substrates, especially whether any of them attends shaping and supporting superior cognitive function or confer resistance to age-related neurodegeneration such as Alzheimer’s disease (AD). Here, applying a state-of-the-art diffusion imaging processing pipeline and finite mixture modelling, we longitudinally examine the structural connectome of Supernormals. We find a unique structural connectome, containing the connections between frontal, cingulate, parietal, temporal, and subcortical regions in the same hemisphere that remains stable over time in Supernormals, relatively to typical agers. The connectome significantly classifies positive vs. negative AD pathology at 72% accuracy in a new sample mixing Supernormals, typical agers, and AD risk [amnestic mild cognitive impairment (aMCI)] subjects. Among this connectome, the mean diffusivity of the connection between right isthmus cingulate cortex and right precuneus most robustly contributes to predicting AD pathology across samples. The mean diffusivity of this connection links negatively to global cognition in those Supernormals with positive AD pathology. But this relationship does not exist in typical agers or aMCI. Our data suggest the presence of a structural connectome supporting cognitive success. Cingulate to precuneus white matter integrity may be useful as a structural marker for monitoring neurodegeneration and may provide critical information for understanding how some older adults maintain or excel cognitively in light of significant AD pathology. |
| first_indexed | 2024-12-14T04:53:41Z |
| format | Article |
| id | doaj.art-a36925ed4bee4f01bcedd540edd0b5f6 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-14T04:53:41Z |
| publishDate | 2020-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-a36925ed4bee4f01bcedd540edd0b5f62022-12-21T23:16:27ZengElsevierNeuroImage: Clinical2213-15822020-01-0128102413Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathologyQuanjing Chen0Timothy M. Baran1Brian Rooks2M. Kerry O'Banion3Mark Mapstone4Zhengwu Zhang5Feng Lin6Elaine C. Hubbard Center for Nursing Research on Aging, School of Nursing, University of Rochester Medical Center, United States; Department of Psychiatry, School of Medicine and Dentistry, University of Rochester Medical Center, United States; Corresponding author at: University of Rochester Medical Center, 430 Elmwood Ave, Rochester, NY 14642, United States.Department of Imaging Sciences, School of Medicine and Dentistry, University of Rochester Medical Center, United States; Department of Biomedical Engineering, University of Rochester, United StatesDepartment of Biostatistics and Computational Biology, School of Medicine and Dentistry, University of Rochester Medical Center, United StatesDepartment of Neuroscience, School of Medicine and Dentistry, University of Rochester Medical Center, United StatesDepartment of Neurology, University of California-Irvine, United StatesDepartment of Biostatistics and Computational Biology, School of Medicine and Dentistry, University of Rochester Medical Center, United StatesElaine C. Hubbard Center for Nursing Research on Aging, School of Nursing, University of Rochester Medical Center, United States; Department of Psychiatry, School of Medicine and Dentistry, University of Rochester Medical Center, United States; Department of Neuroscience, School of Medicine and Dentistry, University of Rochester Medical Center, United States; Department of Neurology, School of Medicine and Dentistry, University of Rochester Medical Center, United States; Department of Brain and Cognitive Sciences, University of Rochester, United States; Corresponding author at: University of Rochester Medical Center, 430 Elmwood Ave, Rochester, NY 14642, United States.Studying older adults with excellent cognitive capacities (Supernormals) provides a unique opportunity for identifying factors related to cognitive success – a critical topic across lifespan. There is a limited understanding of Supernormals’ neural substrates, especially whether any of them attends shaping and supporting superior cognitive function or confer resistance to age-related neurodegeneration such as Alzheimer’s disease (AD). Here, applying a state-of-the-art diffusion imaging processing pipeline and finite mixture modelling, we longitudinally examine the structural connectome of Supernormals. We find a unique structural connectome, containing the connections between frontal, cingulate, parietal, temporal, and subcortical regions in the same hemisphere that remains stable over time in Supernormals, relatively to typical agers. The connectome significantly classifies positive vs. negative AD pathology at 72% accuracy in a new sample mixing Supernormals, typical agers, and AD risk [amnestic mild cognitive impairment (aMCI)] subjects. Among this connectome, the mean diffusivity of the connection between right isthmus cingulate cortex and right precuneus most robustly contributes to predicting AD pathology across samples. The mean diffusivity of this connection links negatively to global cognition in those Supernormals with positive AD pathology. But this relationship does not exist in typical agers or aMCI. Our data suggest the presence of a structural connectome supporting cognitive success. Cingulate to precuneus white matter integrity may be useful as a structural marker for monitoring neurodegeneration and may provide critical information for understanding how some older adults maintain or excel cognitively in light of significant AD pathology.http://www.sciencedirect.com/science/article/pii/S2213158220302503SupernormalsLongitudinal designWhite matter structural connectomeAD pathologyMild cognitive impairment |
| spellingShingle | Quanjing Chen Timothy M. Baran Brian Rooks M. Kerry O'Banion Mark Mapstone Zhengwu Zhang Feng Lin Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology NeuroImage: Clinical Supernormals Longitudinal design White matter structural connectome AD pathology Mild cognitive impairment |
| title | Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology |
| title_full | Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology |
| title_fullStr | Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology |
| title_full_unstemmed | Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology |
| title_short | Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology |
| title_sort | cognitively supernormal older adults maintain a unique structural connectome that is resistant to alzheimer s pathology |
| topic | Supernormals Longitudinal design White matter structural connectome AD pathology Mild cognitive impairment |
| url | http://www.sciencedirect.com/science/article/pii/S2213158220302503 |
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