Exploring Successful Cognitive Aging: Insights Regarding Brain Structure, Function, and Demographics
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Magnetic Resonance Imaging (MRI)
2.2.1. T1-Weighted MRI (T1)
2.2.2. Diffusion-Weighted MRI (dMRI)
2.2.3. Resting Functional Brain MRI (rs-fMRI)
2.3. Neuropsychological Testing
2.4. Definition of a Successful Cognitive Aging Population
2.5. Demographic Factors
2.6. Statistical Analyses
3. Results
3.1. T1
3.2. DMRI
3.3. Rs-fMRI
3.4. Demographic Analysis
4. Discussion
4.1. Grey Matter Morphology
4.2. Brain Network Connectivity Strength
4.3. White Matter Microstructure
4.4. Factors of Life
4.5. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rowe, J.W.; Kahn, R.L. Successful Aging. Gerontologist 1997, 37, 433–440. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.-H.; Park, S. A Meta-Analysis of the Correlates of Successful Aging in Older Adults. Res. Aging 2017, 39, 657–677. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Lin, L.; Wu, S. A Review of Brain Atrophy Subtypes Definition and Analysis for Alzheimer’s Disease Heterogeneity Studies. J. Alzheimer Dis. 2021, 80, 1339–1352. [Google Scholar] [CrossRef] [PubMed]
- Rowe, J.W.; Kahn, R.L. Human aging: Usual and successful. Science 1987, 237, 143–149. [Google Scholar] [CrossRef]
- Hendrie, H.C.; Albert, M.S.; Butters, M.A.; Gao, S.; Knopman, D.S.; Launer, L.J.; Yaffe, K.; Cuthbert, B.N.; Edwards, E.; Wagster, M.V. The NIH Cognitive and Emotional Health Project. Report of the Critical Evaluation Study Committee. Alzheimers Dement. 2006, 2, 12–32. [Google Scholar] [CrossRef]
- Mapstone, M.; Lin, F.; Nalls, M.A.; Cheema, A.K.; Singleton, A.B.; Fiandaca, M.S.; Federoff, H.J. What success can teach us about failure: The plasma metabolome of older adults with superior memory and lessons for Alzheimer’s disease. Neurobiol. Aging 2017, 51, 148–155. [Google Scholar] [CrossRef]
- Lin, F.; Ren, P.; Mapstone, M.; Meyers, S.P.; Porsteinsson, A.; Baran, T.M. Alzheimer’s Disease Neuroimaging Initiative. The cingulate cortex of older adults with excellent memory capacity. Cortex 2017, 86, 83–92. [Google Scholar] [CrossRef]
- Rogalski, E.J.; Gefen, T.; Shi, J.; Samimi, M.; Bigio, E.; Weintraub, S.; Geula, C.; Mesulam, M.-M. Youthful Memory Capacity in Old Brains: Anatomic and Genetic Clues from the Northwestern SuperAging Project. J. Cogn. Neurosci. 2013, 25, 29–36. [Google Scholar] [CrossRef]
- Gefen, T.; Peterson, M.; Papastefan, S.T.; Martersteck, A.; Whitney, K.; Rademaker, A.; Bigio, E.H.; Weintraub, S.; Rogalski, E.; Mesulam, M.-M.; et al. Morphometric and Histologic Substrates of Cingulate Integrity in Elders with Exceptional Memory Capacity. J. Neurosci. 2015, 35, 1781–1791. [Google Scholar] [CrossRef]
- Sun, F.W.; Stepanovic, M.R.; Andreano, J.; Barrett, L.F.; Touroutoglou, A.; Dickerson, B.C. Youthful Brains in Older Adults: Preserved Neuroanatomy in the Default Mode and Salience Networks Contributes to Youthful Memory in Superaging. J. Neurosci. 2016, 36, 9659–9668. [Google Scholar] [CrossRef]
- Lin, F.V.; Wang, X.; Wu, R.; Rebok, G.W.; Chapman, B.P.; Alzheimer’s Disease Neuroimaging Initiative. Identification of Successful Cognitive Aging in the Alzheimer’s Disease Neuroimaging Initiative Study. J. Alzheimers Dis. 2017, 59, 101–111. [Google Scholar] [CrossRef] [PubMed]
- Halaschek-Wiener, J.; Tindale, L.C.; Collins, J.A.; Leach, S.; McManus, B.; Madden, K.; Meneilly, G.; Le, N.D.; Connors, J.M.; Brooks-Wilson, A.R. The Super-Seniors Study: Phenotypic characterization of a healthy 85+ population. PLoS ONE 2018, 13, e0197578. [Google Scholar] [CrossRef] [PubMed]
- Harrison, T.M.; Weintraub, S.; Mesulam, M.-M.; Rogalski, E. Superior Memory and Higher Cortical Volumes in Unusually Successful Cognitive Aging. J. Int. Neuropsychol. Soc. 2012, 18, 1081–1085. [Google Scholar] [CrossRef] [PubMed]
- Rosano, C.; Aizenstein, H.J.; Newman, A.B.; Venkatraman, V.; Harris, T.; Ding, J.; Satterfield, S.; Yaffe, K.; Health ABC Study. Neuroimaging differences between older adults with maintained versus declining cognition over a 10-year period. NeuroImage 2012, 62, 307–313. [Google Scholar] [CrossRef] [PubMed]
- Garo-Pascual, M.; Gaser, C.; Zhang, L.; Tohka, J.; Medina, M.; A Strange, B. Brain structure and phenotypic profile of superagers compared with age-matched older adults: A longitudinal analysis from the Vallecas Project. Lancet Health Longev. 2023, 4, e374–e385. [Google Scholar] [CrossRef] [PubMed]
- Dekhtyar, M.; Papp, K.V.; Buckley, R.; Jacobs, H.I.; Schultz, A.P.; Johnson, K.A.; Sperling, R.A.; Rentz, D.M. Neuroimaging markers associated with maintenance of optimal memory performance in late-life. Neuropsychologia 2017, 100, 164–170. [Google Scholar] [CrossRef]
- Chen, Q.; Baran, T.M.; Rooks, B.; O’Banion, M.K.; Mapstone, M.; Zhang, Z.; Lin, F.; Alzheimer’s Disease Neuroimaging Initiative. Cognitively supernormal older adults maintain a unique structural connectome that is resistant to Alzheimer’s pathology. NeuroImage Clin. 2020, 28, 102413. [Google Scholar] [CrossRef]
- Baran, T.M.; Lin, F.V.; Alzheimer’s Disease Neuroimaging Initiative. Amyloid and FDG PET of Successful Cognitive Aging: Global and Cingulate-Specific Differences. J. Alzheimers Dis. 2018, 66, 307–318. [Google Scholar] [CrossRef]
- Collins, R. What makes UK Biobank special? Lancet 2012, 379, 1173–1174. [Google Scholar] [CrossRef]
- Trehearne, A. Genetics, lifestyle and environment. UK Biobank is an open access resource following the lives of 500,000 participants to improve the health of future generations. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2016, 59, 361–367. [Google Scholar] [CrossRef]
- Miller, K.L.; Alfaro-Almagro, F.; Bangerter, N.K.; Thomas, D.L.; Yacoub, E.; Xu, J.; Bartsch, A.J.; Jbabdi, S.; Sotiropoulos, S.N.; Andersson, J.L.R.; et al. Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nat. Neurosci. 2016, 19, 1523–1536. [Google Scholar] [CrossRef] [PubMed]
- Chung, B.S.; Park, J.S. Automatic segmentation of true color sectioned images using FMRIB Software Library: First trial in brain, gray matter, and white matter. Clin. Anat. 2020, 33, 1197–1203. [Google Scholar] [CrossRef] [PubMed]
- Amann, M.; Andělová, M.; Pfister, A.; Mueller-Lenke, N.; Traud, S.; Reinhardt, J.; Magon, S.; Bendfeldt, K.; Kappos, L.; Radue, E.-W.; et al. Subcortical brain segmentation of two dimensional T1-weighted data sets with FMRIB’s Integrated Registration and Segmentation Tool (FIRST). NeuroImage Clin. 2014, 7, 43–52. [Google Scholar] [CrossRef] [PubMed]
- Fujihara, K.; Takei, Y. FreeSurfer as a Platform for Associating Brain Structure with Function. Brain Nerve. 2018, 70, 841–848. [Google Scholar] [CrossRef] [PubMed]
- Jao, C.-W.; Lau, C.I.; Lien, L.-M.; Tsai, Y.-F.; Chu, K.-E.; Hsiao, C.-Y.; Yeh, J.-H.; Wu, Y.-T. Using Fractal Dimension Analysis with the Desikan–Killiany Atlas to Assess the Effects of Normal Aging on Subregional Cortex Alterations in Adulthood. Brain Sci. 2021, 11, 107. [Google Scholar] [CrossRef] [PubMed]
- Mckee, M.; Britton, A. The positive relationship between alcohol and heart disease in eastern Europe: Potential physiological mechanisms. J. R. Soc. Med. 1998, 91, 402–407. [Google Scholar] [CrossRef]
- Smith, S.M.; Jenkinson, M.; Johansen-Berg, H.; Rueckert, D.; Nichols, T.E.; Mackay, C.E.; Watkins, K.E.; Ciccarelli, O.; Cader, M.Z.; Matthews, P.M.; et al. Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31, 1487–1505. [Google Scholar] [CrossRef] [PubMed]
- De Groot, M.; Vernooij, M.W.; Klein, S.; Ikram, M.A.; Vos, F.M.; Smith, S.M.; Niessen, W.J.; Andersson, J.L. Improving alignment in Tract-based spatial statistics: Evaluation and optimization of image registration. NeuroImage 2013, 76, 400–411. [Google Scholar] [CrossRef]
- Wakana, S.; Caprihan, A.; Panzenboeck, M.M.; Fallon, J.H.; Perry, M.; Gollub, R.L.; Hua, K.; Zhang, J.; Jiang, H.; Dubey, P.; et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage 2007, 36, 630–644. [Google Scholar] [CrossRef]
- Behrens, T.E.; Woolrich, M.W.; Jenkinson, M.; Johansen-Berg, H.; Nunes, R.G.; Clare, S.; Matthews, P.M.; Brady, J.M.; Smith, S.M. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 2003, 50, 1077–1088. [Google Scholar] [CrossRef]
- Behrens, T.; Berg, H.J.; Jbabdi, S.; Rushworth, M.; Woolrich, M. Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? NeuroImage 2007, 34, 144–155. [Google Scholar] [CrossRef] [PubMed]
- Jbabdi, S.; Sotiropoulos, S.N.; Savio, A.M.; Graña, M.; Behrens, T.E.J. Model-based analysis of multishell diffusion MR data for tractography: How to get over fitting problems. Magn. Reson. Med. 2012, 68, 1846–1855. [Google Scholar] [CrossRef] [PubMed]
- Beckmann, C.F.; Smith, S.M. Probabilistic Independent Component Analysis for Functional Magnetic Resonance Imaging. IEEE Trans. Med Imaging 2004, 23, 137–152. [Google Scholar] [CrossRef]
- Kapogiannis, D.; Reiter, D.A.; Willette, A.A.; Mattson, M.P. Posteromedial cortex glutamate and GABA predict intrinsic functional connectivity of the default mode network. NeuroImage 2013, 64, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Anatürk, M.; Suri, S.; Smith, S.M.; Ebmeier, K.P.; Sexton, C.E. Leisure Activities and Their Relationship With MRI Measures of Brain Structure, Functional Connectivity, and Cognition in the UK Biobank Cohort. Front. Aging Neurosci. 2021, 13, 734866. [Google Scholar] [CrossRef]
- Fawns-Ritchie, C.; Deary, I.J. Reliability and validity of the UK Biobank cognitive tests. PLoS ONE 2020, 15, e0231627. [Google Scholar] [CrossRef] [PubMed]
- Sumowski, J.F. Cognitive Reserve as a Useful Concept for Early Intervention Research in Multiple Sclerosis. Front. Neurol. 2015, 6, 176. [Google Scholar] [CrossRef]
- Anatürk, M.; Kaufmann, T.; Cole, J.H.; Suri, S.; Griffanti, L.; Zsoldos, E.; Filippini, N.; Singh-Manoux, A.; Kivimäki, M.; Westlye, L.T.; et al. Prediction of brain age and cognitive age: Quantifying brain and cognitive maintenance in aging. Hum. Brain Mapp. 2020, 42, 1626–1640. [Google Scholar] [CrossRef]
- Lin, L.; Xiong, M.; Jin, Y.; Kang, W.; Wu, S.; Sun, S.; Fu, Z. Quantifying Brain and Cognitive Maintenance as Key Indicators for Sustainable Cognitive Aging: Insights from the UK Biobank. Sustainability 2023, 15, 9620. [Google Scholar] [CrossRef]
- Stahl, K.; Adorjan, K.; Anderson-Schmidt, H.; Budde, M.; Comes, A.L.; Gade, K.; Heilbronner, M.; Kalman, J.L.; Klöhn-Saghatolislam, F.; Kohshour, M.O.; et al. Stability over time of scores on psychiatric rating scales, questionnaires and cognitive tests in healthy controls. BJPsych Open 2022, 8, e55. [Google Scholar] [CrossRef]
- Soares, B.C.; Bacha, J.M.R.; Mello, D.D.; Moretto, E.G.; Fonseca, T.; Vieira, K.S.; de Lima, A.F.; Lange, B.; Torriani-Pasin, C.; Lopes, R.d.D.; et al. Immersive Virtual Tasks With Motor and Cognitive Components: A Feasibility Study With Young and Older Adults. J. Aging Phys. Act. 2021, 29, 400–411. [Google Scholar] [CrossRef] [PubMed]
- Schober, P.; Vetter, T.R. Chi-square Tests in Medical Research. Anesth. Analg. 2019, 129, 1193. [Google Scholar] [CrossRef] [PubMed]
- Murray, M.H.; Blume, J.D. FDRestimation: Flexible False Discovery Rate Computation in R. F1000Research 2021, 10, 441. [Google Scholar] [CrossRef] [PubMed]
- Alfaro-Almagro, F.; McCarthy, P.; Afyouni, S.; Andersson, J.L.; Bastiani, M.; Miller, K.L.; Nichols, T.E.; Smith, S.M. Confound modelling in UK Biobank brain imaging. NeuroImage 2021, 224, 117002. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Martins-Bach, A.B.; Alfaro-Almagro, F.; Douaud, G.; Klein, J.C.; Llera, A.; Fiscone, C.; Bowtell, R.; Elliott, L.T.; Smith, S.M.; et al. Phenotypic and genetic associations of quantitative magnetic susceptibility in UK Biobank brain imaging. Nat. Neurosci. 2022, 25, 818–831. [Google Scholar] [CrossRef] [PubMed]
- Xiong, M.; Lin, L.; Jin, Y.; Kang, W.; Wu, S.; Sun, S. Comparison of Machine Learning Models for Brain Age Prediction Using Six Imaging Modalities on Middle-Aged and Older Adults. Sensors 2023, 23, 3622. [Google Scholar] [CrossRef] [PubMed]
- Fitzhugh, M.C.; Hemesath, A.; Schaefer, S.Y.; Baxter, L.C.; Rogalsky, C. Functional Connectivity of Heschl’s Gyrus Associated With Age-Related Hearing Loss: A Resting-State fMRI Study. Front. Psychol. 2019, 10, 2485. [Google Scholar] [CrossRef]
- Fattah, M.; Raman, M.M.; Reiss, A.L.; Green, T. PTPN11 Mutations in the Ras-MAPK Signaling Pathway Affect Human White Matter Microstructure. Cereb. Cortex 2021, 31, 1489–1499. [Google Scholar] [CrossRef]
- Golub, J.S.; Brickman, A.M.; Ciarleglio, A.J.; Schupf, N.; Luchsinger, J.A. Association of Subclinical Hearing Loss With Cognitive Performance. JAMA Otolaryngol. Head Neck Surg. 2020, 146, 57–67. [Google Scholar] [CrossRef]
- Livingston, G.; Huntley, J.; Sommerlad, A.; Ames, D.; Ballard, C.; Banerjee, S.; Brayne, C.; Burns, A.; Cohen-Mansfield, J.; Cooper, C.; et al. Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet 2020, 396, 413–446. [Google Scholar] [CrossRef]
- Xu, M.; Shao, J.; Liu, B.; Wang, L.; Ding, H.; Zhang, Y. Aging-Related Decline in Phonated and Whispered Speech Perception Not Compensated For by Increased Duration and Intensity: Evidence From Mandarin-Speaking Adult Listeners. J. Speech Lang. Hear. Res. 2023, 66, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Pichora-Fuller, M.K. Cognitive aging and auditory information processing. Int. J. Audiol. 2003, 42 S2, 26–32. [Google Scholar] [CrossRef] [PubMed]
- Boschert, J.; Deecke, L. Cerebral potentials preceding voluntary toe, knee and hip movements and their vectors in human precentral gyrus. Brain Res. 1986, 376, 175–179. [Google Scholar] [CrossRef] [PubMed]
- Conner, K.; Sweeney, C.Y.; Brown, T.; Childs, L.; Rogers, S.; Gregory, T. Practical applications of physical activity for successful cognitive aging. J. Am. Acad. Physician Assist. 2017, 30, 30–35. [Google Scholar] [CrossRef] [PubMed]
- Lipardo, D.S.; Tsang, W.W.N. Falls prevention through physical and cognitive training (falls PACT) in older adults with mild cognitive impairment: A randomized controlled trial protocol. BMC Geriatr. 2018, 18, 193. [Google Scholar] [CrossRef] [PubMed]
- Swagerman, S.C.; de Geus, E.J.; Koenis, M.M.; Pol, H.E.H.; Boomsma, D.I.; Kan, K.-J. Domain dependent associations between cognitive functioning and regular voluntary exercise behavior. Brain Cogn. 2015, 97, 32–39. [Google Scholar] [CrossRef] [PubMed]
- Shiee, N.; Bazin, P.-L.; Zackowski, K.M.; Farrell, S.K.; Harrison, D.M.; Newsome, S.D.; Ratchford, J.N.; Caffo, B.S.; Calabresi, P.A.; Pham, D.L.; et al. Revisiting Brain Atrophy and Its Relationship to Disability in Multiple Sclerosis. PLoS ONE 2012, 7, e37049. [Google Scholar] [CrossRef]
- Nugent, A.C.; Luckenbaugh, D.A.; Wood, S.E.; Bogers, W.; Zarate, C.A.; Drevets, W.C. Automated subcortical segmentation using FIRST: Test-retest reliability, interscanner reliability, and comparison to manual segmentation. Hum. Brain Mapp. 2012, 34, 2313–2329. [Google Scholar] [CrossRef]
- Morys, F.; Dadar, M.; Dagher, A. Obesity impairs cognitive function via metabolic syndrome and cerebrovascular disease: An SEM analysis in 15,000 adults from the UK Biobank. bioRxiv 2020. [Google Scholar] [CrossRef]
- Potvin, O.; Mouiha, A.; Dieumegarde, L.; Duchesne, S.; Alzheimer’s Disease Neuroimaging Initiative. Normative data for subcortical regional volumes over the lifetime of the adult human brain. NeuroImage 2016, 137, 9–20. [Google Scholar] [CrossRef]
- Pfefferbaum, A.; Rohlfing, T.; Rosenbloom, M.J.; Chu, W.; Colrain, I.M.; Sullivan, E.V. Variation in longitudinal trajectories of regional brain volumes of healthy men and women (ages 10 to 85 years) measured with atlas-based parcellation of MRI. NeuroImage 2013, 65, 176–193. [Google Scholar] [CrossRef] [PubMed]
- Betzel, R.F.; Bassett, D.S. Multi-scale brain networks. NeuroImage 2017, 160, 73–83. [Google Scholar] [CrossRef] [PubMed]
- Martín-Signes, M.; Cano-Melle, C.; Chica, A.B. Fronto-parietal networks underlie the interaction between executive control and conscious perception: Evidence from TMS and DWI. Cortex 2021, 134, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Varela-López, B.; Cruz-Gómez, J.; Lojo-Seoane, C.; Díaz, F.; Pereiro, A.; Zurrón, M.; Lindín, M.; Galdo-Álvarez, S. Cognitive reserve, neurocognitive performance, and high-order resting-state networks in cognitively unimpaired aging. Neurobiol. Aging 2022, 117, 151–164. [Google Scholar] [CrossRef] [PubMed]
- Afifi, A.K. The basal ganglia: A neural network with more than motor function. Semin. Pediatr. Neurol. 2003, 10, 3–10. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Liu, L.; Cheng, X.; Ge, H.; Hu, G.; Xue, C.; Qi, W.; Xu, W.; Chen, S.; Gao, R.; et al. Functional Integrity of Executive Control Network Contributed to Retained Executive Abilities in Mild Cognitive Impairment. Front. Aging Neurosci. 2021, 13, 710172. [Google Scholar] [CrossRef] [PubMed]
- Buckner, R.L.; Andrews-Hanna, E.J.R.; Schactera, D.L. The Brain’s Default Network: Anatomy, Function, and Relevance to Disease. Ann. N. Y. Acad. Sci. 2008, 1124, 1–38. [Google Scholar] [CrossRef]
- Dziechciaż, M.; Filip, R. Biological psychological and social determinants of old age: Bio-psycho-social aspects of human aging. Ann. Agric. Environ. Med. 2014, 21, 835–838. [Google Scholar] [CrossRef]
- Michielse, S.; Coupland, N.; Camicioli, R.; Carter, R.; Seres, P.; Sabino, J.; Malykhin, N. Selective effects of aging on brain white matter microstructure: A diffusion tensor imaging tractography study. NeuroImage 2010, 52, 1190–1201. [Google Scholar] [CrossRef]
- Kennedy, K.M.; Raz, N. Aging white matter and cognition: Differential effects of regional variations in diffusion properties on memory, executive functions, and speed. Neuropsychologia 2009, 47, 916–927. [Google Scholar] [CrossRef] [PubMed]
- Hsu, J.-L.; Van Hecke, W.; Bai, C.-H.; Lee, C.-H.; Tsai, Y.-F.; Chiu, H.-C.; Jaw, F.-S.; Hsu, C.-Y.; Leu, J.-G.; Chen, W.-H.; et al. Microstructural white matter changes in normal aging: A diffusion tensor imaging study with higher-order polynomial regression models. NeuroImage 2010, 49, 32–43. [Google Scholar] [CrossRef] [PubMed]
- Cox, S.R.; Ritchie, S.J.; Tucker-Drob, E.M.; Liewald, D.C.; Hagenaars, S.P.; Davies, G.; Wardlaw, J.M.; Gale, C.R.; Bastin, M.E.; Deary, I.J. Ageing and brain white matter structure in 3,513 UK Biobank participants. Nat. Commun. 2016, 7, 13629. [Google Scholar] [CrossRef] [PubMed]
- Zhong, W.-J.; Guo, D.-J.; Zhao, J.-N.; Xie, W.-B.; Chen, W.-J.; Wu, W. Changes of axial and radial diffusivities in cerebral white matter led by normal aging. Diagn. Interv. Imaging 2012, 93, 47–52. [Google Scholar] [CrossRef] [PubMed]
- Bennett, I.J.; Madden, D.J.; Vaidya, C.J.; Howard, D.V.; Howard, J.H. Age-related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging. Hum. Brain Mapp. 2010, 31, 378–390. [Google Scholar] [CrossRef] [PubMed]
- Burzynska, A.; Preuschhof, C.; Bäckman, L.; Nyberg, L.; Li, S.-C.; Lindenberger, U.; Heekeren, H. Age-related differences in white matter microstructure: Region-specific patterns of diffusivity. NeuroImage 2010, 49, 2104–2112. [Google Scholar] [CrossRef] [PubMed]
- Arfanakis, K.; Wilson, R.S.; Barth, C.M.; Capuano, A.W.; Vasireddi, A.; Zhang, S.; Fleischman, D.A.; Bennett, D.A. Cognitive activity, cognitive function, and brain diffusion characteristics in old age. Brain Imaging Behav. 2016, 10, 455–463. [Google Scholar] [CrossRef]
- Zeng, W.; Chen, Y.; Zhu, Z.; Gao, S.; Xia, J.; Chen, X.; Jia, J.; Zhang, Z. Severity of white matter hyperintensities: Lesion patterns, cognition, and microstructural changes. J. Cereb. Blood Flow Metab. 2020, 40, 2454–2463. [Google Scholar] [CrossRef]
- Berron, D.; van Westen, D.; Ossenkoppele, R.; Strandberg, O.; Hansson, O. Medial temporal lobe connectivity and its associations with cognition in early Alzheimer’s disease. Brain 2020, 143, 1233–1248. [Google Scholar] [CrossRef]
- Pietracupa, S.; Belvisi, D.; Piervincenzi, C.; Tommasin, S.; Pasqua, G.; Petsas, N.; De Bartolo, M.I.; Fabbrini, A.; Costanzo, M.; Manzo, N.; et al. White and gray matter alterations in de novo PD patients: Which matter most? J. Neurol. 2023, 270, 2734–2742. [Google Scholar] [CrossRef]
- Stern, Y.; Arenaza-Urquiljo, E.M.; Bartrés-Faz, D.; Belleville, S.; Cantillon, M.; Chetelat, G.; Ewers, M.; Franzmeier, N.; Kempermann, G.; Kremen, W.S.; et al. Whitepaper: Defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimer Dement. 2020, 16, 1305–1311. [Google Scholar] [CrossRef]
- Hüppi, P.S. Growth and development of the brain and impact on cognitive outcomes. Nestle Nutr. Workshop Ser. Pediatr Program. 2010, 65, 137–151. [Google Scholar] [CrossRef] [PubMed]
- Jin, Y.; Lin, L.; Xiong, M.; Sun, S.; Wu, S.-C. Moderating effects of cognitive reserve on the relationship between brain structure and cognitive abilities in middle-aged and older adults. Neurobiol. Aging 2023, 128, 49–64. [Google Scholar] [CrossRef] [PubMed]
- Lin, L.; Jin, Y.; Xiong, M.; Wu, S.; Sun, S. The Protective Power of Cognitive Reserve: Examining White Matter Integrity and Cognitive Function in the Aging Brain for Sustainable Cognitive Health. Sustainability 2023, 15, 11336. [Google Scholar] [CrossRef]
- Jung, J.; Cloutman, L.L.; Binney, R.J.; Ralph, M.A.L. The structural connectivity of higher order association cortices reflects human functional brain networks. Cortex 2017, 97, 221–239. [Google Scholar] [CrossRef] [PubMed]
- Chang, R.C.-C.; Ho, Y.-S.; Wong, S.; Gentleman, S.M.; Ng, H.-K. Neuropathology of cigarette smoking. Acta Neuropathol. 2014, 127, 53–69. [Google Scholar] [CrossRef] [PubMed]
- Ernst, M.; Heishman, S.J.; Bs, L.S.; London, E.D. Smoking History and Nicotine Effects on Cognitive Performance. Neuropsychopharmacology 2001, 25, 313–319. [Google Scholar] [CrossRef] [PubMed]
- Krivanek, T.J.; Gale, S.A.; McFeeley, B.M.; Nicastri, C.M.; Daffner, K.R. Promoting Successful Cognitive Aging: A Ten-Year Update. J. Alzheimers Dis. 2021, 81, 871–920. [Google Scholar] [CrossRef] [PubMed]
- Swan, G.E.; Lessov-Schlaggar, C.N. The Effects of Tobacco Smoke and Nicotine on Cognition and the Brain. Neuropsychol. Rev. 2007, 17, 259–273. [Google Scholar] [CrossRef]
- Gallinat, J.; Meisenzahl, E.; Jacobsen, L.K.; Kalus, P.; Bierbrauer, J.; Kienast, T.; Witthaus, H.; Leopold, K.; Seifert, F.; Schubert, F.; et al. Smoking and structural brain deficits: A volumetric MR investigation. Eur. J. Neurosci. 2006, 24, 1744–1750. [Google Scholar] [CrossRef]
- Campos, M.W.; Serebrisky, D.; Castaldelli-Maia, J.M. Smoking and Cognition. Curr. Drug Abus. Rev. 2016, 9, 76–79. [Google Scholar] [CrossRef]
- Ning, K.; Zhao, L.; Matloff, W.; Sun, F.; Toga, A.W. Association of relative brain age with tobacco smoking, alcohol consumption, and genetic variants. Sci. Rep. 2020, 10, 10. [Google Scholar] [CrossRef] [PubMed]
- Angebrandt, A.; Abulseoud, O.A.; Kisner, M.; Diazgranados, N.; Momenan, R.; Yang, Y.; Stein, E.A.; Ross, T.J. Dose-dependent relationship between social drinking and brain aging. Neurobiol. Aging 2021, 111, 71–81. [Google Scholar] [CrossRef] [PubMed]
- Funk-White, M.; Moore, A.A.; McEvoy, L.K.; Bondi, M.W.; Bergstrom, J.; Kaufmann, C.N. Alcohol use and cognitive performance: A comparison between Greece and the United States. Aging Ment. Health 2021, 26, 2440–2446. [Google Scholar] [CrossRef] [PubMed]
- Piumatti, G.; Moore, S.C.; Berridge, D.M.; Sarkar, C.; Gallacher, J. The relationship between alcohol use and long-term cognitive decline in middle and late life: A longitudinal analysis using UK Biobank. J. Public Health 2018, 40, 313–314. [Google Scholar] [CrossRef]
- Jia, R.-X.; Liang, J.-H.; Xu, Y.; Wang, Y.-Q. Effects of physical activity and exercise on the cognitive function of patients with Alzheimer disease: A meta-analysis. BMC Geriatr. 2019, 19, 181. [Google Scholar] [CrossRef]
- Sewell, K.R.; Erickson, K.I.; Rainey-Smith, S.R.; Peiffer, J.J.; Sohrabi, H.R.; Brown, B.M. Relationships between physical activity, sleep and cognitive function: A narrative review. Neurosci. Biobehav. Rev. 2021, 130, 369–378. [Google Scholar] [CrossRef]
- Willems, S.M.; Wright, D.J.; Day, F.R.; Trajanoska, K.; Joshi, P.K.; Morris, J.A.; Matteini, A.M.; Garton, F.C.; Grarup, N.; Oskolkov, N.; et al. Large-scale GWAS identifies multiple loci for hand grip strength providing biological insights into muscular fitness. Nat. Commun. 2017, 8, 16015. [Google Scholar] [CrossRef]
- Leong, D.P.; Teo, K.K.; Rangarajan, S.; Lopez-Jaramillo, P.; Avezum, A., Jr.; Orlandini, A.; Seron, P.; Ahmed, S.H.; Rosengren, A.; Kelishadi, R.; et al. Prognostic value of grip strength: Findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 2015, 386, 266–273. [Google Scholar] [CrossRef]
- Sayer, A.A.; Syddall, H.E.; Martin, H.J.; Dennison, E.M.; Roberts, H.C.; Cooper, C. Is grip strength associated with health-related quality of life? Findings from the Hertfordshire Cohort Study. Age Ageing 2006, 35, 409–415. [Google Scholar] [CrossRef]
- Seidler, R.; Erdeniz, B.; Koppelmans, V.; Hirsiger, S.; Mérillat, S.; Jäncke, L. Associations between age, motor function, and resting state sensorimotor network connectivity in healthy older adults. NeuroImage 2015, 108, 47–59. [Google Scholar] [CrossRef]
- Gonzalez, C.L.R.; Mills, K.J.; Genee, I.; Li, F.; Piquette, N.; Rosen, N.; Gibb, R. Getting the right grasp on executive function. Front. Psychol. 2014, 5, 285. [Google Scholar] [CrossRef] [PubMed]
- Chou, M.-Y.; Nishita, Y.; Nakagawa, T.; Tange, C.; Tomida, M.; Shimokata, H.; Otsuka, R.; Chen, L.-K.; Arai, H. Role of gait speed and grip strength in predicting 10-year cognitive decline among community-dwelling older people. BMC Geriatr. 2019, 19, 186. [Google Scholar] [CrossRef] [PubMed]
- Jiang, R.; Westwater, M.L.; Noble, S.; Rosenblatt, M.; Dai, W.; Qi, S.; Sui, J.; Calhoun, V.D.; Scheinost, D. Associations between grip strength, brain structure, and mental health in >40,000 participants from the UK Biobank. BMC Med. 2022, 20, 286. [Google Scholar] [CrossRef] [PubMed]
- Sterling, D.A.; O’Connor, J.; Bonadies, J. Geriatric Falls: Injury Severity Is High and Disproportionate to Mechanism. J. Trauma: Inj. Infect. Crit. Care 2001, 50, 116–119. [Google Scholar] [CrossRef] [PubMed]
- Niino, N.; Tsuzuku, S.; Ando, F.; Shimokata, H. Frequencies and circumstances of falls in the National Institute for Longevity Sciences, Longitudinal Study of Aging. J. Epidemiol. 2000, 10, 90–94. [Google Scholar] [CrossRef] [PubMed]
- DeVita, P.; Hortobagyi, T.; Allen, J.L.; Franz, J.R.; Mani, D.; Almuklass, A.M.; Hamilton, L.D.; Vieira, T.M.; Botter, A.; Enoka, R.M.; et al. Age causes a redistribution of joint torques and powers during gait. J. Appl. Physiol. 1985, 88, 1804–1811. [Google Scholar] [CrossRef] [PubMed]
- Kerrigan, D.; Lee, L.W.; Collins, J.J.; Riley, P.O.; Lipsitz, L.A. Reduced hip extension during walking: Healthy elderly and fallers versus young adults. Arch. Phys. Med. Rehabil. 2001, 82, 26–30. [Google Scholar] [CrossRef]
- Quan, M.; Xun, P.; Chen, C.; Wen, J.; Wang, Y.; Wang, R.; Chen, P.; He, K. Walking Pace and the Risk of Cognitive Decline and Dementia in Elderly Populations: A Meta-analysis of Prospective Cohort Studies. J. Gerontol. A Biol. Sci. Med. Sci. 2016, 72, 266–270. [Google Scholar] [CrossRef]
- Latimer, C.S.; Searcy, J.L.; Bridges, M.T.; Brewer, L.D.; Popović, J.; Blalock, E.M.; Landfield, P.W.; Thibault, O.; Porter, N.M. Reversal of Glial and Neurovascular Markers of Unhealthy Brain Aging by Exercise in Middle-Aged Female Mice. PLoS ONE 2011, 6, e26812. [Google Scholar] [CrossRef]
- Nishijima, T.; Llorens-Martín, M.; Tejeda, G.S.; Inoue, K.; Yamamura, Y.; Soya, H.; Trejo, J.L.; Torres-Alemán, I. Cessation of voluntary wheel running increases anxiety-like behavior and impairs adult hippocampal neurogenesis in mice. Behav. Brain Res. 2013, 245, 34–41. [Google Scholar] [CrossRef]
- Mitnitski, A.; Howlett, S.E.; Rockwood, K. Heterogeneity of Human Aging and Its Assessment. J. Gerontol. A Biol. Sci. Med. Sci. 2016, 72, 877–884. [Google Scholar] [CrossRef] [PubMed]
- Ferrucci, L.; Kuchel, G.A. Heterogeneity of Aging: Individual Risk Factors, Mechanisms, Patient Priorities, and Outcomes. J. Am. Geriatr. Soc. 2021, 69, 610–612. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Sun, S.; Kang, W.; Wu, S.; Lin, L. A review of neuroimaging-based data-driven approach for Alzheimer’s disease heterogeneity analysis. Rev. Neurosci. 2023, in press. [Google Scholar] [CrossRef] [PubMed]
IC | Resting-State Network | IC | Resting-State Network |
---|---|---|---|
1 | Anterior default mode network | 12 | Sensorimotor network 3 |
2 | Lateral visual network | 13 | Left cingulo-opercular network |
3 | Sensorimotor network | 14 | Anterior default mode network 2 |
4 | Medial visual network | 15 | Cerebellar network |
5 | Right frontoparietal network | 16 | Executive control network |
6 | Left frontoparietal network | 17 | Auditory network 2 |
7 | Posterior default mode network 2 | 18 | Basal ganglia network |
8 | Medial visual network 2 | 19 | Lateral visual network 2 |
9 | Posterior default mode network | 20 | Precuneus/pcc default mode network |
10 | Sensorimotor network 2 | 21 | Right cingulo-opercular network |
11 | Auditory network |
Testing | Description | Cognitive Domain | UKB ID |
---|---|---|---|
Pair-matching | Number of incorrect matches made in round | Visual declarative memory | 399 |
Numeric memory | Maximum number of digits remembered correctly | Working memory | 4282 |
Fluid intelligence | Fluid intelligence score assessment | Verbal and numerical reasoning | 20016 |
Paired associate learning | Number of correctly associated word pairs | Verbal declarative memory | 20197 |
Matrix pattern completion | Number of correctly solved puzzles | Non-verbal reasoning | 6373 |
Reaction time | Mean time taken to correctly identify matches | Processing speed | 20023 |
Symbol digit substitution | Number of correct symbol digit matches made | Processing speed | 23324 |
Tower rearranging | Number of correctly solved puzzles | Executive function | 21004 |
Trail-making | Duration needed to complete an alphanumeric path | Executive function | 6350 |
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Xu, X.; Lin, L.; Wu, S.; Sun, S. Exploring Successful Cognitive Aging: Insights Regarding Brain Structure, Function, and Demographics. Brain Sci. 2023, 13, 1651. https://doi.org/10.3390/brainsci13121651
Xu X, Lin L, Wu S, Sun S. Exploring Successful Cognitive Aging: Insights Regarding Brain Structure, Function, and Demographics. Brain Sciences. 2023; 13(12):1651. https://doi.org/10.3390/brainsci13121651
Chicago/Turabian StyleXu, Xinze, Lan Lin, Shuicai Wu, and Shen Sun. 2023. "Exploring Successful Cognitive Aging: Insights Regarding Brain Structure, Function, and Demographics" Brain Sciences 13, no. 12: 1651. https://doi.org/10.3390/brainsci13121651