Understanding brain resilience in superagers: a systematic review

Godoy, Laiz Laura de; Alves, César Augusto Pinheiro Ferreira; Martín-Saavedra, Juan Sebastián; Neto, Adalberto Studart; Nitrini, Ricardo; Leite, Claudia da Costa; Bisdas, Sotirios

doi:10.1007/s00234-020-02562-1

Cited by 36 publications

(36 citation statements)

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“…Associations of decreased gray matter volume in temporal, frontal, and parietal regions with progression to dementia have been demonstrated in individuals without A β 51,52 . Selective sparing of these cortical regions, most notably the anterior cingulate cortex and medial temporal lobe, is frequently reported in superagers compared to age‐matched controls and has been associated with resilience to cognitive decline 53–55 . Whether the oldest‐old with good cognitive health in the present study are protected by relatively preserved cortical regions is unknown from the present analyses without a control group, however the anterior cingulate and medial temporal thickness were still negatively associated with cognition.…”

Section: Discussionmentioning

confidence: 55%

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Pelkmans

Legdeur

Kate

et al. 2021

Ann Clin Transl Neurol

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Objective To investigate the relationship between amyloid‐β (Aβ) deposition and markers of brain structure on cognitive decline in oldest‐old individuals with initial normal cognition. Methods We studied cognitive functioning in four domains at baseline and change over time in fifty‐seven cognitively intact individuals from the EMIF‐AD 90+ study. Predictors were Aβ status determined by [18F]‐flutemetamol PET (normal = Aβ − vs. abnormal = Aβ+), cortical thickness in 34 regions and hippocampal volume. Mediation analyses were performed to test whether effects of Aβ on cognitive decline were mediated by atrophy of specific anatomical brain areas. Results Subjects had a mean age of 92.7 ± 2.9 years, of whom 19 (33%) were Aβ+. Compared to Aβ−, Aβ+ individuals showed steeper decline on memory (β ± SE = −0.26 ± 0.09), and processing speed (β ± SE = −0.18 ± 0.08) performance over 1.5 years (P < 0.05). Furthermore, medial and lateral temporal lobe atrophy was associated with steeper decline in memory and language across individuals. Mediation analyses revealed that part of the memory decline observed in Aβ+ individuals was mediated through parahippocampal atrophy. Interpretation These results show that Aβ abnormality even in the oldest old with initially normal cognition is not part of normal aging, but is associated with a decline in cognitive functioning. Other pathologies may also contribute to decline in the oldest old as cortical thickness predicted cognitive decline similarly in individuals with and without Aβ pathology.

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Section: Discussionmentioning

confidence: 55%

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Pelkmans

Legdeur

Kate

et al. 2021

Ann Clin Transl Neurol

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“…Complementing these determinants are the constructs of brain reserve (corresponding to structure) (Coffey et al, 1999 ) and cognitive reserve (corresponding to function) (Stern, 2002 ), whose presence (or lack thereof) could maintain (or negatively affect) cognitive performance. For example, older individuals could be (a) super agers, with high reserve and preserved brain structure and function, showing preserved cognition (de Godoy et al, 2020 ); (b) normal agers, with altered brain structure and function, showing gradual cognitive decline; or (c) poor agers, with low reserve and significantly altered brain structure and function and significant cognitive decline (Solé-Padullés et al, 2009 ). Altogether, a balance among structure, function and reserve most likely regulates an individual's ability to compensate in the face of pathology.…”

Section: Discussionmentioning

confidence: 99%

Functional Connectivity and Compensation of Phonemic Fluency in Aging

Mohanty

Gonzalez-Burgos

Díaz‐Flores

et al. 2021

Front. Aging Neurosci.

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Neural compensatory mechanisms associated with broad cognitive abilities have been studied. However, those associated with specific cognitive subdomains (e.g., verbal fluency) remain to be investigated in healthy aging. Here, we delineate: (a) neural substrates of verbal (phonemic) fluency, and (b) compensatory mechanisms mediating the association between these neural substrates and phonemic fluency. We analyzed resting-state functional magnetic resonance imaging from 133 right-handed, cognitively normal individuals who underwent the Controlled Oral Word Association Test (COWAT) to record their phonemic fluency. We evaluated functional connectivity in an established and extended language network comprising Wernicke, Broca, thalamic and anti-correlated modules. (a) We conducted voxel-wise multiple linear regression to identify the brain areas associated with phonemic fluency. (b) We used mediation effects of cognitive reserve, measured by the Wechsler Adult Intelligence Scale—Information subtest, upon the association between functional connectivity and phonemic fluency tested to investigate compensation. We found that: (a) Greater functional connectivity between the Wernicke module and brain areas within the anti-correlated module was associated with better performance in phonemic fluency, (b) Cognitive reserve was an unlikely mediator in younger adults. In contrast, cognitive reserve was a partial mediator of the association between functional connectivity and phonemic fluency in older adults, likely representing compensation to counter the effect of aging. We conclude that in healthy aging, higher performance in phonemic fluency at older ages could be attributed to greater functional connectivity partially facilitated by higher cognitive reserve, presumably reflecting compensatory mechanisms to minimize the effect of aging.

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“…First, 3D volumetric T1weighted images were acquired (TR ¼7.7 ms; TE ¼ 3.1 ms; TI ¼ 600ms; in-plane resolution ¼ 0.5 Â 0.5 mm; 2 section thickness ¼ 1mm, isotropic) and were used for 1 H-MR spectroscopy voxel placement and to enable subsequent voxel segmentation to address the partial volume averaging. 1 H-MR spectroscopy data were acquired with a single-voxel point-resolved spectroscopy sequence, with a bandwidth of 5000 Hz. The standardized VOI measuring 20 Â 20 Â 20 mm 3 was always positioned on the posterior cingulate cortex as shown in Fig 1.…”

Section: Mr Imagingmentioning

confidence: 99%

“…the complex phenomenon of superior cognitive performance in older adults. 1 Subjects exhibiting this outstanding phenotype are newly described as "superagers" 2 and have been studied by imaging, through structural 3 and functional MR imaging. 4 To date, it is known that superagers show selective cortical preservation involving regions of the default mode and salience networks, which also exhibit strong functional connectivity.…”

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confidence: 99%

“…4 To date, it is known that superagers show selective cortical preservation involving regions of the default mode and salience networks, which also exhibit strong functional connectivity. 5 There is a paucity of data, in particular generated by 1 H-MRS, related to the metabolic profile of the brains of superagers. 6 Previous studies have reported the correlation between 1 H-MR spectroscopy parameters of metabolite concentration with measures of intelligence, [7][8][9] affect, 10 creativity, 11 and personality 12 in cohorts of healthy human individuals, mostly younger adults.…”

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confidence: 99%

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The Brain Metabolic Signature in Superagers Using In Vivo ¹H-MRS: A Pilot Study

Godoy

Neto

Wylezinska-Arridge

et al. 2021

AJNR Am J Neuroradiol

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BACKGROUND AND PURPOSE: Youthful memory performance in older adults may reflect an underlying resilience to the conventional pathways of aging. Subjects having this unusual characteristic have been recently termed "superagers." This study aimed to explore the significance of imaging biomarkers acquired by 1 H-MRS to characterize superagers and to differentiate them from their normal-aging peers.MATERIALS AND METHODS: Fifty-five patients older than 80 years of age were screened using a detailed neuropsychological protocol, and 25 participants, comprising 12 superagers and 13 age-matched controls, were statistically analyzed. We used state-of-theart 3T 1 H-MR spectroscopy to quantify 18 neurochemicals in the posterior cingulate cortex of our subjects. All 1 H-MR spectroscopy data were analyzed using LCModel. Results were further processed using 2 approaches to investigate the technique accuracy: 1) comparison of the average concentration of metabolites estimated with Cramer-Rao lower bounds ,20%; and 2) calculation and comparison of the weighted means of metabolites' concentrations. RESULTS:The main finding observed was a higher total N-acetyl aspartate concentration in superagers than in age-matched controls using both approaches (P ¼ .02 and P ¼ .03 for the weighted means), reflecting a positive association of total N-acetyl aspartate with higher cognitive performance.CONCLUSIONS: 1 H-MR spectroscopy emerges as a promising technique to unravel neurochemical mechanisms related to cognitive aging in vivo and providing a brain metabolic signature in superagers. This may contribute to monitoring future interventional therapies to avoid or postpone the pathologic processes of aging.

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Understanding brain resilience in superagers: a systematic review

Cited by 36 publications

References 50 publications

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Functional Connectivity and Compensation of Phonemic Fluency in Aging

The Brain Metabolic Signature in Superagers Using In Vivo ¹H-MRS: A Pilot Study

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Understanding brain resilience in superagers: a systematic review

Cited by 36 publications

References 50 publications

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Amyloid‐β, cortical thickness, and subsequent cognitive decline in cognitively normal oldest‐old

Functional Connectivity and Compensation of Phonemic Fluency in Aging

The Brain Metabolic Signature in Superagers Using In Vivo 1H-MRS: A Pilot Study

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Product

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The Brain Metabolic Signature in Superagers Using In Vivo ¹H-MRS: A Pilot Study