Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-19T07:13:32.006Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurobiological findings associated with high cognitive performance in older adults: a systematic review

Published online by Cambridge University Press:  18 April 2018

Wyllians Vendramini Borelli Open the ORCID record for Wyllians Vendramini Borelli [Opens in a new window] ,
Lucas Porcello Schilling ,
Graciane Radaelli ,
Luciana Borges Ferreira ,
Leonardo Pisani ,
Mirna Wetters Portuguez  and
Jaderson Costa da Costa
Wyllians Vendramini Borelli
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Lucas Porcello Schilling
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Graciane Radaelli
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Luciana Borges Ferreira
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Leonardo Pisani
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Mirna Wetters Portuguez
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
Jaderson Costa da Costa*
Affiliation:
Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Porto Alegre, Brazil
*
Correspondence should be addressed to: Jaderson Costa da Costa, MD, Ph.D., Brain Institute of Rio Grande do Sul (BraIns), Pontifical Catholic University of Rio Grande do Sul, Av. Ipiranga, 6690, Porto Alegre, RS, 90610-000, Brazil. Phone: 5551 3320 5959. Email: [email protected].
Get access

Abstract

Objectives:

to perform a comprehensive literature review of studies on older adults with exceptional cognitive performance.

Design:

We performed a systematic review using two major databases (MEDLINE and Web of Science) from January 2002 to November 2017.

Results:

Quantitative analysis included nine of 4,457 studies and revealed that high-performing older adults have global preservation of the cortex, especially the anterior cingulate region, and hippocampal volumes larger than normal agers. Histological analysis of this group also exhibited decreased amyloid burden and neurofibrillary tangles compared to cognitively normal older controls. High performers that maintained memory ability after three years showed reduced amyloid positron emission tomography at baseline compared with high performers that declined. A single study on blood plasma found a set of 12 metabolites predicting memory maintenance of this group.

Conclusion:

Structural and molecular brain preservation of older adults with high cognitive performance may be associated with brain maintenance. The operationalized definition of high-performing older adults must be carefully addressed using appropriate age cut-off and cognitive evaluation, including memory and non-memory tests. Further studies with a longitudinal approach that include a younger control group are essential.

Keywords

memoryagingmagnetic resonance imaging
Type
Review Article
Information
International Psychogeriatrics , Volume 30 , Issue 12: Issue Theme: Positive Psychiatry , December 2018 , pp. 1813 - 1825
Copyright
Copyright © International Psychogeriatric Association 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ashare, R. L., Ray, R., Lerman, C. and Strasser, A. A. (2012). Cognitive effects of the acetylcholinesterase inhibitor, donepezil, in healthy, non-treatment seeking smokers: a pilot feasibility study. Drug and Alcohol Dependence, 126, 263–267. doi: 10.1016/j.drugalcdep.2012.04.019.Google Scholar
Barulli, D. and Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends in Cognitive Sciences, 17, 502–509. doi: 10.1016/j.tics.2013.08.012.Google Scholar
Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H. and Del Tredici, K. (2006). Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathologica, 112, 389–404. doi: 10.1007/s00401-006-0127-z.Google Scholar
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychology and Aging, 17, 85–100. doi: 10.1037//0882-7974.17.1.85.Google Scholar
Cook Maher, A. et al. (2017). Psychological well-being in elderly adults with extraordinary episodic memory. Plos One, 12, e0186413. doi: 10.1371/journal.pone.0186413.Google Scholar
Cook, A. H. et al. (2017). Rates of cortical atrophy in adults 80 years and older with superior vs average episodic memory. JAMA, 317, 1373. doi: 10.1001/jama.2017.0627.Google Scholar
Cummings, J. L., Morstorf, T. and Zhong, K. (2014). Alzheimer's disease drug-development pipeline: few candidates, frequent failures. Alzheimer's Research & Therapy, 6, 37. doi: 10.1186/alzrt269.Google Scholar
Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S. and Cabeza, R. (2008). Que PASA? The posterior-anterior shift in aging. Cerebral Cortex, 18, 1201–1209. doi: 10.1093/cercor/bhm155.Google Scholar
de Frias, C. M., Lövdén, M., Lindenberger, U. and Nilsson, L.-G. (2007). Revisiting the dedifferentiation hypothesis with longitudinal multi-cohort data. Intelligence, 35, 381–392. doi: 10.1016/j.intell.2006.07.011.Google Scholar
Dekhtyar, M. et al. (2017). Neuroimaging markers associated with maintenance of optimal memory performance in late-life. Neuropsychologia, 100, 164–170. doi: 10.1016/j.neuropsychologia.2017.04.037.Google Scholar
Depp, C. A., Harmell, A. and Vahia, I. V. (2011). Successful cognitive aging. Current Topics in Behavioral Neurosciences, 10, 35–50. doi: 10.1007/7854_2011_158.Google Scholar
Depp, C., Vahia, I. and Jeste, D. (2010). Successful aging: focus on cognitive and emotional health. Annual Review of Clinical Psychology, 6, 527–550.Google Scholar
Eyler, L. T., Sherzai, A., Kaup, A. R. and Jeste, D. V. (2011). A review of functional brain imaging correlates of successful cognitive aging. Biological Psychiatry, 70, 115–122. doi: 10.1016/j.biopsych.2010.12.032.Google Scholar
Gefen, T. et al. (2014). Longitudinal neuropsychological performance of cognitive SuperAgers. Journal of the American Geriatrics Society, 62, 1598–600. doi: 10.1111/jgs.12967.Google Scholar
Gefen, T. et al. (2015). Morphometric and histologic substrates of cingulate integrity in elders with exceptional memory capacity. Journal of Neuroscience, 35, 1781–1791. doi: 10.1523/JNEUROSCI.2998-14.2015.Google Scholar
Habeck, C., Razlighi, Q., Gazes, Y., Barulli, D., Steffener, J. and Stern, Y. (2016). Cognitive reserve and brain maintenance: orthogonal concepts in theory and practice. Cerebral Cortex, 27, 3962–3969. doi: 10.1093/cercor/bhw208.Google Scholar
Harada, C. N., Natelson Love, M. C. and Triebel, K. L. (2013). Normal cognitive aging. Clinics in Geriatric Medicine, 29, 737–752. doi: 10.1016/j.cger.2013.07.002.Google Scholar
Harrison, T. M., Weintraub, S., Mesulam, M.-M. M.-M. and Rogalski, E. (2012). Superior memory and higher cortical volumes in unusually successful cognitive aging. Journal of the International Neuropsychological Society, 18, 1081–1085. doi: 10.1017/S1355617712000847.Google Scholar
Hedden, T. and Gabrieli, J. D. E. (2004). Insights into the ageing mind: a view from cognitive neuroscience. Nature Reviews Neuroscience, 5, 87–96. doi: 10.1038/nrn1323.Google Scholar
Heuninckx, S., Wenderoth, N. and Swinnen, S. P. (2008). Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. Journal of Neuroscience, 28, 91–99. doi: 10.1523/JNEUROSCI.3300-07.2008.Google Scholar
Janeczek, M. et al. (2017). Variations in acetylcholinesterase activity within human cortical pyramidal neurons across age and cognitive trajectories. Cerebral Cortex, 1–9. doi: 10.1093/cercor/bhx047.Google Scholar
Mapstone, M. et al. (2017). What success can teach us about failure: the plasma metabolome of older adults with superior memory and lessons for Alzheimer's disease. Neurobiology of Aging, 51, 148–155. doi: 10.1016/j.neurobiolaging.2016.11.007.Google Scholar
Moher, D., Liberati, A., Tetzlaff, J. and Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ, 339, b2535–b2535. doi: 10.1136/bmj.b2535.Google Scholar
Nikonenko, I., Nikonenko, A., Mendez, P., Michurina, T. V, Enikolopov, G. and Muller, D. (2013). Nitric oxide mediates local activity-dependent excitatory synapse development. Proceedings of the National Academy of Sciences of the United States of America, 110, E4142–E4151. doi: 10.1073/pnas.1311927110.Google Scholar
Nyberg, L., Lövdén, M., Riklund, K., Lindenberger, U. and Bäckman, L. (2012). Memory aging and brain maintenance. Trends in Cognitive Sciences, 16, 292–305. doi: 10.1016/j.tics.2012.04.005.Google Scholar
O'Brien, J. L. et al. (2010). Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology, 74, 1969–1976. doi: 10.1212/WNL.0b013e3181e3966e.Google Scholar
Park, D. C. and Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–196. doi: 10.1146/annurev.psych.59.103006.093656.Google Scholar
Prince, M., Wimo, A., Guerchet, M., Gemma-Claire, A., Wu, Y.-T. and Prina, M. (2015). World Alzheimer Report 2015: The Global Impact of Dementia – An Analysis of Prevalence, Incidence, Cost and Trends. London: Alzheimer's Disease International, 84. doi: 10.1111/j.0963-7214.2004.00293.x.Google Scholar
Riley, K. P., Snowdon, D. A. and Markesbery, W. R. (2002). Alzheimer's neurofibrillary pathology and the spectrum of cognitive function: findings from the nun study. Annals of Neurology, 51, 567–577. doi: 10.1002/ana.10161.Google Scholar
Rogalski, E. J. et al. (2013). Youthful memory capacity in old brains: anatomic and genetic clues from the northwestern superaging project. Journal of Cognitive Neuroscience, 25, 29–36. doi: 10.1162/jocn_a_00300.Google Scholar
Rönnlund, M., Nyberg, L., Bäckman, L. and Nilsson, L.-G. (2005). Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychology and Aging, 20, 3–18. doi: 10.1037/0882-7974.20.1.3.Google Scholar
Salthouse, T. A. (2009). When does age-related cognitive decline begin? Neurobiology of Aging, 30, 507–514. doi: 10.1016/j.neurobiolaging.2008.09.023.Google Scholar
Schaie, K. W. (2005). Developmental Influences on Adult Intelligence: The Seattle Longitudinal Study. New York: Oxford University Press. doi: 10.1093/acprof:oso/9780195156737.001.0001.Google Scholar
Schuman, E. M. and Madison, D. V. (1991). A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science, 254, 1503–1506. Available at: http://www.ncbi.nlm.nih.gov/pubmed/1720572.Google Scholar
Shimizu, E., Tang, Y. P., Rampon, C. and Tsien, J. Z. (2000). NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science, 290, 1170–1174. Available at: http://www.ncbi.nlm.nih.gov/pubmed/11073458.Google Scholar
Stern, Y. (2009). Cognitive reserve☆. Neuropsychologia, 47, 2015–2028. doi: 10.1016/j.neuropsychologia.2009. 03.004.Google Scholar
Sumowski, J. F., Wylie, G. R., DeLuca, J. and Chiaravalloti, N. (2010). Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain, 133, 362–374. doi: 10.1093/brain/awp307.Google Scholar
Sun, F. W., Stepanovic, M. R., Andreano, J., Barrett, L. F., Touroutoglou, A. and Dickerson, B. C. (2016). Youthful brains in older adults: preserved neuroanatomy in the default mode and salience networks contributes to youthful memory in superaging. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 36, 9659–9668. doi: 10.1523/JNEUROSCI.1492-16.2016.Google Scholar