Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-02T20:29:47.594Z Has data issue: false hasContentIssue false
  • English
  • Français

Quantifying Cognitive Reserve in Older Adults by Decomposing Episodic Memory Variance: Replication and Extension

Published online by Cambridge University Press:  18 July 2013

Laura B. Zahodne ,
Jennifer J. Manly ,
Adam M. Brickman ,
Karen L. Siedlecki ,
Charles DeCarli  and
Yaakov Stern
Laura B. Zahodne
Affiliation:
Cognitive Neuroscience Division, Department of Neurology and Taub Institute for Research on Alzheimer's Disease and The Aging Brain, Columbia University College of Physicians and Surgeons, New York, New York
Jennifer J. Manly
Affiliation:
Cognitive Neuroscience Division, Department of Neurology and Taub Institute for Research on Alzheimer's Disease and The Aging Brain, Columbia University College of Physicians and Surgeons, New York, New York
Adam M. Brickman
Affiliation:
Cognitive Neuroscience Division, Department of Neurology and Taub Institute for Research on Alzheimer's Disease and The Aging Brain, Columbia University College of Physicians and Surgeons, New York, New York
Karen L. Siedlecki
Affiliation:
Department of Psychology, Fordham University, New York, New York
Charles DeCarli
Affiliation:
Department of Neurology, School of Medicine, University of California, Davis, California
Yaakov Stern*
Affiliation:
Cognitive Neuroscience Division, Department of Neurology and Taub Institute for Research on Alzheimer's Disease and The Aging Brain, Columbia University College of Physicians and Surgeons, New York, New York
*
Correspondence and reprint requests to: Yaakov Stern, Columbia University, Sergievsky Center/Taub Institute, 630 168th Street, P & S Box 16, New York, NY 10032. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The theory of cognitive reserve attempts to explain why some individuals are more resilient to age-related brain pathology. Efforts to explore reserve have been hindered by measurement difficulties. Reed et al. (2010) proposed quantifying reserve as residual variance in episodic memory performance that remains after accounting for demographic factors and brain pathology (whole brain, hippocampal, and white matter hyperintensity volumes). This residual variance represents the discrepancy between an individual's predicted and actual memory performance. The goals of the present study were to extend these methods to a larger, community-based sample and to investigate whether the residual reserve variable is explained by age, predicts longitudinal changes in language, and predicts dementia conversion independent of age. Results support this operational measure of reserve. The residual reserve variable was associated with higher reading ability, lower likelihood of meeting criteria for mild cognitive impairment, lower odds of dementia conversion independent of age, and less decline in language abilities over 3 years. Finally, the residual reserve variable moderated the negative impact of memory variance explained by brain pathology on language decline. This method has the potential to facilitate research on the mechanisms of cognitive reserve and the efficacy of interventions designed to impart reserve. (JINS, 2013, 19, 1–9)

Keywords

CognitionAgingMild cognitive impairmentDementiaStatistical modelsMagnetic resonance imaging
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 8 , September 2013 , pp. 854 - 862
Copyright
Copyright © The International Neuropsychological Society 2013 

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

American Psychiatric Association. (1987). Diagnostic and statistical manual of mental disorders, revised third edition. Washington, DC: American Psychiatric Association.Google Scholar
Bezzola, L., Mérillat, S., Gaser, C., Jäncke, L. (2011). Training-induced neural plasticity in golf novices. Journal of Neuroscience, 31, 12444–12448.CrossRefGoogle ScholarPubMed
Borenstein, A.R., Copenhaver, C.I., Mortimer, J.A. (2006). Early-life risk factors for Alzheimer disease. Alzheimer Disease and Associated Disorders, 20, 63–72.CrossRefGoogle ScholarPubMed
Brickman, A.M., Schupf, N., Manly, J.J., Luchsinger, J.A., Andrews, H., Tang, M.X., Brown, T.R. (2008). Brain morphology in older African Americans, Caribbean Hispanics, and whites from northern Manhattan. Archives of Neurology, 65, 1053–1061.CrossRefGoogle ScholarPubMed
Buschke, H., Fuld, P.A. (1974). Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology, 24, 1010–1025.CrossRefGoogle ScholarPubMed
Cosentino, S., Manly, J., Mungas, D. (2007). Do reading tests measure the same construct in multiethnic and multilingual older persons? Journal of the International Neuropsychological Society, 13, 228–236.CrossRefGoogle ScholarPubMed
Crane, P.K., Narasimhalu, K., Gibbons, L.E., Pedraza, O., Mehta, K.M., Tang, Y., Mungas, D.M. (2008). Composite scores for executive function items: Demographic heterogeneity and relationships with quantitative MRI. Journal of the International Neuropsychological Society, 14, 746–759.CrossRefGoogle Scholar
DeCarli, C., Grady, C.L., Clark, C.M., Katz, D.A., Brady, D.R., Murphy, D.G.M., Rapoport, S.I. (1996). Comparison of positron emission tomography, cognition, and brain volume in Alzheimer's disease with and without severe abnormalities of white matter. Journal of Neurology, Neurosurgery, and Psychiatry, 60, 158–167.CrossRefGoogle ScholarPubMed
DeCarli, C., Maisog, J., Murphy, D.G., Teichberg, D., Rapoport, S.I., Horwitz, B. (1992). Method for quantification of brain, ventricular, and subarachnoid CSF volumes from MR images. Journal of Computer Assisted Tomography, 16, 274–284.CrossRefGoogle ScholarPubMed
DeCarli, C., Murphy, D.G.M., Tranh, M., Brady, C.L., Haxby, J.V., Gillette, J.A., Rapoport, S.I. (1995). The effect of white matter hyperintensity volume on brain structure, cognitive performance, and cerebral metabolism of glucose in 51 healthy adults. Neurology, 45, 2077–2084.CrossRefGoogle ScholarPubMed
Del Ser, T., Gonzalez Montalvo, J.I., Martinez Espinosa, S., Delgado Villapalos, C., Bermejo, F. (1997). Estimation of premorbid intelligence in Spanish people with the Word Accentuation Test and its application to the diagnosis of dementia. Brain and Cognition, 33, 343–356.CrossRefGoogle Scholar
Engvig, A., Fjell, A.M., Westlye, L.T., Moberget, T., Sundseth, Ø., Larsen, V.A., Walhovd, K.B. (2010). Effects of memory training on cortical thickness in the elderly. Neuroimage, 52, 1667–1676.CrossRefGoogle ScholarPubMed
Engvig, A., Fjell, A.M., Westlye, L.T., Moberget, T., Sundseth, Ø., Larsen, V.A., Walhovd, K.B. (2012). Memory training impacts short-term changes in aging white matter: A longitudinal diffusion tensor imaging study. Human Brain Mapping, 33, 2390–2406.CrossRefGoogle ScholarPubMed
Goodglass, H., Kaplan, E. (1983). The assessment of aphasia and related disorders. Philadelphia: Lea & Febiger.Google Scholar
Hall, C.B., Derby, C., LeValley, A., Katz, M.J., Verghese, J., Lipton, R.B. (2007). Education delays accelerated decline on a memory test in persons who develop dementia. Neurology, 69, 1657–1664.CrossRefGoogle ScholarPubMed
Jones, R.N. (2003). Racial bias in the assessment of cognitive functioning of older adults. Aging and Mental Health, 7, 83–102.CrossRefGoogle ScholarPubMed
Jones, R.N., Manly, J., Glymour, M.M., Rentz, D.M., Jefferson, A.L., Stern, Y. (2011). Conceptual and measurement challenges in reserve on cognitive reserve. Journal of the International Neuropsychological Society, 17, 593–601.CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., Weintraub, S. (1983). Boston Naming Test. Philadelphia: Lea & Febiger.Google Scholar
Lövdén, M., Bodammer, N.C., Kühn, S., Kaufmann, J., Schütze, H., Tempelmann, C., Lindenberger, U. (2010). Experience-dependent plasticity of white-matter microstructure extends into old age. Neuropsychologia, 48, 3878–3883.CrossRefGoogle ScholarPubMed
Manly, J.J., Bell-McGinty, S., Tang, M.X., Schupf, N., Stern, Y., Mayeux, R. (2005). Implementing diagnostic criteria and estimating frequency of mild cognitive impairment in an urban community. Archives of Neurology, 62, 1739–1746.CrossRefGoogle Scholar
Manly, J.J., Jacobs, D.S.M., Touradji, P., Small, S.A., Stern, Y. (2002). Reading level attenuates differences in neuropsychological test performance between African American and White elders. Journal of the International Neuropsychological Society, 8, 341–384.CrossRefGoogle ScholarPubMed
Manly, J.J., Tang, M.X., Schupf, N., Stern, Y., Vonsattel, J.P., Mayeux, R. (2008). Frequency and course of mild cognitive impairment in a multiethnic community. Annals of Neurology, 63, 494–506.CrossRefGoogle Scholar
Muthén, L.K., Muthén, B.O. (1998–2011). Mplus User's Guide. Sixth Edition. Los Angeles, CA: Muthén & Muthén.Google Scholar
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E. (1984). Clinical diagnosis of Alzheimer's disease: Report of the NINCDSADRDA work group under the auspices of the Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology, 34, 939–944.CrossRefGoogle ScholarPubMed
Obrist, W.D., Thompson, H.K. Jr., Wang, H.S., Wilkinson, W.E. (1975). Regional cerebral blood flow estimated by 133-xenon inhalation. Stroke, 6, 245–256.CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.CrossRefGoogle ScholarPubMed
Reed, B.R., Dowling, M., Farias, S.T., Sonnen, J., Strauss, M., Schneider, J.A., Mungas, D. (2011). Cognitive activities during adulthood are more important than education in building reserve. Journal of the International Neuropsychological Society, 17, 615–624.CrossRefGoogle ScholarPubMed
Reed, B.R., Mungas, D., Farias, S.T., Harvey, D., Beckett, L., Widaman, K., DeCarli, C. (2010). Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain, 133, 2196–2209.CrossRefGoogle ScholarPubMed
Satz, P., Cole, M.A., Hardy, D.J., Rassovsky, Y. (2011). Brain and cognitive reserve: Mediator(s) and construct validity, a critique. Journal of Clinical and Experimental Neuropsychology, 33, 121–130.CrossRefGoogle Scholar
Scarmeas, N., Levy, G., Tang, M.X., Manly, J., Stern, Y. (2001). Influence of leisure activity on the incidence of Alzheimer's disease. Neurology, 57, 2236–2242.CrossRefGoogle ScholarPubMed
Scarmeas, N., Zarahn, E., Anderson, K.E., Habeck, C.G., Hilton, J., Flynn, J., Stern, Y. (2003). Association of life activities with cerebral blood flow in Alzheimer disease: Implications for the cognitive reserve hypothesis. Archives of Neurology, 60, 359–365.CrossRefGoogle ScholarPubMed
Schlegel, A.A., Rudelson, J.J., Tse, P.U. (2012). White matter structure changes as adults learn a second language. Journal of Cognitive Neuroscience, 24, 1664–1670.CrossRefGoogle Scholar
Siedlecki, K.L., Manly, J.J., Brickman, A.M., Schupf, N., Tang, M.X., Stern, Y. (2010). Do neuropsychological tests have the same meaning in Spanish speakers as they do in English speakers? Neuropsychology, 24, 402–411.CrossRefGoogle ScholarPubMed
Siedlecki, K.L., Stern, Y., Reuben, A., Sacco, R.L., Elkind, M.S., Wright, C.B. (2009). Construct validity of cognitive reserve in a multiethnic cohort: The Northern Manhattan Study. Journal of the International Neuropsychological Society, 15, 558–569.CrossRefGoogle Scholar
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the Neuropsychological Society, 8, 448–460.CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47, 2015–2028.CrossRefGoogle ScholarPubMed
Stern, Y., Alexander, G.E., Prohovnik, I., Mayeux, R. (1992). Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer's disease. Annals of Neurology, 32, 371–375.CrossRefGoogle ScholarPubMed
Stern, Y., Alexander, G.E., Prohovnik, I., Stricks, L., Link, B., Lenon, M.C., Mayeux, R. (1995). Relationship between lifetime occupation and parietal flow: Implications for a reserve against Alzheimer's disease pathology. Neurology, 45, 55–60.CrossRefGoogle ScholarPubMed
Stern, Y., Andrews, H., Pittman, J., Sano, M., Tatemichi, T., Lantigua, R., Mayeux, R. (1992). Diagnosis of dementia in a heterogeneous population. Development of a neuropsychological paradigm-based diagnosis of dementia and quantified correction for the effects of education. Archives of Neurology, 49, 453–460.CrossRefGoogle Scholar
Stern, Y., Gurland, B., Tatemichi, T.K., Tang, M.X., Wilder, D., Mayeux, R. (1994). Influence of education and occupation on the incidence of Alzheimer's disease. Journal of the American Medical Society, 271, 1004–1010.Google ScholarPubMed
Stern, Y., Habeck, C., Moeller, J., Scarmeas, N., Anderson, K.E., Hilton, H.J., van Heertum, R. (2005). Brain networks associated with cognitive reserve in healthy young and old adults. Cerebral Cortex, 15, 394–402.CrossRefGoogle ScholarPubMed
Stern, Y., Zarahn, E., Habeck, C., Holtzer, R., Rakitin, B.C., Kumar, A., Brown, T. (2008). A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cerebral Cortex, 18, 959–967.CrossRefGoogle Scholar
Takeuchi, H., Sekiguchi, A., Taki, Y., Tokoyama, S., Yomogida, Y., Komuro, N., Kawashima, R. (2010). Training of working memory impacts structural connectivity. Journal of Neuroscience, 30, 3297–3303.CrossRefGoogle ScholarPubMed
Tang, M.X., Cross, P., Andrews, H., Jacobs, D.M., Small, S., Bell, K., Mayeux, R. (2001). Incidence of AD in African-Americans, Caribbean Hispanics, and Caucasians in northern Manhattan. Neurology, 56, 49–56.CrossRefGoogle ScholarPubMed
Van Petten, C. (2004). Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: Review and meta-analysis. Neuropsychologia, 42, 1394–1413.CrossRefGoogle ScholarPubMed
Wechsler, D. (1987). Wechsler Adult Intelligence Scale—revised. San Antonio: The Psychological Corporation.Google Scholar
Wilkinson, G.S. (1993). Wide Range Achievement Test 3—administration manual. Wilmington: Jastak Associates, Inc.Google Scholar