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Comparison of Education and Episodic Memory as Modifiers of Brain Atrophy Effects on Cognitive Decline: Implications for Measuring Cognitive Reserve

Published online by Cambridge University Press:  18 January 2021

Dan Mungas Open the ORCID record for Dan Mungas [Opens in a new window] ,
Evan Fletcher ,
Brandon E. Gavett Open the ORCID record for Brandon E. Gavett [Opens in a new window] ,
Keith Widaman ,
Laura B. Zahodne Open the ORCID record for Laura B. Zahodne [Opens in a new window] ,
Timothy J. Hohman ,
Elizabeth Rose Mayeda ,
N. Maritza Dowling ,
David K. Johnson  and
Sarah Tomaszewski Farias
Dan Mungas*
Affiliation:
Department of Neurology, University of California, Davis, 4860 Y Street, Sacramento, CA95817, USA
Evan Fletcher
Affiliation:
Department of Neurology, University of California, Davis, 1544 Newton Court, Davis, CA95616, USA
Brandon E. Gavett
Affiliation:
Department of Psychology, University of Western Australia, School of Psychological Science (M304), 35 Stirling Hwy, Perth, WA6009, Australia
Keith Widaman
Affiliation:
Graduate School of Education, University of California, Riverside, 1207 Sproul Hall, 900 University Avenue, Riverside, CA92521, USA
Laura B. Zahodne
Affiliation:
Department of Psychology, University of Michigan, 530 Church Street, Ann Arbor, MI48109, Australia
Timothy J. Hohman
Affiliation:
Department of Neurology, Vanderbilt University, Vanderbilt Memory & Alzheimer’s Center, 1207 17th Ave South, Suite 204F, Nashville, TN37212, USA
Elizabeth Rose Mayeda
Affiliation:
Department of Epidemiology, University of California, Los Angeles, UCLA Pub Hlth - Epidemiology, BOX 951772, 46-070B CHS, Los Angeles, CA90095, USA
N. Maritza Dowling
Affiliation:
Department of Acute & Chronic Care, The George Washington School of Nursing, 1919 Pennsylvania Street NW, Suite 500, Washington, DC20006, USA
David K. Johnson
Affiliation:
Department of Neurology, University of California, Davis, 100 N. Wiget Lane, Suite 150, Walnut Creek, CA94598, USA
Sarah Tomaszewski Farias
Affiliation:
Department of Neurology, University of California, Davis, 4860 Y Street, Sacramento, CA95817, USA
*
*Correspondence and reprint requests to: Dan Mungas, Department of Neurology, UC Davis Medical Center, 4860 Y Street, Suite 3900, Sacramento, CA 95817, USA. E-mail: [email protected]
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Abstract

Objective:

This study compared the level of education and tests from multiple cognitive domains as proxies for cognitive reserve.

Method:

The participants were educationally, ethnically, and cognitively diverse older adults enrolled in a longitudinal aging study. We examined independent and interactive effects of education, baseline cognitive scores, and MRI measures of cortical gray matter change on longitudinal cognitive change.

Results:

Baseline episodic memory was related to cognitive decline independent of brain and demographic variables and moderated (weakened) the impact of gray matter change. Education moderated (strengthened) the gray matter change effect. Non-memory cognitive measures did not incrementally explain cognitive decline or moderate gray matter change effects.

Conclusions:

Episodic memory showed strong construct validity as a measure of cognitive reserve. Education effects on cognitive decline were dependent upon the rate of atrophy, indicating education effectively measures cognitive reserve only when atrophy rate is low. Results indicate that episodic memory has clinical utility as a predictor of future cognitive decline and better represents the neural basis of cognitive reserve than other cognitive abilities or static proxies like education.

Keywords

Agingcognitive changeEducationCognitive reserveMRIGray matter changeCognitive declineBrain atrophy
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 5 , May 2021 , pp. 401 - 411
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

Amieva, H., Mokri, H., Le Goff, M., Meillon, C., Jacqmin-Gadda, H., Foubert-Samier, A., … Dartigues, J.F. (2014). Compensatory mechanisms in higher-educated subjects with Alzheimer’s disease: A study of 20 years of cognitive decline. Brain, 137(Pt 4), 1167–1175. https://doi.org/10.1093/brain/awu035 CrossRefGoogle ScholarPubMed
Ashburner, J. & Friston, K.J. (2000). Voxel-based morphometry – The methods. Neuroimage, 11(6 Pt 1), 805–821. https://doi.org/10.1006/nimg.2000.0582 CrossRefGoogle ScholarPubMed
Barulli, D. & Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: Emerging concepts in cognitive reserve. Trends in Cognitive Sciences, 17(10), 502–509. https://doi.org/10.1016/j.tics.2013.08.012 CrossRefGoogle ScholarPubMed
Blom, G. (1958). Statistical Estimates and Transformed Beta-Variables. New York: Wiley.Google Scholar
Brewster, P.W.H., Melrose, R.J., Marquine, M.J., Johnson, J.K., Napoles, A., MacKay-Brandt, A., … Mungas, D. (2014). Life experience and demographic influences on cognitive function in older adults. Neuropsychology, 28(6), 846–858. https://doi.org/10.1037/neu0000098 CrossRefGoogle ScholarPubMed
Carmichael, O., Mungas, D., Beckett, L., Harvey, D., Tomaszewski Farias, S., Reed, B., … Decarli, C. (2012). MRI predictors of cognitive change in a diverse and carefully characterized elderly population. Neurobiology of Aging, 33(1), 83–95. https://doi.org/10.1016/j.neurobiolaging.2010.01.021 CrossRefGoogle Scholar
DeCarli, C., Fletcher, E., Ramey, V., Harvey, D., & Jagust, W. (2005). Anatomical mapping of white matter hyperintensities (WMH) exploring the relationships between periventricular WMH, deep WMH, and total WMH burden. Stroke, 36, 50–55.CrossRefGoogle ScholarPubMed
Dowling, N.M., Tomaszewski Farias, S., Reed, B.R., Sonnen, J.A., Strauss, M.E., Schneider, J.A., … Mungas, D. (2011). Neuropathological associates of multiple cognitive functions in two community-based cohorts of older adults. Journal of the International Neuropsychological Society: JINS, 17(4), 602–614. https://doi.org/10.1017/S1355617710001426 CrossRefGoogle ScholarPubMed
Early, D.R., Widaman, K.F., Harvey, D., Beckett, L., Park, L.Q., Farias, S.T., … Mungas, D. (2013). Demographic predictors of cognitive change in ethnically diverse older persons. Psychology and Aging, 28(3), 633–645. https://doi.org/10.1037/a0031645 CrossRefGoogle ScholarPubMed
Fletcher, E. (2014). Using prior information to enhance sensitivity of longitudinal brain change computation. In Chen, C.H. (Ed.), Frontiers of medical imaging (pp. 63–81). Singapore; Hackensack, NJ: World Scientific.CrossRefGoogle Scholar
Fletcher, E., Carmichael, O., Pasternak, O., Maier-Hein, K.H., & DeCarli, C. (2014). Early brain loss in circuits affected by Alzheimer’s disease is predicted by Fornix microstructure but may be independent of gray matter. Frontiers in Aging Neuroscience, 6, 1–9. https://doi.org/10.3389/fnagi.2014.00106 CrossRefGoogle ScholarPubMed
Fletcher, E., Gavett, B., Harvey, D., Farias, S.T., Olichney, J., Beckett, L., … Mungas, D. (2018). Brain volume change and cognitive trajectories in aging. Neuropsychology, 32(4), 436–449. https://doi.org/10.1037/neu0000447 CrossRefGoogle Scholar
Fletcher, E., Knaack, A., Singh, B., Lloyd, E., Wu, E., Carmichael, O., & DeCarli, C. (2013). Combining boundary-based methods with tensor-based morphometry in the measurement of longitudinal brain change. IEEE Transactions on Medical Imaging, 32(2), 223–236. https://doi.org/10.1109/tmi.2012.2220153 CrossRefGoogle ScholarPubMed
Fletcher, E., Villeneuve, S., Maillard, P., Harvey, D., Reed, B., Jagust, W., & Decarli, C. (2016). Beta-amyloid, hippocampal atrophy and their relation to longitudinal brain change in cognitively normal individuals. Neurobiology of Aging, 40, 173–180. https://doi.org/10.1016/j.neurobiolaging.2016.01.133 CrossRefGoogle ScholarPubMed
Gavett, B.E., Fletcher, E., Harvey, D., Farias, S.T., Olichney, J., Beckett, L., … Mungas, D. (2018). Ethnoracial differences in brain structure change and cognitive change. Neuropsychology, 32(5), 529–540. https://doi.org/10.1037/neu0000452 CrossRefGoogle ScholarPubMed
Gross, A.L., Mungas, D.M., Crane, P.K., Gibbons, L.E., MacKay-Brandt, A., Manly, J.J., … Jones, R.N. (2015). Effects of education and race on cognitive decline: An integrative study of generalizability versus study-specific results. Psychology and Aging, 30(4), 863–880. https://doi.org/10.1037/pag0000032 CrossRefGoogle ScholarPubMed
Hinton, L., Carter, K., Reed, B.R., Beckett, L., Lara, E., DeCarli, C., & Mungas, D. (2010). Recruitment of a community-based cohort for research on diversity and risk of dementia. Alzheimer’s Disease and Associated Disorders, 24(3), 234–241. https://doi.org/10.1097/WAD.0b013e3181c1ee01 CrossRefGoogle ScholarPubMed
Jones, R.N., Manly, J., Glymour, M.M., Rentz, D.M., Jefferson, A.L., & Stern, Y. (2011). Conceptual and measurement challenges in research on cognitive reserve. Journal of the International Neuropsychological Society, 17(4), 593–601. https://doi.org/10.1017/S1355617710001748 CrossRefGoogle ScholarPubMed
Lee, D.Y., Fletcher, E., Martinez, O., Zozulya, N., Kim, J., Tran, J., … DeCarli, C. (2010). Vascular and degenerative processes differentially affect regional interhemispheric connections in normal aging, mild cognitive impairment, and Alzheimer disease. Stroke, 41(8), 1791–1797. https://doi.org/10.1161/STROKEAHA.110.582163 CrossRefGoogle ScholarPubMed
Masel, M.C., & Peek, M.K. (2009). Ethnic differences in cognitive function over time. Annals of Epidemiology, 19(11), 778–783. https://doi.org/10.1016/j.annepidem.2009.06.008 CrossRefGoogle ScholarPubMed
McKenzie, C., Bucks, R.S., Weinborn, M., Bourgeat, P., Salvado, O., & Gavett, B.E. (2020). Cognitive reserve predicts future executive function decline in older adults with Alzheimer’s disease pathology but not age-associated pathology. Neurobiology of Aging, 88, 119–127. https://doi.org/10.1016/j.neurobiolaging.2019.12.022 CrossRefGoogle Scholar
Melrose, R.J., Brewster, P., Marquine, M.J., MacKay-Brandt, A., Reed, B., Farias, S.T., & Mungas, D. (2015). Early life development in a multiethnic sample and the relation to late life cognition. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 70(4), 519–531. https://doi.org/10.1093/geronb/gbt126 CrossRefGoogle Scholar
Mungas, D., Beckett, L., Harvey, D., Farias, S.T., Reed, B., Carmichael, O., … DeCarli, C. (2010). Heterogeneity of cognitive trajectories in diverse older persons. Psychology and Aging, 25(3), 606–619. https://doi.org/10.1037/a0019502 CrossRefGoogle ScholarPubMed
Mungas, D., Early, D.R., Glymour, M.M., Zeki Al Hazzouri, A., & Haan, M.N. (2018). Education, bilingualism, and cognitive trajectories: Sacramento Area Latino Aging Study (SALSA). Neuropsychology, 32(1), 77–88. https://doi.org/10.1037/neu0000356 CrossRefGoogle Scholar
Mungas, D., Gavett, B., Fletcher, E., Farias, S.T., DeCarli, C., & Reed, B. (2018). Education amplifies brain atrophy effect on cognitive decline: Implications for cognitive reserve. Neurobiology of Aging, 68, 142–150. https://doi.org/10.1016/j.neurobiolaging.2018.04.002 CrossRefGoogle ScholarPubMed
Mungas, D., Reed, B.R., Crane, P.K., Haan, M.N., & Gonzalez, H. (2004). Spanish and English Neuropsychological Assessment Scales (SENAS): Further development and psychometric characteristics. Psychological Assessment, 16(4), 347–359. https://doi.org/10.1037/1040-3590.16.4.347 CrossRefGoogle ScholarPubMed
Mungas, D., Reed, B.R., Farias, S.T., & Decarli, C. (2009). Age and education effects on relationships of cognitive test scores with brain structure in demographically diverse older persons. Psychology and Aging, 24(1), 116–128. https://doi.org/10.1037/a0013421 CrossRefGoogle ScholarPubMed
Mungas, D., Reed, B.R., Haan, M.N., & Gonzalez, H. (2005a). Spanish and English Neuropsychological Assessment Scales: Relationship to demographics, language, cognition, and independent function. Neuropsychology, 19(4), 466–475.CrossRefGoogle ScholarPubMed
Mungas, D., Reed, B.R., Marshall, S.C., & Gonzalez, H.M. (2000). Development of psychometrically matched English and Spanish language neuropsychological tests for older persons. Neuropsychology, 14(2), 209–223.CrossRefGoogle ScholarPubMed
Mungas, D., Reed, B.R., Tomaszewski Farias, S., & DeCarli, C. (2005b). Criterion-referenced validity of a neuropsychological test battery: Equivalent performance in elderly Hispanics and Non-Hispanic Whites. Journal of the International Neuropsychological Society, 11, 620–630.CrossRefGoogle ScholarPubMed
Mungas, D., Widaman, K.F., Reed, B.R., & Tomaszewski Farias, S. (2011). Measurement invariance of neuropsychological tests in diverse older persons. Neuropsychology, 25(2), 260–269. https://doi.org/10.1037/a0021090 CrossRefGoogle ScholarPubMed
Muthén, L.K., & Muthén, B.O. (1998). Mplus User’s Guide (8th ed.). Los Angeles, CA: Muthén & Muthén.Google Scholar
Park, D.C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–196. https://doi.org/10.1146/annurev.psych.59.103006.093656 CrossRefGoogle ScholarPubMed
Reed, B.R., Dowling, M., Tomaszewski Farias, S., 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(4), 615–624. https://doi.org/10.1017/S1355617711000014 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(Pt 8), 2196–2209. https://doi.org/10.1093/brain/awq154 CrossRefGoogle ScholarPubMed
Scarmeas, N., Albert, S.M., Manly, J.J., & Stern, Y. (2006). Education and rates of cognitive decline in incident Alzheimer’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 77(3), 308–316.CrossRefGoogle ScholarPubMed
Steffener, J., Barulli, D., Habeck, C., O’Shea, D., Razlighi, Q., & Stern, Y. (2014). The role of education and verbal abilities in altering the effect of age-related gray matter differences on cognition. PloS One, 9(3), e91196. https://doi.org/10.1371/journal.pone.0091196 CrossRefGoogle ScholarPubMed
Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society, 8(3), 448–460.CrossRefGoogle ScholarPubMed
Stern, Y. (2006). Cognitive reserve and Alzheimer disease. Alzheimer’s Disease and Associated Disorders, 20(2), 112–117.CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 2015–2028. https://doi.org/10.1016/j.neuropsychologia.2009.03.004 CrossRefGoogle ScholarPubMed
Stern, Y., Albert, S., Tang, M.X., & Tsai, W.Y. (1999). Rate of memory decline in AD is related to education and occupation: Cognitive reserve? Neurology, 53(9), 1942–1947.CrossRefGoogle ScholarPubMed
Stern, Y., Arenaza-Urquijo, E.M., Bartres-Faz, D., Belleville, S., Cantilon, M., Chetelat, G., … Conceptual Frameworks Workgroup (2018). Whitepaper: Defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimers Dement. https://doi.org/10.1016/j.jalz.2018.07.219 Google Scholar
Ye, B.S., Seo, S.W., Cho, H., Kim, S.Y., Lee, J.S., Kim, E.J., … Na, D.L. (2013). Effects of education on the progression of early- versus late-stage mild cognitive impairment. International Psychogeriatrics, 25(4), 597–606. https://doi.org/10.1017/S1041610212002001 CrossRefGoogle ScholarPubMed
Zahodne, L.B., Manly, J.J., Brickman, A.M., Siedlecki, K.L., Decarli, C., & Stern, Y. (2013). Quantifying cognitive reserve in older adults by decomposing episodic memory variance: Replication and extension. Journal of the International Neuropsychological Society, 19(8), 854–862. https://doi.org/10.1017/S1355617713000738 CrossRefGoogle Scholar
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