Cognitive reserve and lifestyle: Moving towards preclinical Alzheimer's disease

Frontiers in Aging Neuroscience

Volumn 7, Issue JUN, 2015, Pages

  Arenaza Urquijo, Eider M ^a,b,c,d   Wirth, Miranka ^a,b,c,d   Chételat, Gaël ^a,b,c,d  

^a Centre Cyceron   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d CAEN UNIVERSITY HOSPITAL   (France)

Author keywords

Alzheimer's disease; Amyloid; Brain reserve; Cognitive reserve; Compensation; Neuroimaging; Neuroprotection; Preclinical Alzheimer's disease

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN; APOLIPOPROTEIN E;

AGING; ALZHEIMER DISEASE; ARTICLE; BRAIN ATROPHY; BRAIN REGION; BRAIN SIZE; COGNITION; COGNITIVE RESERVE; COMPENSATION; CORTICAL SYNCHRONIZATION; DEMENTIA; DISEASE COURSE; EDUCATIONAL STATUS; EPISODIC MEMORY; FRONTOTEMPORAL DEMENTIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC RISK; GLUCOSE METABOLISM; HUMAN; HUNTINGTON CHOREA; LIFESTYLE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; NEUROPATHOLOGY; NEUROPROTECTION; OCCUPATION; POSTERIOR CINGULATE; POSTSYNAPTIC DENSITY;

EID: 84936108933     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2015.00134     Document Type: Article

References (95)

1. Alexander, G. E., Furey, M. L., Grady, C. L., Pietrini, P., Brady, D. R., Mentis, M. J., and Schapiro, M. B. (1997). Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: implications for the cognitive reserve hypothesis. Am. J. Psychiatry 154, 165-172.
2. Amieva, H., Jacqmin-Gadda, H., Orgogozo, J.-M., Le Carret, N., Helmer, C., Letenneur, L., Barberger-Gateau, P., Fabrigoule, C., and Dartigues, J.-F. (2005). The 9 year cognitive decline before dementia of the Alzheimer type: a prospective population-based study. Brain J. Neurol. 128, 1093-1101.
3. Arenaza-Urquijo, E. M., Landeau, B., La Joie, R., Mevel, K., Mézenge, F., Perrotin, A., Desgranges, B., Bartrés-Faz, D., Eustache, F., and Chételat, G. (2013a). Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. NeuroImage 83, 450-457.
4. Arenaza-Urquijo, E. M., Molinuevo, J.-L., Sala-Llonch, R., Solé-Padullés, C., Balasa, M., Bosch, B., Olives, J., Antonell, A., Lladó, A., Sánchez-Valle, R., et al. (2013b). Cognitive Reserve Proxies Relate to Gray Matter Loss in Cognitively Healthy Elderly with Abnormal Cerebrospinal Fluid Amyloid-β Levels. J. Alzheimers Dis. JAD.
5. Barnes, D. E., and Yaffe, K. (2011). The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol. 10, 819-828. doi:10.1016/S1474- 4422(11)70072-2.
6. Bartrés-Faz, D., and Arenaza-Urquijo, E. M. (2011a). Structural and functional imaging correlates of cognitive and brain reserve hypotheses in healthy and pathological aging. Brain Topogr. 24, 340-357.
7. Bartrés-Faz, D., and Arenaza-Urquijo, E. M. (2011b). Structural and functional imaging correlates of cognitive and brain reserve hypotheses in healthy and pathological aging. Brain Topogr. 24, 340-357.
8. Bartrés-Faz, D., Solé-Padullés, C., Junqué, C., Rami, L., Bosch, B., Bargalló, N., Falcón, C., Sánchez-Valle, R., and Molinuevo, J. L. (2009). Interactions of cognitive reserve with regional brain anatomy and brain function during a working memory task in healthy elders. Biol. Psychol. 80, 256-259.
9. Barulli, D., and Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn. Sci. 17, 502-509.
10. Bastin, C., Yakushev, I., Bahri, M. A., Fellgiebel, A., Eustache, F., Landeau, B., Scheurich, A., Feyers, D., Collette, F., Chételat, G., et al. (2012). Cognitive reserve impacts on inter individual variability in resting-state cerebral metabolism in normal aging. NeuroImage 63, 713-722.
11. Bennett, D. A., Arnold, S. E., Valenzuela, M. J., Brayne, C., and Schneider, J. A. (2014). Cognitive and social lifestyle: links with neuropathology and cognition in late life. Acta Neuropathol. (Berl.) 127, 137-150.
12. Bennett, D. A., Schneider, J. A., Tang, Y., Arnold, S. E., and Wilson, R. S. (2006). The effect of social networks on the relation between Alzheimer's disease pathology and level of cognitive function in old people: a longitudinal cohort study. Lancet Neurol. 5, 406-412.
13. Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Mendes de Leon, C. F., Arnold, S. E., Barnes, L. L., and Bienias, J. L. (2003). Education modifies the relation of AD pathology to level of cognitive function in older persons. Neurology 60, 1909-1915.
14. Biswal B., Yetkin F.Z., Haughton V.M., Hyde, J.S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Mag. Reson. Med., 34. 537-541.
15. Bosch, B., Bartrés-Faz, D., Rami, L., Arenaza-Urquijo, E. M., Fernández-Espejo, D., Junqué, C., Solé-Padullés, C., Sánchez-Valle, R., Bargalló, N., Falcón, C., et al. (2010). Cognitive reserve modulates task-induced activations and deactivations in healthy elders, amnestic mild cognitive impairment and mild Alzheimer's disease. Cortex J. Devoted Study Nerv. Syst. Behav. 46, 451-461.
16. Brown, B. M., Peiffer, J. J., Taddei, K., Lui, J. K., Laws, S. M., Gupta, V. B., Taddei, T., Ward, V. K., Rodrigues, M. A., Burnham, S., et al. (2013). Physical activity and amyloid-β plasma and brain levels: results from the Australian Imaging, Biomarkers and Lifestyle Study of Ageing. Mol. Psychiatry 18, 875-881.
17. Borroni, B., Premi, E., Bozzali, M. and Padovani., A. (2012). Reserve mechanisms in neurodegenerative diseases: from bench to bedside and back again. Curr. Med. Chem. 19, 6112-6118.
18. Bozzali, M., Dowling, C., Serra, L., Spanò, B., Torso, M., Marra, C., Castelli, D., Dowell., N.G., Koch, G., Caltagirone, C., Cercignani, M. (2015). The impact of cognitive reserve on brain functional connectivity in Alzheimer's disease. J Alzheimers Dis. 44, 243-250.
19. Burdette, J. H., Laurienti, P. J., Espeland, M. A., Morgan, A., Telesford, Q., Vechlekar, C. D., Hayasaka, S., Jennings, J. M., Katula, J. A., Kraft, R. A., et al. (2010). Using network science to evaluate exercise-associated brain changes in older adults. Front. Aging Neurosci. 2, 23.
20. Chételat, G., Villemagne, V. L., Pike, K. E., Baron, J.-C., Bourgeat, P., Jones, G., Faux, N. G., Ellis, K. A., Salvado, O., Szoeke, C., et al. (2010). Larger temporal volume in elderly with high versus low beta-amyloid deposition. Brain J. Neurol. 133, 3349-3358.
21. Coffey, C. E., Saxton, J. A., Ratcliff, G., Bryan, R. N., and Lucke, J. F. (1999). Relation of education to brain size in normal aging: implications for the reserve hypothesis. Neurology 53, 189-196.
22. Costa, D. A., Cracchiolo, J. R., Bachstetter, A. D., Hughes, T. F., Bales, K. R., Paul, S. M., Mervis, R. F., Arendash, G. W., and Potter, H. (2007). Enrichment improves cognition in AD mice by amyloid-related and unrelated mechanisms. Neurobiol. Aging 28, 831-844.
23. Elman, J. A., Oh, H., Madison, C. M., Baker, S. L., Vogel, J. W., Marks, S. M., Crowley, S., O'Neil, J. P., and Jagust, W. J. (2014). Neural compensation in older people with brain amyloid-β deposition. Nat. Neurosci. 17, 1316-1318.
24. Erickson, K. I., Voss, M. W., Prakash, R. S., Basak, C., Szabo, A., Chaddock, L., Kim, J. S., Heo, S., Alves, H., White, S. M., et al. (2011). Exercise training increases size of hippocampus and improves memory. Proc. Natl. Acad. Sci. U. S. A. 108, 3017-3022.
25. Erickson, K. I., Weinstein, A. M., and Lopez, O. L. (2012). Physical Activity, Brain Plasticity, and Alzheimer's Disease. Arch. Med. Res. doi:10.1016/j.arcmed.2012.09.008.
26. Ewers, M., Insel, P. S., Stern, Y., and Weiner, M. W. (2013). Cognitive reserve associated with FDG-PET in preclinical Alzheimer disease. Neurology 80, 1194-1201.
27. Foubert-Samier, A., Catheline, G., Amieva, H., Dilharreguy, B., Helmer, C., Allard, M., and Dartigues, J.-F. (2012). Education, occupation, leisure activities, and brain reserve: a population-based study. Neurobiol. Aging 33, 423.e15-25.
28. Fratiglioni, L., Wang, H. X., Ericsson, K., Maytan, M., and Winblad, B. (2000). Influence of social network on occurrence of dementia: a community-based longitudinal study. Lancet 355, 1315-1319.
29. Garibotto, V., Borroni, B., Kalbe, E., Herholz, K., Salmon, E., Holtoff, V., Sorbi, S., Cappa, S. F., Padovani, A., Fazio, F., et al. (2008). Education and occupation as proxies for reserve in aMCI converters and AD: FDG-PET evidence. Neurology 71, 1342-1349.
30. Hall, C. B., Derby, C., LeValley, A., Katz, M. J., Verghese, J., and Lipton, R. B. (2007). Education delays accelerated decline on a memory test in persons who develop dementia. Neurology 69, 1657-1664.
31. Hall, C. B., Lipton, R. B., Sliwinski, M., Katz, M. J., Derby, C. A., and Verghese, J. (2009). Cognitive activities delay onset of memory decline in persons who develop dementia. Neurology 73, 356-361.
32. Head, D., Bugg, J. M., Goate, A. M., Fagan, A. M., Mintun, M. A., Benzinger, T., Holtzman, D. M., and Morris, J. C. (2012). Exercise Engagement as a Moderator of the Effects of APOE Genotype on Amyloid Deposition. Arch. Neurol. 69, 636-643.
33. Helzner, E. P., Scarmeas, N., Cosentino, S., Portet, F., and Stern, Y. (2007). Leisure activity and cognitive decline in incident Alzheimer disease. Arch. Neurol. 64, 1749-1754.
34. Huijbers, W., Mormino, E. C., Schultz, A. P., Wigman, S., Ward, A. M., Larvie, M., Amariglio, R. E., Marshall, G. A., Rentz, D. M., Johnson, K. A., et al. (2015). Amyloid-β deposition in mild cognitive impairment is associated with increased hippocampal activity, atrophy and clinical progression. Brain J. Neurol.
35. Jagust, W. J., and Mormino, E. C. (2011). Lifespan brain activity, β-amyloid, and Alzheimer's disease. Trends Cogn. Sci. 15, 520-526.
36. Jolles, D.D., Van Buchem M.A., Crone E.A., and Rombouts S.A. (2013). Functional brain connectivity at rest changes after working memory training. Human Brain Mapp. 34, 396- 406.
37. Johnson, S. C., Christian, B. T., Okonkwo, O. C., Oh, J. M., Harding, S., Xu, G., Hillmer, A. T., Wooten, D. W., Murali, D., Barnhart, T. E., et al. (2014). Amyloid burden and neural function in people at risk for Alzheimer's Disease. Neurobiol. Aging 35, 576-584.
38. Jones, R.N., Manly, J., Glymour, M.M., Rentz, D.M., Jefferson, A.L., and Stern, Y. (2011). Conceptual and measurement challenges in research on cognitive reserve. J. Int. Neuropsychol. Soc. 17, 593-601.
39. Katzman, R. (1993). Education and the prevalence of dementia and Alzheimer's disease. Neurology 43, 13-20.
40. Katzman, R., Aronson, M., Fuld, P., Kawas, C., Brown, T., Morgenstern, H., Frishman, W., Gidez, L., Eder, H., and Ooi, W. L. (1989). Development of dementing illnesses in an 80- year-old volunteer cohort. Ann. Neurol. 25, 317-324.
41. Kemppainen, N. M., Aalto, S., Karrasch, M., Någren, K., Savisto, N., Oikonen, V., Viitanen, M., Parkkola, R., and Rinne, J. O. (2008). Cognitive reserve hypothesis: Pittsburgh Compound B and fluorodeoxyglucose positron emission tomography in relation to education in mild Alzheimer's disease. Ann. Neurol. 63, 112-118.
42. Kidron, D., Black, S. E., Stanchev, P., Buck, B., Szalai, J. P., Parker, J., Szekely, C., and Bronskill, M. J. (1997). Quantitative MR volumetry in Alzheimer's disease. Topographic markers and the effects of sex and education. Neurology 49, 1504-1512.
43. Landau, S. M., Marks, S. M., Mormino, E. C., Rabinovici, G. D., Oh, H., O'Neil, J. P., Wilson, R. S., and Jagust, W. J. (2012). Association of Lifetime Cognitive Engagement and Low β-Amyloid Deposition. Arch. Neurol. 69, 623-629.
44. Lazarov, O., Robinson, J., Tang, Y.-P., Hairston, I. S., Korade-Mirnics, Z., Lee, V. M.-Y., Hersh, L. B., Sapolsky, R. M., Mirnics, K., and Sisodia, S. S. (2005). Environmental enrichment reduces Abeta levels and amyloid deposition in transgenic mice. Cell 120, 701- 713.
45. Liang, K. Y., Mintun, M. A., Fagan, A. M., Goate, A. M., Bugg, J. M., Holtzman, D. M., Morris, J. C., and Head, D. (2010). Exercise and Alzheimer's disease biomarkers in cognitively normal older adults. Ann. Neurol. 68, 311-318.
46. Liao, Y.-C., Liu, R.-S., Teng, E. L., Lee, Y.-C., Wang, P.-N., Lin, K.-N., Chung, C.-P., and Liu, H.-C. (2005). Cognitive reserve: a SPECT study of 132 Alzheimer's disease patients with an education range of 0-19 years. Dement. Geriatr. Cogn. Disord. 20, 8-14.
47. Liu, Y., Julkunen, V., Paajanen, T., Westman, E., Wahlund, L.-O., Aitken, A., Sobow, T., Mecocci, P., Tsolaki, M., Vellas, B., et al. (2012a). Education increases reserve against Alzheimer's disease-evidence from structural MRI analysis. Neuroradiology. 54: 929-938.
48. Liu, Y., Julkunen, V., Paajanen, T., Westman, E., Wahlund, L.-O., Aitken, A., Sobow, T., Mecocci, P., Tsolaki, M., Vellas, B., et al. (2012b). Education increases reserve against Alzheimer's disease--evidence from structural MRI analysis. Neuroradiology 54, 929-938.
49. Lo, R. Y., Jagust, W. J., and Alzheimer's Disease Neuroimaging Initiative (2013). Effect of cognitive reserve markers on Alzheimer pathologic progression. Alzheimer Dis. Assoc. Disord. 27, 343-350.
50. Meng, X., and D'Arcy, C. (2012). Education and dementia in the context of the cognitive reserve hypothesis: a systematic review with meta-analyses and qualitative analyses. PloS One 7, e38268. doi:10.1371/journal.pone.0038268.
51. Mortimer, J. A. (1997). Brain reserve and the clinical expression of Alzheimer's disease. Geriatrics 52 Suppl 2, S50-53.
52. Mortimer, J. A., Borenstein, A. R., Gosche, K. M., and Snowdon, D. A. (2005). Very early detection of Alzheimer neuropathology and the role of brain reserve in modifying its clinical expression. J. Geriatr. Psychiatry Neurol. 18, 218-223.
53. Nyberg, L., Lövdén, M., Riklund, K., Lindenberger, U., and Bäckman, L. (2012). Memory aging and brain maintenance. Trends Cogn. Sci. 16, 292-305.
54. Okonkwo, O. C., Schultz, S. A., Oh, J. M., Larson, J., Edwards, D., Cook, D., Koscik, R., Gallagher, C. L., Dowling, N. M., Carlsson, C. M., et al. (2014). Physical activity attenuates age-related biomarker alterations in preclinical AD. Neurology 83, 1753-1760.
55. Park, D. C., Lautenschlager, G., Hedden, T., Davidson, N. S., Smith, A. D., and Smith, P. K. (2002). Models of visuospatial and verbal memory across the adult life span. Psychol. Aging 17, 299-320.
56. Park, D. C., and Reuter-Lorenz, P. (2009). The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 60, 173-196.
57. Piras, F., Cherubini, A., Caltagirone, C., and Spalletta, G. (2011). Education mediates microstructural changes in bilateral hippocampus. Hum. Brain Mapp. 32, 282-289.
58. Querbes, O., Aubry, F., Pariente, J., Lotterie, J.-A., Démonet, J.-F., Duret, V., Puel, M., Berry, I., Fort, J.-C., and Celsis, P. (2009). Early diagnosis of Alzheimer's disease using cortical thickness: impact of cognitive reserve. Brain J. Neurol. 132, 2036-2047.
59. Rasmusson, D. X., Carson, K. A., Brookmeyer, R., Kawas, C., and Brandt, J. (1996). Predicting rate of cognitive decline in probable Alzheimer's disease. Brain Cogn. 31, 133- 147.
60. Rentz, D. M., Locascio, J. J., Becker, J. A., Moran, E. K., Eng, E., Buckner, R. L., Sperling, R. A., and Johnson, K. A. (2010). Cognition, reserve, and amyloid deposition in normal aging. Ann. Neurol. 67, 353-364.
61. Richards, M., and Deary, I. J. (2005). A life course approach to cognitive reserve: a model for cognitive aging and development? Ann. Neurol. 58, 617-622.
62. Richards, M., and Sacker, A. (2003). Lifetime antecedents of cognitive reserve. J. Clin. Exp. Neuropsychol. 25, 614-624.
63. Roe, C. M., Xiong, C., Miller, J. P., and Morris, J. C. (2007). Education and Alzheimer disease without dementia: support for the cognitive reserve hypothesis. Neurology 68, 223- 228.
64. Satz, P., Cole, M. A., Hardy, D. J., and Rassovsky, Y. (2011). Brain and cognitive reserve: mediator(s) and construct validity, a critique. J. Clin. Exp. Neuropsychol. 33, 121-130.
65. Satz, P., Morgenstern, H., Miller, E. N., Selnes, O. A., McArthur, J. C., Cohen, B. A., Wesch, J., Becker, J. T., Jacobson, L., and D'Elia, L. F. (1993). Low education as a possible risk factor for cognitive abnormalities in HIV-1: findings from the multicenter AIDS Cohort Study (MACS). J. Acquir. Immune Defic. Syndr. 6, 503-511.
66. Scarmeas, N., Levy, G., Tang, M. X., Manly, J., and Stern, Y. (2001). Influence of leisure activity on the incidence of Alzheimer's disease. Neurology 57, 2236-2242.
67. Scarmeas, N., Stern, Y., Tang, M.-X., Mayeux, R., and Luchsinger, J. A. (2006). Mediterranean diet and risk for Alzheimer's disease. Ann. Neurol. 59, 912-921.
68. Scarmeas, N., Zarahn, E., Anderson, K. E., Habeck, C. G., Hilton, J., Flynn, J., Marder, K. S., Bell, K. L., Sackeim, H. A., Van Heertum, R. L., et al. (2003a). Association of life activities with cerebral blood flow in Alzheimer disease: implications for the cognitive reserve hypothesis. Arch. Neurol. 60, 359-365.
69. Scarmeas, N., Zarahn, E., Anderson, K. E., Hilton, J., Flynn, J., Van Heertum, R. L., Sackeim, H. A., and Stern, Y. (2003b). Cognitive reserve modulates functional brain responses during memory tasks: a PET study in healthy young and elderly subjects. NeuroImage 19, 1215-1227.
70. Scarmeas, N., Zarahn, E., Anderson, K. E., Honig, L. S., Park, A., Hilton, J., Flynn, J., Sackeim, H. A., and Stern, Y. (2004). Cognitive reserve-mediated modulation of positron emission tomographic activations during memory tasks in Alzheimer disease. Arch. Neurol. 61, 73-78.
71. Seo, S. W., Im, K., Lee, J.-M., Kim, S. T., Ahn, H. J., Go, S. M., Kim, S.-H., and Na, D. L. (2011). Effects of demographic factors on cortical thickness in Alzheimer's disease. Neurobiol. Aging 32, 200-209.
72. Del Ser, T., Hachinski, V., Merskey, H., and Munoz, D. G. (1999). An autopsy-verified study of the effect of education on degenerative dementia. Brain J. Neurol. 122 (Pt 12), 2309- 2319.
73. Shpanskaya, K. S., Choudhury, K. R., Hostage, C., Murphy, K. R., Petrella, J. R., Doraiswamy, P. M., and Alzheimer's Disease Neuroimaging Initiative (2014). Educational attainment and hippocampal atrophy in the Alzheimer's disease neuroimaging initiative cohort. J. Neuroradiol. J. Neuroradiol. 41, 350-357.
74. Solé-Padullés, C., Bartrés-Faz, D., Junqué, C., Vendrell, P., Rami, L., Clemente, I. C., Bosch, B., Villar, A., Bargalló, N., Jurado, M. A., et al. (2009). Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease. Neurobiol. Aging 30, 1114-1124.
75. Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R., Jr, Kaye, J., Montine, T. J., et al. (2011). Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging- Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. J. Alzheimers Assoc. 7, 280-292.
76. Staff, R. T., Murray, A. D., Deary, I. J., and Whalley, L. J. (2004). What provides cerebral reserve? Brain J. Neurol. 127, 1191-1199.
77. Stern, Y. (2009). Cognitive reserve. Neuropsychologia 47, 2015-2028.
78. Stern, Y. (2002). What is cognitive reserve? Theory and research application of the reserve concept. J. Int. Neuropsychol. Soc. JINS 8, 448-460.
79. Stern, Y., Albert, S., Tang, M. X., and Tsai, W. Y. (1999). Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology 53, 1942-1947.
80. Stern, Y., Alexander, G. E., Prohovnik, I., and Mayeux, R. (1992). Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer's disease. Ann. Neurol. 32, 371-375.
81. Stern, Y., Gurland, B., Tatemichi, T. K., Tang, M. X., Wilder, D., and Mayeux, R. (1994). Influence of education and occupation on the incidence of Alzheimer's disease. JAMA J. Am. Med. Assoc. 271, 1004-1010.
82. Suo, C., León, I., Brodaty, H., Trollor, J., Wen, W., Sachdev, P., and Valenzuela, M. J. (2012). Supervisory experience at work is linked to low rate of hippocampal atrophy in late life. NeuroImage 63, 1542-1551.
83. Takeuchi, H., Taki, Y., Nouchi, R., Hashizume, H., Sekiguchi, A., Kotozaki, Y., Nakagawa, S., Miyauchi, C.M., Sassa, Y., and Kawashima, R. (2013). Effects of working memory training on functional connectivity and cerebral blood flow during rest. Cortex 49, 2106-2025.
84. Teri, L., McCurry, S. M., Edland, S. D., Kukull, W. A., and Larson, E. B. (1995). Cognitive decline in Alzheimer's disease: a longitudinal investigation of risk factors for accelerated decline. J. Gerontol. A. Biol. Sci. Med. Sci. 50A, M49-55.
85. Unverzagt, F. W., Hui, S. L., Farlow, M. R., Hall, K. S., and Hendrie, H. C. (1998). Cognitive decline and education in mild dementia. Neurology 50, 181-185.
86. Valenzuela, M. J., Jones, M., Wen, W., Rae, C., Graham, S., Shnier, R., and Sachdev, P. (2003). Memory training alters hippocampal neurochemistry in healthy elderly. Neuroreport 14, 1333-1337.
87. Valenzuela, M. J., and Sachdev, P. (2006). Brain reserve and dementia: a systematic review. Psychol. Med. 36, 441-454.
88. Valenzuela, M. J., Sachdev, P., Wen, W., Chen, X., and Brodaty, H. (2008). Lifespan mental activity predicts diminished rate of hippocampal atrophy. PloS One 3, e2598. doi:10.1371/journal.pone.0002598.
89. Vemuri, P., Lesnick, T. G., Przybelski, S. A., Knopman, D. S., Roberts, R. O., Lowe, V. J., Kantarci, K., Senjem, M. L., Gunter, J. L., Boeve, B. F., et al. (2012). Effect of lifestyle activities on Alzheimer disease biomarkers and cognition. Ann. Neurol. 72, 730-738.
90. Vemuri, P., and Mormino, E. C. (2013). Cognitively stimulating activities to keep dementia at bay. Neurology 81, 308-309.
91. Wilson, R. S., Li, Y., Aggarwal, N. T., Barnes, L. L., McCann, J. J., Gilley, D. W., and Evans, D. A. (2004). Education and the course of cognitive decline in Alzheimer disease. Neurology 63, 1198-1202.
92. Wilson, R. S., Mendes De Leon, C. F., Barnes, L. L., Schneider, J. A., Bienias, J. L., Evans, D. A., and Bennett, D. A. (2002). Participation in cognitively stimulating activities and risk of incident Alzheimer disease. JAMA J. Am. Med. Assoc. 287, 742-748.
93. Wirth, M., Haase, C. M., Villeneuve, S., Vogel, J., and Jagust, W. J. (2014a). Neuroprotective pathways: lifestyle activity, brain pathology, and cognition in cognitively normal older adults. Neurobiol. Aging 35, 1873-1882.
94. Wirth, M., Villeneuve, S., La Joie, R., Marks, S. M., and Jagust, W. J. (2014b). Gene- Environment Interactions: Lifetime Cognitive Activity, APOE Genotype, and Beta-Amyloid Burden. J. Neurosci. Off. J. Soc. Neurosci. 34, 8612-8617.
95. Wisdom, N. M., Mignogna, J., and Collins, R. L. (2012). Variability in Wechsler Adult Intelligence Scale-IV subtest performance across age. Arch. Clin. Neuropsychol. Off. J. Natl. Acad. Neuropsychol. 27, 389-397.