The benefits of staying active in old age: Physical activity counteracts the negative influence of PICALM, BIN1, and CLU risk alleles on episodic memory functioning

Psychology and Aging

Volumn 29, Issue 2, 2014, Pages 440-449

  Ferencz, Beata ^a,b   Laukka, Erika J ^a,b   Welmer, Anna Karin ^a   Kalpouzos, Grégoria ^b   Angleman, Sara ^b   Keller, Lina ^b,c   Graff, Caroline ^c,d   Lövdén, Martin ^a,b   Bäckman, Lars ^a,b  

^a AGING RESEARCH CENTER   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Cognitive aging; Episodic memory; Genetic risk; Physical activity

Indexed keywords

BINDING PROTEIN; BIOLOGICAL MARKER; BRIDGING INTEGRATOR 1 PROTEIN; CLUSTERIN; HOSPHATIDYLINOSITOL BINDING CLATHRIN ASSEMBLY PROTEIN; UNCLASSIFIED DRUG; BIN1 PROTEIN, HUMAN; CLATHRIN ASSEMBLY PROTEIN; CLU PROTEIN, HUMAN; NUCLEAR PROTEIN; PICALM PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ADL DISABILITY; AGED; ALLELE; ALZHEIMER DISEASE; ARTICLE; COGNITION; DAILY LIFE ACTIVITY; DISCRIMINANT VALIDITY; DSM-IV; EPISODIC MEMORY; FEMALE; GENETIC RISK; GENOTYPE; HEALTH STATUS; HOMOZYGOTE; HUMAN; MAJOR CLINICAL STUDY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; NEUROPSYCHOLOGICAL TEST; PHYSICAL ACTIVITY; PREVALENCE; RISK FACTOR; SELF REPORT; SENESCENCE; TASK PERFORMANCE; AGING; EXERCISE; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; PHYSIOLOGY; PSYCHOLOGY; SWEDEN; VERY ELDERLY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; AGED, 80 AND OVER; AGING; ALLELES; ALZHEIMER DISEASE; CLUSTERIN; COGNITION; EXERCISE; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MEMORY, EPISODIC; MIDDLE AGED; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; NUCLEAR PROTEINS; RISK FACTORS; SWEDEN; TUMOR SUPPRESSOR PROTEINS;

EID: 84903181008     PISSN: 08827974     EISSN: 19391498     Source Type: Journal    
DOI: 10.1037/a0035465     Document Type: Article

References (66)

1. Ambrose, C. T. (2012). Neuroangiogenesis: A vascular basis for Alzheimer's disease and cognitive decline during aging. Journal of Alzheimer's Disease, 32, 773-788.
2. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.
3. Bäckman, L. (2008). Memory and cognition in preclinical dementia: What we know and what we do not know. The Canadian Journal of Psychiatry, 53, 354-360.
4. Bäckman, L., Jones, S., Berger, A. K., Laukka, E. J.,&Small, B. J. (2005). Cognitive impairment in preclinical Alzheimer's disease: A metaanalysis. Neuropsychology, 19, 520-531.
5. Barral, S., Bird, T., Goate, A., Farlow, M. R., Diaz-Arrastia, R., Bennett, D. A., . . . Mayeux, R. (2012). National Institute on Aging Late-Onset Alzheimer's Disease Genetics Study. Genotype patterns at PICALM, CR1, BIN1, CLU, and APOE genes are associated with episodic memory. Neurology, 78, 1464-1471.
6. Belsky, J., Jonassaint, C., Pluess, M., Stanton, M., Brummett, B., & Williams, R. (2009). Vulnerability genes or plasticity genes? Molecular Psychiatry, 14, 746-754.
7. Bertram, L., McQueen, M. B., Mullin, K., Blacker, D.,&Tanzi, R. E. (2007). Systematic meta-analyses of Alzheimer disease genetic association studies: The AlzGene database. Nature Genetics, 39, 17-23.
8. Biffi, A., Anderson, C. D., Desikan, R. S., Sabuncu, M., Cortellini, L., Schmansky, N., . . . Rosand, J. (2010). Genetic variation and neuroimaging measures in Alzheimer disease. Archives of Neurology, 67, 677-685.
9. Colcombe, S. J., Erickson, K. I., Scalf, P. E., Kim, J. S., Prakash, R., Mcauley, E., . . . Kramer, A. F. (2006). Aerobic exercise training increases brain volume in aging humans. The Journals of Gerontology: Series A: Biological Sciences and Medical Sciences, 61, 1166-1170.
10. Colcombe, S.,&Kramer, A. F. (2003). Fitness effects on the cognitive function of older adults: A meta-analytic study. Psychological Science, 14, 125-130.
11. Dahl, M., Allwood, C. M.,&Hagberg, B. (2009). The realism in older people's confidence judgments of answers to general knowledge questions. Psychology and Aging, 24, 234-238.
12. Darki, F., Peyrar-Janvid, M., Matsson, H., Kere, J.,&Klingberg, T. (2012). Three dyslexia susceptibility genes, DYX1C1, DCDC2, and KIAA0319, affect temporo-parietal white matter structure. Biological Psychiatry, 72, 671-676.
13. Ducci, F., Enoch, M. A., Hodgkinson, C., Xu, K., Catena, M., Robin, R. W.,&Goldman, D. (2008). Interaction between a functional MAOA locus and childhood sexual abuse predicts alcoholism and antisocial personality disorder in adult women. Molecular Psychiatry, 13, 334-347.
14. Dureman, I. (1960). SRB:1. Stockholm, Sweden: Psykologiförlaget.
15. Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., & Engel, S. E. (2000). Remembering episodes: A selective role for the hippocampus during retrieval. Nature Neuroscience, 3, 1149-1152.
16. Elias-Sonnenschein, L. S., Bertram, L.,&Visser, P. J. (2012). Relationship between genetic risk factors and markers for Alzheimer's disease pathology. Biomarkers Medicine, 6, 477-495.
17. Erickson, K. I., Banducci, S. E., Weinstein, A. M., Macdonald, A. W., Ferrell, R. E., Halder, I., . . . Manuck, S. B. (2013). The brain-derived neurotrophic factor Val66Met polymorphism moderates an effect of physical activity on working memory performance. Psychological Science, 24, 1770-1779.
18. Erickson, K. I., Voss, M. W., Prakash, R. S., Basak, C., Szabo, A., Chaddock, L., . . . Kramer, A. F. (2011). Exercise training increases size of hippocampus and improves memory. PNAS Proceedings of the National Academy of Sciences of the United States of America, 108, 3017-3022.
19. Gerecke, K. M., Kolobova, A., Allen, S.,&Fawer, J. L. (2013). Exercise protects against chronic restraint stress-induced oxidative stress in the cortex and hippocampus. Brain Research, 1509, 66-78.
20. Habib, R., Nyberg, L.,&Nilsson, L. G. (2007). Cognitive and noncognitive factors contributing to the longitudinal identification of successful older adults in the Betula study. Neuropsychology, Development, and Cognition: Section B, Aging, Neuropsychology and Cognition, 14, 257-273.
21. Head, D., Bugg, J. M., Goate, A. M., Fagan, A. M., Mintun, M. A., Benzinger, T., . . . Morris, J. C. (2012). Exercise engagement as a moderator of APOE effects on amyloid deposition. Archives of Neurology, 69, 636-643.
22. Intlekofer, K. A.,&Cotman, C. W. (2013). Exercise counteracts declining hippocampal function in aging and Alzheimer's disease. Neurobiology of Disease, 57, 47-55.
23. Jones, L., Harold, D.,&Williams, J. (2010). Genetic evidence for the involvement of lipid metabolism in Alzheimer's disease. Biochimica et biophysica acta, 1801, 754-761.
24. Josefsson, M., de Luna, X., Pudas, S., Nilsson, L.-G.,&Nyberg, L. (2012). Genetic and lifestyle predictors of 15-year longitudinal change in episodic memory. Journal of American Geriatrics Society, 60, 2308-2312.
25. Kempermann, G. (2008). The neurogenic reserve hypothesis: What is adult hippocampal neurogenesis good for? Trends in Neurosciences, 31, 163-169.
26. Kivipelto, M., Rovio, S., Ngandu, T., Kareholt, I., Eskeline, M., Winblad, B., . . . Nissinen, A. (2008). Apolipoprotein APOE e4 magnifies lifestyle risks for dementia: A population-based study. Journal of Cellular and Molecular Medicine, 12, 2762-2771.
27. Laukka, E. J., Lövdén, M., Herlitz, A., Karlsson, S., Ferencz, B., Pantzar, A., . . . Bäckman, L. (2013). Genetic effects on old-age cognitive functioning: A population-based study. Psychology and Aging, 28, 262-274.
28. Li, S. C., Chicherio, C., Nyberg, L., von Oertzen, T., Nagel, I. E., Papenberg, G., . . . Montine, T. J. (2010). Ebbinghaus revisited: Influences of the BDNF Val66Met polymorphism on backward serial recall are modulated by human aging. Journal of Cognitive Neuroscience, 22, 2164-2173.
29. Li, S. C., Papenberg, G., Nagel, I. E., Preuschhof, C., Schröder, J., Nietfeld, W., . . . Bäckman, L. (2013). Aging magnifies the effects of dopamine transporter and D2 receptor genes on backward serial memory. Neurobiology of Aging, 34, 358.e1-358e.10.
30. Liang, K. Y., Mintun, M. A., Fagan, A. M., Goate, A. M., Bugg, J. M., Holtzman, D. M., . . . Head, D. (2010). Exercise and Alzheimer's disease biomarkers in cognitively normal adults. Annals of Neurology, 68, 311-318.
31. Lin, M. T.,&Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature, 443, 787-795.
32. Lindenberger, U., Nagel, I. E., Chicherio, C., Li, S. C., Heekeren, H. R., & Bäckman, L. (2008). Age-related decline in brain resources modulates genetic effects on cognitive functioning. Frontiers in neuroscience, 2, 234-244.
33. Lindwall, M.,&Rennemark, M. (2007). The effect of change in exercise behaviour on cognitive functioning in older people. Journal of Sport Science, 25, 314-315.
34. Lista, I.,&Sorrentino, G. (2010). Biological mechanisms of physical activity in preventing cognitive decline. Cellular and Molecular Neurobiology, 30, 493-503.
35. Marosi, K., Bori, Z., Hart, N., Sárga, L., Koltai, E., Radák, Z.,&Nyakas, C. (2012). Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats. Neuroscience, 226, 21-28.
36. Meijer, E. P., Goris, A. H., van Dongen, D. L., Bast, A.,&Westerterp, K. R. (2002). Exercise-induced oxidative stress in older adults as a function of habitual activity level. Journal of American Geriatric Society, 50, 349-353.
37. Murtagh, E. M., Murphy, M. H.,&Boone-Heinonen, J. (2010). Walking: The first steps in cardiovascular disease prevention. Current Opinion in Cardiology, 25, 490-496.
38. Nelson, M. E., Rejeski, W. J., Blair, S. N., Duncan, P. W., Judge, J. O., King, A. C., . . . Castaneda-Sceppa, C. (2007). Physical activity and public health in older adults: Recommendation from the American College of Sports Medicine and the American Heart Association. Medicine & Science in Sports&Exercise, 39, 1435-1445.
39. Nilsson, L. G., Adolfsson, R., Bäckman, L., Cruts, M., Nyberg, L., Small, B. J.,&Broeckoven, C. (2006). The influence of APOE status on episodic and semantic memory: Data from a population-based study. Neuropsychology, 20, 645-657.
40. Nilsson, L. G., Bäckman, L., Erngrund, K., Nyberg, L., Adolfsson, R., Bucht, G., . . . Winblad, B. (1997). The Betula prospective cohort study: Memory, health, and aging. Aging, Neuropsychology, and Cognition, 4, 1-32.
41. Nyberg, L., Lövdén, M., Riklund, K., Lindenberger, U.,&Bäckman, L. (2012). Memory aging and brain maintenance. Trends in Cognitive Sciences, 16, 292-305.
42. Nyberg, L., McIntosh, A. R., Houle, S., Nilsson, L. G.,&Tulving, E. (1996). Activation of medial temporal structures during episodic memory retrieval. Nature, 380, 715-717.
43. Papenberg, G., Bäckman, L., Nagel, I. E., Nietfeld, W., Schröder, J., Bertram, L., . . . Li, S. C. (2013). Dopaminergic gene polymorphisms affect long-term forgetting in old age: Further support for the magnification hypothesis. Journal of Cognitive Neuroscience, 25, 571-579.
44. Podewils, L. J., Guallar, E., Kuller, L. H., Fried, L. P., Lopez, O. L., Carlson, M.,&Lyketsos, C. G. (2005). Physical activity, APOE genotype, and dementia risk: Findings from the Cardiovascular Health Cognition Study. American Journal of Epidemiology, 161, 639-651.
45. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., . . . Acker, J. D. (2005). Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex, 15, 1676-1689.
46. Rennemark, M., Lindwall, M., Halling, A.,&Berglund, J. (2009). Relationships between physical activity and perceived qualities of life in old age: Results from the Swedish National study on Aging and Care. Aging & Mental Health, 13, 1-8.
47. Retz, W., Freitag, C. M., Retz-Junginger, P., Wenzler, D., Schneider, M., Kissling, C., . . . Rösler, M. (2008). A functional serotonin transporter promoter gene polymorphism increases ADHD symptoms in delinquents: Inter action with adverse childhood environment. Psychiatry Research, 158, 123-131.
48. Rodríguez-Rodríguez, E., Sánchez-Juan, P., Vázquez-Higuera, J. L., Mateo, I., Pozueta, A., Berciano, J., . . . Combarros, O. (2013). Genetic risk score predicting accelerated progression from mild cognitive impairment to Alzheimer's disease. Journal of Neural Transmission, 120, 807-812.
49. Rönnlund, M., Nyberg, L., Bäckman, L.,&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.
50. Rydwik, E., Welmer, A. K., Kåreholt, I., Angleman, S., Fratiglioni, L., & Wang, H. X. (2013). Adherence to physical exercise recommendations in people over 65: The SNAC-Kungsholmen study. European Journal of Public Health, 23, 799-804.
51. Salthouse, T. A.,&Babcock, R. L. (1991). Decomposing adult age differences in working memory. Developmental Psychology, 27, 763-776.
52. Schjeide, B. M. M., Schnack, C., Lambert, J. C., Lill, C. M., Kirchheiner, J., Tumani, H., . . . Bertram, L. (2011). The role of clusterin, complement receptor 1, and phosphatidylinositol binding clathrin assembly protein in Alzheimer disease risk and cerebrospinal fluid biomarker levels. Archives of General Psychiatry, 68, 207-213.
53. Serrano, F.,&Klann, E. (2004). Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Research Reviews, 3, 431-443.
54. Small, B. J., Dixon, R. A., McArdle, J. J.,&Grimm, K. J. (2012). Do changes in lifestyle engagement moderate cognitive decline in normal aging? Evidence from the Victoria Longitudinal Study. Neuropsychology, 26, 144-155.
55. Smith, P. J., Blumenthal, J. A., Hoffman, B. M., Cooper, H., Strauman, T. A., Welsh-Bohmer, K., . . . Sherwood, A. (2010). Aerobic exercise and neurocognitive performance: A meta-analytic review of randomized controlled trials. Psychosomatic Medicine, 72, 239-252.
56. Spirduso, W. W. (1975). Reaction and movement time as a function of age and physical activity level. Journal of Gerontology, 30, 435-440.
57. Squire, L. R. (1986). Mechanisms of memory. Science, 232, 1612-1619.
58. Taylor, S. E., Way, B. M., Welch, W. T., Hilmert, C. J., Lehman, B. J., & Eisenberger, N. I. (2006). Early family environment, current adversity, the serotonin transporter promoter polymorphism, and depressive symptomatology. Biological Psychiatry, 60, 671-676.
59. Trougakos, I. P.,&Gonos, E. S. (2006). Regulation of clusterin/apolipoprotein J, a functional homologue to the small heat shock proteins, by oxidative stress in ageing and age-related diseases. Free Radical Research, 40, 1324-1334.
60. Voelcker-Rehage, C.,&Niemann, C. (2013). Structural and functional brain changes related to different types of physical activity across the life span. Neuroscience and Biobehavioral Reviews, 49, 2268-2295.
61. Wang, H. X., Jin, Y., Hendrie, H. C., Liang, C., Yang, L., Cheng, Y., . . . Gao, S. (2013). Late life leisure activities and risk of cognitive decline. Journals of Gerontology: Series A: Biological Sciences and Medical Sciences, 68, 205-213.
62. World Health Organization. (2010). Global recommendations on physical activity for health. Retrieved from http://whqlibdoc.who.int/publications/2010/9789241599979_eng.pdf
63. Wisdom, N. M., Callahan, J. L.,&Hawkins, K. A. (2011). The effects of apolipoprotein E on non-impaired cognitive functioning: A meta-analysis. Neurobiology of Aging, 32, 63-74.
64. Woodard, J. L., Sugarman, M. A., Nielson, K. A., Smith, J. C., Seidenberg, M., Durgerian, S., . . . Rao, S. M. (2012). Lifestyle and genetic contributions to cognitive decline and hippocampal structure and function in healthy aging. Current Alzheimer Research, 9, 436-446.
65. Yonelinas, A. P. (2001). Components of episodic memory: The contribution of recollection and familiarity. Philosophical Transactions of the Royal Society of London: Series B: Biological Sciences, 356, 1363-1374.
66. Zazzo, R. (1974). Test des deux barrages. Actualités pédagogiques et psychologiques [Test of the two dams. News pedagogical and psychological.]. Neuchâtel, Switzerland: Delachaux et Nestlé.