APOE moderates compensatory recruitment of neuronal resources during working memory processing in healthy older adults

Neurobiology of Aging

Volumn 56, Issue , 2017, Pages 127-137

  Scheller, Elisa ^a,b   Peter, Jessica ^a,c   Schumacher, Lena V ^a,b   Lahr, Jacob ^a,b   Mader, Irina ^a,b   Kaller, Christoph P ^a,b   Klöppel, Stefan ^a,b,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Aging; APOE; Functional magnetic resonance imaging; Moderator analysis; Multiple regression; Neuronal compensation; Working memory

Indexed keywords

APOLIPOPROTEIN E4;

ADULT; AGE; AGED; ARTICLE; BRAIN REGION; BRAIN SIZE; COGNITION; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; INSULA; LEFT HEMISPHERE; MALE; MULTIPLE REGRESSION; NORMAL HUMAN; POSTCENTRAL GYRUS; PRIORITY JOURNAL; PUTAMEN; RIGHT HEMISPHERE; SUPERIOR OCCIPITAL GYRUS; SUPERIOR ORBITAL GYRUS; TASK PERFORMANCE; THALAMUS; VOXEL BASED MORPHOMETRY; WORKING MEMORY; AGING; ALLELE; ALZHEIMER DISEASE; BRAIN; DIAGNOSTIC IMAGING; GENETIC VARIATION; GENETICS; GENOTYPE; HETEROZYGOTE; MIDDLE AGED; NEUROPHYSIOLOGICAL RECRUITMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; REGRESSION ANALYSIS; RISK; SHORT TERM MEMORY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; ALLELES; ALZHEIMER DISEASE; APOLIPOPROTEIN E4; BRAIN; COGNITION; FEMALE; GENETIC VARIATION; GENOTYPE; HETEROZYGOTE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; RECRUITMENT, NEUROPHYSIOLOGICAL; REGRESSION ANALYSIS; RISK;

EID: 85019864049     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2017.04.015     Document Type: Article

References (97)

1. Agosta, F., Galantucci, S., Filippi, M., Advanced magnetic resonance imaging of neurodegenerative diseases. Neurol. Sci. 38 (2017), 41–51.
2. Alexander, D.M., Williams, L.M., Gatt, J.M., Dobson-Stone, C., Kuan, S.A., Todd, E.G., Schofield, P.R., Cooper, N.J., Gordon, E., The contribution of apolipoprotein E alleles on cognitive performance and dynamic neural activity over six decades. Biol. Psychol. 75 (2007), 229–238.
3. Ashburner, J., A fast diffeomorphic image registration algorithm. NeuroImage 38 (2007), 95–113.
4. Axmacher, N., Henseler, M.M., Jensen, O., Weinreich, I., Elger, C.E., Fell, J., Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc. Natl. Acad. Sci. 107 (2010), 3228–3233.
5. Axmacher, N., Mormann, F., Fernández, G., Cohen, M.X., Elger, C.E., Fell, J., Sustained neural activity patterns during working memory in the human medial temporal lobe. J. Neurosci. 27 (2007), 7807–7816.
6. Barulli, D., Stern, Y., Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn. Sci. 17 (2013), 502–509.
7. Bauer, D.J., Curran, P.J., Probing interactions in fixed and multilevel regression: inferential and graphical techniques. Multivar. Behav. Res. 40 (2005), 373–400.
8. Bondi, M.W., Houston, W.S., Eyler, L.T., Brown, G.G., fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology 64 (2005), 501–508.
9. Bonnelle, V., Ham, T.E., Leech, R., Kinnunen, K.M., Mehta, M.A., Greenwood, R.J., Sharp, D.J., Salience network integrity predicts default mode network function after traumatic brain injury. Proc. Natl. Acad. Sci. 109 (2012), 4690–4695.
10. Bookheimer, S., Burggren, A., APOE-4 genotype and neurophysiological vulnerability to Alzheimer's and cognitive aging. Annu. Rev. Clin. Psychol. 5 (2009), 343–362.
11. Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., The Brain's default network. Ann. N. Y. Acad. Sci. 1124 (2008), 1–38.
12. Cabeza, R., Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 17 (2002), 85–100.
13. Cabeza, R., Anderson, N.D., Locantore, J.K., McIntosh, A.R., Aging gracefully: compensatory brain activity in high-performing older adults. NeuroImage 17 (2002), 1394–1402.
14. Cabeza, R.E., Dennis, N.A., Frontal lobes and aging: deterioration and compensation. Stuss, D.T., Knight, R.T., (eds.) Principles of Frontal Lobe Function, 2013, Oxford University Press, New York, 628–652.
15. Caselli, R.J., Dueck, A.C., Locke, D.E.C., Hoffman-Snyder, C.R., Woodruff, B.K., Rapcsak, S.Z., Reiman, E.M., Longitudinal modeling of frontal cognition in APOE ε4 homozygotes, heterozygotes, and noncarriers. Neurology 76 (2011), 1383–1388.
16. Cavedo, E., Lista, S., Khachaturian, Z., Aisen, P., Amouyel, P., Herholz, K., Jack, C.R., Sperling, R., Cummings, J., Blennow, K., O'Bryant, S., Frisoni, G.B., Khachaturian, A., Kivipelto, M., Klunk, W., Broich, K., Andrieu, S., de Schotten, M.T., Mangin, J.-F., Lammertsma, A.A., Johnson, K., Teipel, S., Drzezga, A., Bokde, A., Colliot, O., Bakardjian, H., Zetterberg, H., Dubois, B., Vellas, B., Schneider, L.S., Hampel, H., The road ahead to cure Alzheimer's disease: development of biological markers and neuroimaging methods for prevention trials across all stages and target populations. J. Prev. Alzheimers Dis. 1 (2014), 181–202.
17. Chen, C.-J., Chen, C.-C., Wu, D., Chi, N.-F., Chen, P.-C., Liao, Y.-P., Chiu, H.-W., Hu, C.-J., Effects of the apolipoprotein E ε4 allele on functional MRI during n-back working memory tasks in healthy middle-aged adults. Am. J. Neuroradiol 34 (2013), 1197–1202.
18. Chen, Y., Chen, K., Zhang, J., Li, X., Shu, N., Wang, J., Zhang, Z., Reiman, E.M., Disrupted functional and structural networks in cognitively normal elderly subjects with the APOE ε4 allele. Neuropsychopharmacology 40 (2015), 1181–1191.
19. Cieslik, E.C., Mueller, V.I., Langner, R., Eickhoff, S.B., Three key regions for supervisory attentional control: evidence from neuroimaging meta-analyses. Neurosci. Biobehav. Rev. 48 (2015), 22–34.
20. Cohen, J., Cohen, P., West, S.G., Aiken, L.S., Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences. third ed., 2003, Erlbaum Associates, Mahwah (NJ).
21. Corbo, R.M., Scacchi, R., Apolipoprotein E (APOE) allele distribution in the world. Is APOE⋆4 a ‘thrifty’ allele?. Ann. Hum. Genet. 63 (1999), 301–310.
22. Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Small, G.W., Roses, A.D., Haines, J.L., Pericak-Vance, M.A., Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261 (1993), 921–923.
23. Crivello, F., Lemaître, H., Dufouil, C., Grassiot, B., Delcroix, N., Tzourio-Mazoyer, N., Tzourio, C., Mazoyer, B., Effects of ApoE-ɛ4 allele load and age on the rates of grey matter and hippocampal volumes loss in a longitudinal cohort of 1186 healthy elderly persons. NeuroImage 53 (2010), 1064–1069.
24. Damoiseaux, J.S., Beckmann, C.F., Arigita, E.J.S., Barkhof, F., Scheltens, P., Stam, C.J., Smith, S.M., Rombouts, S.A.R.B., Reduced resting-state brain activity in the “default network” in normal aging. Cereb. Cortex 18 (2008), 1856–1864.
25. Darki, F., Klingberg, T., The role of fronto-parietal and fronto-striatal networks in the development of working memory: a longitudinal study. Cereb. Cortex 25 (2015), 1587–1595.
26. Davis, S.W., Dennis, N.A., Daselaar, S.M., Fleck, M.S., Cabeza, R., Qué PASA? The posterior–anterior shift in aging. Cereb. Cortex 18 (2008), 1201–1209.
27. D'Esposito, M., Deouell, L.Y., Gazzaley, A., Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci. 4 (2003), 863–872.
28. Duverne, S., Motamedinia, S., Rugg, M.D., The relationship between aging, performance, and the neural correlates of successful memory encoding. Cereb. Cortex 19 (2009), 733–744.
29. Eickhoff, S.B., Stephan, K.E., Mohlberg, H., Grefkes, C., Fink, G.R., Amunts, K., Zilles, K., A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25 (2005), 1325–1335.
30. Evans, S., Dowell, N.G., Tabet, N., Tofts, P.S., King, S.L., Rusted, J.M., Cognitive and neural signatures of the APOE E4 allele in mid-aged adults. Neurobiol. Aging 35 (2014), 1615–1623.
31. Faraco, C.C., Puente, A.N., Brown, C., Terry, D.P., Stephen Miller, L., Lateral temporal hyper-activation as a novel biomarker of mild cognitive impairment. Neuropsychologia 51 (2013), 2281–2293.
32. Farrer, L.A., Cupples, L.A., Haines, J.L., Hyman, B., Kukull, W.A., Mayeux, R., Myers, R.H., Pericak-Vance, M.A., Risch, N., van Duijn, C.M., Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium. JAMA 278 (1997), 1349–1356.
33. Filbey, F.M., Chen, G., Sunderland, T., Cohen, R.M., Failing compensatory mechanisms during working memory in older apolipoprotein e-ε4 healthy adults. Brain Imaging Behav. 4 (2010), 177–188.
34. Filbey, F.M., Slack, K.J., Sunderland, T.P., Cohen, R.M., Functional magnetic resonance imaging and magnetoencephalography differences associated with APOEɛ 4 in young healthy adults. Neuroreport 17 (2006), 1585–1590.
35. Filippini, N., Ebmeier, K.P., MacIntosh, B.J., Trachtenberg, A.J., Frisoni, G.B., Wilcock, G.K., Beckmann, C.F., Smith, S.M., Matthews, P.M., Mackay, C.E., Differential effects of the APOE genotype on brain function across the lifespan. NeuroImage 54 (2011), 602–610.
36. Filippini, N., Nickerson, L.D., Beckmann, C.F., Ebmeier, K.P., Frisoni, G.B., Matthews, P.M., Smith, S.M., Mackay, C.E., Age-related adaptations of brain function during a memory task are also present at rest. NeuroImage 59 (2012), 3821–3828.
37. Flöel, A., tDCS-enhanced motor and cognitive function in neurological diseases. NeuroImage 85 (2014), 934–947.
38. Fouquet, M., Besson, F.L., Gonneaud, J., Joie, R.L., Chételat, G., Imaging brain effects of APOE4 in cognitively normal individuals across the lifespan. Neuropsychol. Rev. 24 (2014), 290–299.
39. Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Essen, D.C.V., Raichle, M.E., The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9673–9678.
40. Friston, K.J., Frith, C.D., Turner, R., Frackowiak, R.S.J., Characterizing evoked hemodynamics with fMRI. Neuroimage 2 (1995), 157–165.
41. Goh, J.O.S., Functional dedifferentiation and altered connectivity in older adults: neural accounts of cognitive aging. Aging Dis. 2 (2011), 30–48.
42. Grady, C.L., Protzner, A.B., Kovacevic, N., Strother, S.C., Afshin-Pour, B., Wojtowicz, M., Anderson, J.A.E., Churchill, N., McIntosh, A.R., A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. Cereb. Cortex 20 (2010), 1432–1447.
43. Greenwood, P.M., Espeseth, T., Lin, M.-K., Reinvang, I., Parasuraman, R., Longitudinal change in working memory as a function of APOE genotype in midlife and old age. Scand. J. Psychol. 55 (2014), 268–277.
44. Hafkemeijer, A., van der Grond, J., Rombouts, S.A.R.B., Imaging the default mode network in aging and dementia. Biochim. Biophys. Acta 1822 (2012), 431–441.
45. Hale, S., Rose, N.S., Myerson, J., Strube, M.J., Sommers, M., Tye-Murray, N., Spehar, B., The structure of working memory abilities across the adult life span. Psychol. Aging 26 (2011), 92–110.
46. Han, S.D., Houston, W.S., Jak, A.J., Eyler, L.T., Nagel, B.J., Fleisher, A.S., Brown, G.G., Corey-Bloom, J., Salmon, D.P., Thal, L.J., Bondi, M.W., Verbal paired-associate learning by APOE genotype in non-demented older adults: fMRI evidence of a right hemispheric compensatory response. Neurobiol. Aging 28 (2007), 238–247.
47. Hayes, A.F., Introduction to Mediation, Moderation, and Conditional Process Analysis. 2013, Guilford Publications, New York.
48. Heinzel, S., Schulte, S., Onken, J., Duong, Q.-L., Riemer, T.G., Heinz, A., Kathmann, N., Rapp, M.A., Working memory training improvements and gains in non-trained cognitive tasks in young and older adults. Aging Neuropsychol. Cogn. 21 (2014), 146–173.
49. Jaccard, J., Turrisi, R., Interaction effects in multiple regression. Sage University Paper Series on Quantitative Applications in the Social Sciences, 07–072, second ed., 2003, Sage, Thousand Oaks (CA).
50. Jaeggi, S.M., Buschkuehl, M., Perrig, W.J., Meier, B., The concurrent validity of the N-back task as a working memory measure. Memory 18 (2010), 394–412.
51. Johnson, P.O., Neyman, J., Tests of certain linear hypotheses and their application to some educational problems. Stat. Res. Mem. 1 (1936), 57–93.
52. Kaller, C.P., Heinze, K., Mader, I., Unterrainer, J.M., Rahm, B., Weiller, C., Köstering, L., Linking planning performance and gray matter density in mid-dorsolateral prefrontal cortex: moderating effects of age and sex. NeuroImage 63 (2012), 1454–1463.
53. Kannurpatti, S.S., Motes, M.A., Rypma, B., Biswal, B.B., Neural and vascular variability and the fMRI-BOLD response in normal aging. Magn. Reson. Imaging 28 (2010), 466–476.
54. Klingberg, T., Training and plasticity of working memory. Trends Cogn. Sci. 14 (2010), 317–324.
55. LaBar, K.S., Gitelman, D.R., Parrish, T.B., Mesulam, M.-M., Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects. Neuroimage 10 (1999), 695–704.
56. Lindenberger, U., Age-related decline in brain resources magnifies genetic effects on cognitive functioning. Front. Neurosci. 2 (2008), 234–244.
57. Lindenberger, U., Human cognitive aging: corriger la fortune?. Science 346 (2014), 572–578.
58. Luis, C.A., Keegan, A.P., Mullan, M., Cross validation of the Montreal Cognitive Assessment in community dwelling older adults residing in the Southeastern US. Int. J. Geriatr. Psychiatry 24 (2009), 197–201.
59. Meinzer, M., Lindenberg, R., Antonenko, D., Flaisch, T., Floel, A., Anodal transcranial direct current stimulation temporarily reverses age-associated cognitive decline and functional brain activity changes. J. Neurosci. 33 (2013), 12470–12478.
60. Menon, V., Uddin, L.Q., Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214 (2010), 655–667.
61. Mondadori, C.R.A., de Quervain, D.J.-F., Buchmann, A., Mustovic, H., Wollmer, M.A., Schmidt, C.F., Boesiger, P., Hock, C., Nitsch, R.M., Papassotiropoulos, A., Henke, K., Better memory and neural efficiency in young apolipoprotein E ε4 carriers. Cereb. Cortex 17 (2007), 1934–1947.
62. Nasreddine, Z.S., Phillips, N.A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J.L., Chertkow, H., The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53 (2005), 695–699.
63. Owen, A.M., McMillan, K.M., Laird, A.R., Bullmore, E., N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Mapp. 25 (2005), 46–59.
64. Papenberg, G., Lindenberger, U., Bäckman, L., Aging-related magnification of genetic effects on cognitive and brain integrity. Trends Cogn. Sci. 19 (2015), 506–514.
65. Park, D.C., Reuter-Lorenz, P.A., The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 60 (2009), 173–196.
66. Persson, J., Pudas, S., Nilsson, L.-G., Nyberg, L., Longitudinal assessment of default-mode brain function in aging. Neurobiol. Aging 35 (2014), 2107–2117.
67. Price, C.J., Friston, K.J., Scanning patients with tasks they can perform. Hum. Brain Mapp. 8 (1999), 102–108.
68. Prvulovic, D., Van de Ven, V., Sack, A.T., Maurer, K., Linden, D.E.J., Functional activation imaging in aging and dementia. Psychiatry Res. Neuroimaging 140 (2005), 97–113.
69. Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function. Proc. Natl. Acad. Sci. 98 (2001), 676–682.
70. Rasch, B., Papassotiropoulos, A., de Quervain, D.-F., Imaging genetics of cognitive functions: focus on episodic memory. NeuroImage 53 (2010), 870–877.
71. Redick, T.S., Lindsey, D.R.B., Complex span and n-back measures of working memory: a meta-analysis. Psychon. Bull. Rev. 20 (2013), 1102–1113.
72. Reuter-Lorenz, P.A., Aging and cognitive neuroimaging a fertile union. Perspect. Psychol. Sci. 8 (2013), 68–71.
73. Reuter-Lorenz, P.A., Cappell, K.A., Neurocognitive aging and the compensation hypothesis. Curr. Dir. Psychol. Sci. 17 (2008), 177–182.
74. Roalf, D.R., Moberg, P.J., Xie, S.X., Wolk, D.A., Moelter, S.T., Arnold, S.E., Comparative accuracies of two common screening instruments for classification of Alzheimer's disease, mild cognitive impairment, and healthy aging. Alzheimers Dement 9 (2013), 529–537.
75. Rottschy, C., Langner, R., Dogan, I., Reetz, K., Laird, A.R., Schulz, J.B., Fox, P.T., Eickhoff, S.B., Modelling neural correlates of working memory: a coordinate-based meta-analysis. NeuroImage 60 (2012), 830–846.
76. Rusted, J.M., Evans, S.L., King, S.L., Dowell, N., Tabet, N., Tofts, P.S., APOE e4 polymorphism in young adults is associated with improved attention and indexed by distinct neural signatures. NeuroImage 65 (2013), 364–373.
77. Sala-Llonch, R., Arenaza-Urquijo, E.M., Junqué, C., Bartrés-Faz, D., Dynamic functional reorganizations and relationship with working memory performance in healthy aging. Front. Hum. Neurosci., 6, 2012, 152.
78. Salthouse, T.A., When does age-related cognitive decline begin?. Neurobiol. Aging 30 (2009), 507–514.
79. Salthouse, T.A., Selective review of cognitive aging. J. Int. Neuropsychol. Soc. 16 (2010), 754–760.
80. Salthouse, T.A., Neuroanatomical substrates of age-related cognitive decline. Psychol. Bull. 137 (2011), 753–784.
81. Salthouse, T.A., Babcock, R.L., Decomposing adult age differences in working memory. Dev. Psychol., 27, 1991, 763.
82. Sambataro, F., Murty, V.P., Callicott, J.H., Tan, H.-Y., Das, S., Weinberger, D.R., Mattay, V.S., Age-related alterations in default mode network: impact on working memory performance. Neurobiol. Aging 31 (2010), 839–852.
83. Scheller, E., Minkova, L., Leitner, M., Klöppel, S., Attempted and successful compensation in preclinical and early manifest neurodegeneration - a review of task fMRI studies. Front. Psychiatry, 5, 2014, 132.
84. Schneider-Garces, N.J., Gordon, B.A., Brumback-Peltz, C.R., Shin, E., Lee, Y., Sutton, B.P., Maclin, E.L., Gratton, G., Fabiani, M., Span, CRUNCH, and beyond: working memory capacity and the aging brain. J. Cogn. Neurosci. 22 (2010), 655–669.
85. Shen, S., Sterr, A., Is DARTEL-based voxel-based morphometry affected by width of smoothing kernel and group size? A study using simulated atrophy. J. Magn. Reson. Imaging 37 (2013), 1468–1475.
86. Small, B.J., Rosnick, C.B., Fratiglioni, L., Bäckman, L., Apolipoprotein E and cognitive performance: a meta-analysis. Psychol. Aging 19 (2004), 592–600.
87. Sperling, R.A., The potential of functional MRI as a biomarker in early Alzheimer's disease. Neurobiol. Aging 32:Suppl 1 (2011), S37–S43.
88. 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., Park, D.C., Reiman, E.M., Rowe, C.C., Siemers, E., Stern, Y., Yaffe, K., Carrillo, M.C., Thies, B., Morrison-Bogorad, M., Wagster, M.V., Phelps, C.H., 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 7 (2011), 280–292.
89. Spreng, R.N., Wojtowicz, M., Grady, C.L., Reliable differences in brain activity between young and old adults: a quantitative meta-analysis across multiple cognitive domains. Neurosci. Biobehav. Rev. 34 (2010), 1178–1194.
90. Stern, Y., Cognitive reserve. Neuropsychologia 47 (2009), 2015–2028.
91. Taylor, J.L., Scanlon, B.K., Farrell, M., Hernandez, B., Adamson, M.M., Ashford, J.W., Noda, A., Murphy, G.M. Jr., Weiner, M.W., APOE-epsilon4 and aging of medial temporal lobe gray matter in healthy adults older than 50 years. Neurobiol. Aging 35 (2014), 2479–2485.
92. Trachtenberg, A.J., Filippini, N., Mackay, C.E., The effects of APOE-ε4 on the BOLD response. Neurobiol. Aging 33 (2012), 323–334.
93. Tsvetanov, K.A., Henson, R.N.A., Tyler, L.K., Davis, S.W., Shafto, M.A., Taylor, J.R., Williams, N., Cam-CAN, Rowe, J.B., The effect of ageing on fMRI: correction for the confounding effects of vascular reactivity evaluated by joint fMRI and MEG in 335 adults. Hum. Brain Mapp. 36 (2015), 2248–2269.
94. Wilson, R.S., Leurgans, S.E., Boyle, P.A., Bennett, D.A., Cognitive decline in prodromal Alzheimer disease and mild cognitive impairment. Arch. Neurol. 68 (2011), 351–356.
95. Wisdom, N.M., Callahan, J.L., Hawkins, K.A., The effects of apolipoprotein E on non-impaired cognitive functioning: a meta-analysis. Neurobiol. Aging 32 (2011), 63–74.
96. Wishart, H., Saykin, A., Rabin, L., Santulli, R., Flashman, L., Guerin, S., Mamourian, A., Belloni, D., Rhodes, C., McAllister, T., Increased brain activation during working memory in cognitively intact adults with the APOE ε4 allele. Am. J. Psychiatry 163 (2006), 1603–1610.
97. Zaitsev, M., Dold, C., Sakas, G., Hennig, J., Speck, O., Magnetic resonance imaging of freely moving objects: prospective real-time motion correction using an external optical motion tracking system. NeuroImage 31 (2006), 1038–1050.