Alzheimer disease biomarkers, attentional control, and semantic memory retrieval: Synergistic and mediational effects of biomarkers on a sensitive cognitive measure in non-demented older adults

Neuropsychology

Volumn 29, Issue 3, 2015, Pages 368-381

  Aschenbrenner, Andrew J ^a   Balota, David A ^a   Tse, Chi Shing ^b   Fagan, Anne M ^c   Holtzman, David M ^c   Benzinger, Tammie L S ^d   Morris, John C ^c  

^a WASHINGTON UNIVERSITY   (United States)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Attention; Biomarkers; Semantic retrieval

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; BIOLOGICAL MARKER; PITTSBURGH COMPOUND B; TAU PROTEIN; AMYLOID BETA PROTEIN;

ACCURACY; AGED; ALZHEIMER DISEASE; ARTICLE; CEREBROSPINAL FLUID; CLINICAL DEMENTIA RATING; COGNITION; CONTROLLED STUDY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MEMORY CONSOLIDATION; MINI MENTAL STATE EXAMINATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PSYCHOMETRY; SEMANTIC MEMORY; ATTENTION; BRAIN; DIAGNOSTIC IMAGING; FEMALE; GENETICS; MALE; MEMORY; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PHOSPHORYLATION; PHYSIOLOGY; PSYCHOLOGY; SCINTISCANNING; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; APOLIPOPROTEINS E; ATTENTION; BIOMARKERS; BRAIN; COGNITION; FEMALE; GENOTYPE; HUMANS; MALE; MEMORY; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PHOSPHORYLATION; RADIONUCLIDE IMAGING; TAU PROTEINS;

EID: 84928982200     PISSN: 08944105     EISSN: 19311559     Source Type: Journal    
DOI: 10.1037/neu0000133     Document Type: Article

References (71)

1. Aizenstein, H. J., Nebes, R. D., Saxton, J. A., Price, J. C., Mathis, C. A., Tsopelas, N. D., . . . Klunk, W. E. (2008). Frequent amyloid deposition without significant cognitive impairment among the elderly. Archives of Neurology, 65, 1509-1517. doi:10.1001/archneur.65.11.1509
2. Armitage, S. G. (1946). An analysis of certain psychological tests used in evaluation of brain injury. Psychological Monographs: General and Applied, 60, 1-48. doi:10.1037/h0093567
3. Balota, D. A., Burgess, G. C., Cortese, M. J., & Adams, D. R. (2002). The word-frequency mirror effect in young, old, and early-stage Alzheimer's disease: Evidence for two processes in episodic recognition. Journal of Memory and Language, 46, 199-226. doi:10.1006/jmla.2001.2803
4. Balota, D. A., & Duchek, J. M. (1991). Semantic priming effects, lexical repetition effects, and contextual disambiguation effects in healthy aged individuals and individuals with senile dementia of the Alzheimer type. Brain and Language, 40, 181-201. doi:10.1016/0093-934X(91)90124-J
5. Balota, D. A., & Faust, M. (2001). Attention in dementia of the Alzheimer's type. Handbook of Neuropsychology, 6, 51-80.
6. Balota, D. A., Tse, C. S., Hutchison, K. A., Spieler, D. H., Duchek, J. M., & Morris, J. C. (2010). Predicting conversion to dementia of the Alzheimer's type in a healthy control sample: The power of errors in Stroop color naming. Psychology and Aging, 25, 208-218. doi:10.1037/a0017474
7. Balota, D. A., Watson, J. M., Duchek, J. M., & Ferraro, F. R. (1999). Cross-modal semantic and homograph priming in healthy young, healthy old, and in Alzheimer's disease individuals. Journal of the International Neuropsychological Society, 5, 626-640. doi:10.1017/S1355617799577060
8. Berg, L., McKeel, D. W., Miller, J. P., Storandt, M., Rubin, E. H., Morris, J. C., . . . Saunders, A. M. (1998). Clinicopathologic studies in cognitively healthy aging and Alzheimer disease: Relation of histologic markers to dementia severity, age, sex, and Apolipoprotein E genotype. Archives of Neurology, 55, 326-335. doi:10.1001/archneur.55.3.326
9. Blacker, D., Haines, J. L., Rodes, L., Terwedow, H., Go, R. C. P., Harrell, L. E., . . . Tanzi, R. (1997). ApoE-4 and age at onset of Alzheimer's disease: The NIMH Genetics Initiative. Neurology, 48, 139-147. doi: 10.1212/WNL.48.1.139
10. Canning, S. J. D., Leach, L., Stuss, D., Ngo, L., & Black, S. E. (2004). Diagnostic utility of abbreviated fluency measures in Alzheimer disease and vascular dementia. Neurology, 62, 556-562. doi:10.1212/WNL.62.4.556
11. Diniz, B. S. O., Pinto Jr., J. A., & Forlenza, O. V. (2008). Do CSF total tau, phosphorylated tau, and β-amyloid 42 help to predict progression of mild cognitive impairment to Alzheimer's disease? A systematic review and meta-analysis of the literature. World Journal of Biological Psychiatry, 9, 172-182. doi:10.1080/15622970701535502
12. Doraiswamy, P. M., Sperling, R. A., Coleman, R. E., Johnson, K. A., Reiman, E. M., Davis, M. D., . . . Pontecorvo, M. J. (2012). Amyloidassessed by florbetapir F 18 PET and 18-month cognitive decline: A multicenter study. Neurology, 79, 1636-1644. doi:10.1212/WNL.0b013e3182661f74
13. Duchek, J. M., Balota, D. A., Thomas, J. B., Snyder, A. Z., Rich, P., Benzinger, T. L., . . . Ances, B. M. (2013). Relationship between Stroop performance and resting state functional connectivity in cognitively normal older adults. Neuropsychology, 27, 516-528. doi:10.1037/a0033402
14. Duchek, J. M., Balota, D. A., Tse, C. S., Holtzman, D. M., Fagan, A. M., & Goate, A. M. (2009). The utility of intraindividual variability in selective attention tasks as an early marker for Alzheimer's disease. Neuropsychology, 23, 746-758. doi:10.1037/a0016583
15. Fagan, A. M., Mintun, M. A., Shah, A. R., Aldea, P., Roe, C. M., Mach, R. H., . . . Holtzman, D. M. (2009). Cerebrospinal fluid tau and p-tau181 increase with cortical amyloid deposition in cognitively normal individuals: Implications for future clinical trials of Alzheimer's disease. EMBO Molecular Medicine, 1, 371-380. doi:10.1002/emmm.200900048
16. Fagan, A. M., Roe, C. M., Xiong, C., Mintun, M. A., Morris, J. C., & Holtzman, D. M. (2007). Cerebrospinal fluid tau/beta-amyloid42 ratio as a prediction of cognitive decline in nondemented older adults. Archives of Neurology, 64, 343-349. doi:10.1001/archneur.64.3.noc60123
17. Faust, M. E., & Balota, D. A. (2007). Inhibition, facilitation, and attentional control in dementia of the Alzheimer's type: The role of unifying principles in cognitive theory development. Inhibition in Cognition, 213-238.
18. Faust, M. E., Balota, D. A., Spieler, D. H., & Ferraro, F. R. (1999). Individual differences in information-processing rate and amount: Implications for group differences in response latency. Psychological Bulletin, 125, 777-799. doi:10.1037/0033-2909.125.6.777
19. Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). "Mini-mental state": A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189-198. doi: 10.1016/0022-3956(75)90026-6
20. Goodglass, H., & Kaplan, E. (1983). Boston Diagnostic Aphasia Examination Booklet, III, ORAL EXPRESSION, J. Animal Naming (Fluency in Controlled Association). Philadelphia: Lea & Febiger.
21. Grober, E., Buschke, H., Crystal, H., Bang, S., & Dresner, R. (1988). Screening for dementia by memory testing. Neurology, 38, 900-903. doi:10.1212/WNL.38.6.900
22. Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York, NY: Guilford Press.
23. Hedden, T., OH, H., Younger, A. P., & Patel, T. A. (2013). Meta-analysis of amyloid-cognition relations in cognitively normal older adults. Neurology, 80, 1341-1348. doi:10.1212/WNL.0b013e31828ab35d
24. Hodges, J. R., Salmon, D. P., & Butters, N. (1992). Semantic memory impairment in Alzheimer's disease: Failure of access or degraded knowledge? Neuropsychologia, 30, 301-314. doi:10.1016/0028-3932(92)90104-T
25. Hutchison, K. A., Balota, D. A., & Duchek, J. M. (2010). The utility of Stroop task switching as a marker for early-stage Alzheimer's disease. Psychology and Aging, 25, 545-559. doi:10.1037/a0018498
26. Jack, C. R., Lowe, V. J., Senjem, M. L., Weigand, S. D., Kemp, B. J., Shiung, M. M., . . . Peterson, R. C. (2008). 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain: A Journal of Neurology, 131, 665-680. doi:10.1093/brain/awm336
27. Jacoby, L. L. (1999). Ironic effects of repetition: Measuring age-related differences in memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 25, 3-22. doi:10.1037/0278-7393.25.1.3
28. Jagust, W. J., Landau, S. M., Shaw, L. M., Trojanowski, J. Q., Koeppe, R. A., Reiman, E. M., . . . Mathis, C. A. (2009). Relationships between biomarkers in aging and dementia. Neurology, 73, 1193-1199. doi: 10.1212/WNL.0b013e3181bc010c
29. Kirshner, H. S., Webb, W. G., & Kelly, M. P. (1984). The naming disorder of dementia. Neuropsychologia, 22, 23-30. doi:10.1016/0028-3932(84)90004-6
30. Klunk, W. E., Engler, H., Nordberg, A., Wang, Y., Blomqvist, G., Holt, D. P., . . . Langstrom, B. (2004). Imaging brain amyloid in Alzheimer's disease with Pittsburgh compound-B. Annals of Neurology, 55, 306-319. doi:10.1002/ana.20009
31. Logan, J., Fowler, J. S., Volkow, N. D., Wang, G.-J., Ding, Y.-S., & Alexoff, D. L. (1996). Distribution volume ratios without blood sampling from graphical analysis of PET data. Journal of Cerebral Blood Flow & Metabolism: Clinical and Experimental, 16, 834-840. doi: 10.1097/00004647-199609000-00008
32. MacDonald, A. W., Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 1835-1838. doi:10.1126/science.288.5472.1835
33. MacLeod, C. M. (1991). Half a century of research on the Stroop effect: An integrative review. Psychological Bulletin, 109, 163-203. doi:10.1037/0033-2909.109.2.163
34. Marczinski, C. A., & Kertesz, A. (2006). Category and letter fluency in semantic dementia, primary progressive aphasia, and Alzheimer's disease. Brain and Language, 97, 258-265. doi:10.1016/j.bandl.2005.11.001
35. Mattsson, N., Andreasson, U., Persson, S., Arai, H., Batish, S. D., Bernardini, S., . . . Blennow, K. (2011). The Alzheimer's Association external quality control program for cerebrospinal fluid biomarkers. Alzheimer's & Dementia, 7, 386-395e6. doi:10.1016/j.jalz.2011.05.2243
36. Mintun, M. A., LaRossa, G. N., Sheline, Y. I., Dence, C. S., Lee, S. Y., Mach, R. H., . . . Morris, J. C. (2006). [11C]PIB in a nondemented population: Potential antecedent marker of Alzheimer disease. Neurology, 67, 446-452. doi:10.1212/01.wnl.0000228230.26044.a4
37. Mormino, E. C., Kluth, J. T., Madison, C. M., Rabinovici, G. D., Baker, S. L., Miller, B. L., . . . Jagust, W. J. (2009). Episodic memory loss is related to hippocampal-mediated β-amyloid deposition in elderly subjects. Brain: A Journal of Neurology, 132, 1310-1323. doi:10.1093/brain/awn320
38. Morris, J. C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43, 2412-2414. doi:10.1212/WNL.43.11.2412-a
39. Morris, J. C., Blennow, K., Froelich, L., Nordberg, A., Soininen, H., Waldemar, G., . . . Dubois, B. (2014). Harmonized diagnostic criteria for Alzheimer's disease: Recommendations. Journal of Internal Medicine, 275, 204-213. doi:10.1111/joim.12199
40. Morris, J. C., Roe, C. M., Xiong, C., Fagan, A. M., Goate, A. M., Holtzman, D. M., & Mintun, M. A. (2010). APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Annals of Neurology, 67, 122-131. doi:10.1002/ana.21843
41. Morris, J. C., Storandt, M., McKeel Jr., D. W., Rubin, E. H., Price, J. L., Grant, E. A., & Berg, L. (1996). Cerebral amyloid deposition and diffuse plaques in "normal" aging Evidence for presymptomatic and very mild Alzheimer's disease. Neurology, 46, 707-719. doi:10.1212/WNL.46.3.707
42. Mungas, D., Tractenberg, R., Schneider, J. A., Crane, P. K., & Bennett, D. A. (2014). A 2-process model for neuropathology of Alzheimer's disease. Neurobiology of Aging, 35, 301-308. doi:10.1016/j.neurobiolaging.2013.08.007
43. Nebes, R. D., Snitz, B. E., Cohen, A. D., Aizenstein, H. J., Saxton, J. A., Halligan, E. M., . . . Klunk, W. E. (2013). Cognitive aging in persons with minimal amyloid-β and white matter hyperintensities. Neuropsychologia, 51, 2202-2209. doi:10.1016/j.neuropsychologia.2013.07.017
44. Nelson, D. L., McEvoy, C. L., & Schreiber, T. A. (2004). The University of South Florida free association, rhyme, and word fragment norms. Behavior Research Methods, Instruments & Computers, 36, 402-407. doi:10.3758/BF03195588
45. Perry, R. J., & Hodges, J. R. (1999). Attention and executive deficits in Alzheimer's disease: A critical review. Brain: A Journal of Neurology, 122, 383-404. doi:10.1093/brain/122.3.383
46. Pike, K. E., Ellis, K. A., Villemagne, V. L., Good, N., Chételat, G., Ames, D., . . . Rowe, C. C. (2011). Cognition and beta-amyloid in preclinical Alzheimer's disease: Data from the AIBL study. Neuropsychologia, 49, 2384-2390. doi:10.1016/j.neuropsychologia.2011.04.012
47. Price, J. L., McKeel, Jr., D. W., Buckles, V. D., Roe, C. M., Xiong, C., Grundman, M., . . . Morris, J. C. (2009). Neuropathology of nondemented aging: Presumptive evidence for preclinical Alzheimer disease. Neurobiology of Aging, 30, 1026-1036. doi:10.1016/j.neurobiolaging .2009.04.002
48. Reiman, E. M., Chen, K., Liu, X., Bandy, D., Yu, M., Lee, W., . . . Caselli, R. J. (2009). Fibrillar amyloid-β burden in cognitively normal people at 3 levels of genetic risk for Alzheimer's disease. Proceedings of the National Academy of Sciences, USA, 106, 6820-6825.
49. Rodrigue, K. M., Kennedy, K. M., Devous, M. D., Rieck, J. R., Hebrank, A. C., Diaz-Arrastia, R., . . . Park, D. C. (2012). β-Amyloid burden in healthy aging regional distribution and cognitive consequences. Neurology, 78, 387-395. doi:10.1212/WNL.0b013e318245d295
50. Roe, C. M., Fagan, A. M., Grant, E. A., Hassenstab, J., Moulder, K. L., Dreyfus, D. M., . . . Morris, J. C. (2013). Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later. Neurology, 80, 1784-1791. doi:10.1212/WNL.0b013e3182918ca6
51. Rogers, T. T., Hocking, J., Noppeney, U., Mechelli, A., Gorno-Tempini, M. L., Patterson, K., & Price, C. J. (2006). Anterior temporal cortex and semantic memory: Reconciling findings from neuropsychology and functional imaging. Cognitive, Affective & Behavioral Neuroscience, 6, 201-213. doi:10.3758/CABN.6.3.201
52. Small, B. J., Rosnick, C. B., Fratiglioni, L., & Bäckman, L. (2004). Apolipoprotein E and cognitive performance: A meta-analysis. Psychology and Aging, 19, 592-600. doi:10.1037/0882-7974.19.4.592
53. Smith, E. E., Shoben, E. J., & Rips, L. J. (1974). Structure and process in semantic memory: A featural model for semantic decisions. Psychological Review, 81, 214-241. doi:10.1037/h0036351
54. Soldan, A., Pettigrew, C., Li, S., Wang, M.-C., Moghekar, A., Selnes, O. A., . . . O'Brien, R. (2013). Relationship of cognitive reserve and cerebrospinal fluid biomarkers to the emergence of clinical symptoms in preclinical Alzheimer's disease. Neurobiology of Aging, 34, 2827-2834. doi:10.1016/j.neurobiolaging.2013.06.017
55. Sperling, R. A., Johnson, K. A., Doraiswamy, P. M., Reiman, E. M., Fleisher, A. S., Sabbagh, M. N., . . . Pontecorvo, M. J. (2013). Amyloid deposition detected with florbetapir F 18 (18F-AV-45) is related to lower episodic memory performance in clinically normal older individuals. Neurobiology of Aging, 34, 822-831. doi:10.1016/j.neurobiolaging .2012.06.014
56. Spieler, D. H., Balota, D. A., & Faust, M. E. (1996). Stroop performance in healthy younger and older adults and in individuals with dementia of the Alzheimer's type. Journal of Experimental Psychology: Human Perception and Performance, 22, 461-479. doi:10.1037/0096-1523.22.2.461
57. Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47, 2015-2028. doi:10.1016/j.neuropsychologia.2009.03.004
58. Storandt, M., Balota, D. A., Aschenbrenner, A. J., & Morris, J. C. (2014). Clinical and psychological characteristics of the initial cohort of the Dominantly Inherited Alzheimer Network (DIAN). Neuropsychology, 28, 19-29. doi:10.1037/neu0000030
59. Storandt, M., Grant, E. A., Miller, J. P., & Morris, J. C. (2006). Longitudinal course and neuropathologic outcomes in original vs. revised MCI and in pre-MCI. Neurology, 67, 467-473.
60. Storandt, M., Head, D., Fagan, A. M., Holtzman, D. M., & Morris, J. C. (2012). Toward a multifactorial model of Alzheimer disease. Neurobiology of Aging, 33, 2262-2271. doi:10.1016/j.neurobiolaging.2011.11.029
61. Storandt, M., Mintun, M. A., Head, D., & Morris, J. C. (2009). Cognitive decline and brain volume loss as signatures of cerebral amyloid-βpeptide deposition identified with Pittsburgh compound B. Archives of Neurology, 66, 1476-1481. doi:10.1001/archneurol.2009.272
62. Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643-662. doi:10.1037/h0054651
63. Su, Y., D'Angelo, G. M., Vlassenko, A. G., Zhou, G., Snyder, A. Z., Marcus, D. S., . . . Benzinger, T. L. S. (2013). Quantitative analysis of PiB-PET with FreeSurfer ROIs. PLoS ONE, 8(11), e73377. doi:10.1371/journal.pone.0073377
64. Tse, C. S., Balota, D. A., Moynan, S. C., Duchek, J. M., & Jacoby, L. L. (2010). The utility of placing recollection in opposition to familiarity in early discrimination of healthy aging and very mild dementia of the Alzheimer's type. Neuropsychology, 24, 49-67. doi:10.1037/a0014887
65. Tse, C. S., Balota, D. A., Yap, M. J., Duchek, J. M., & McCabe, D. P. (2010). Effects of healthy aging and early stage dementia of the Alzheimer's type on components of response time distributions. Neuropsychology, 24, 300-315. doi:10.1037/a0018274
66. Twamley, E. W., Ropacki, S. A. L., & Bondi, M. W. (2006). Neuropsychological and neuroimaging changes in preclinical Alzheimer's disease. Journal of the International Neuropsychological Society, 12, 707-735. doi:10.1017/S1355617706060863
67. Van Overschelde, J. P., Rawson, K. A., & Dunlosky, J. (2004). Category norms: An updated and expanded version of the Battig and Montague (1969) norms. Journal of Memory and Language, 50, 289-335. doi: 10.1016/j.jml.2003.10.003
68. Vemuri, P., Weigand, S. D., Przybelski, S. A., Knopman, D. S., Smith, G. E., Trojanowski, J. Q., . . . Jack, C. R. (2011). Cognitive reserve and Alzheimer's disease biomarkers are independent determinants of cognition. Brain: A Journal of Neurology, 134, 1479-1492. doi:10.1093/brain/awr049
69. Vemuri, P., Wiste, H. J., Weigand, S. D., Shaw, L. M., Trojanowski, J. Q., Weiner, M. W., . . . Jack, C. R. (2009). MRI and CSF biomarkers in normal, MCI, and AD subjects: Diagnostic discrimination and cognitive correlations. Neurology, 73, 287-293. doi:10.1212/WNL.0b013e 3181af79e5
70. Wechsler, D. (1997). WAIS-III administration and scoring manual. San Antionio, TX: Psychological Corporation.
71. 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. doi:10.1016/j.neurobiolaging .2009.02.003