Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-24T03:07:17.042Z Has data issue: false hasContentIssue false

Context-specific memory and apolipoprotein E (ApoE) ε4: Cognitive evidence from the NIMH prospective study of risk for Alzheimer's disease

Published online by Cambridge University Press:  01 May 2004

JAMES A. LEVY
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
JUDY BERGESON
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
KAREN PUTNAM
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
VIRGINIA ROSEN
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
ROBERT COHEN
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
FRANCOIS LALONDE
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
NADEEM MIRZA
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
GARY LINKER
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
TREY SUNDERLAND
Affiliation:
Geriatric Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland

Abstract

The aim of the study was to determine whether the ε4 allele of the apolipoprotein E (ApoE) gene was associated primarily with context-specific memory among individuals at genetic risk for developing Alzheimer's disease. The effect of ApoE status on comprehensive neuropsychological results was examined in 176 healthy adults during baseline cognitive testing in the NIMH Prospective Study of Biomarkers for Older Controls at Risk for Alzheimer's Disease (NIMH Prospective BIOCARD Study). The presence of the ε4 allele was associated with significantly lower total scores on the Logical Memory II subtest of the Wechsler Memory Scale–Revised and percent of information retained after delay. Further analysis indicated the prose recall and retention effect was partially explained by a small subgroup of ε4 homozygotes, suggesting a gradually progressive process that may be presaged with specific cognitive measures. The current results may represent an ε4-associated breakdown between gist-related information and context-bound veridical recall. This relative disconnection may be understood in light of putative ε4-related preclinical accumulation of Alzheimer pathology (tangles and plaques) in the entorhinal cortex (EC) and among frontal networks, as well as the possibility of less-efficient compensatory strategies. (JINS, 2004, 10, 362–370.)

Type
Research Article
Copyright
© 2004 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albert, M.S., Moss, M.B., Tanzi, R., & Jones, K. (2001). Preclinical prediction of AD using neuropsychological tests. Journal of the International Neuropsychological Society, 7, 631639.Google Scholar
Arnaiz, E., Jelic, V., Almkvist, O., Wahlund, L.-O., Winblad, B., Valind, S., & Nordberg, A. (2001). Impaired cerebral glucose metabolism and cognitive functioning predict deterioration in mild cognitive impairment. NeuroReport, 12, 851855.Google Scholar
Backman, L. & Small, B.J. (1998). Influences of cognitive support on episodic remembering: Tracing the process of loss from normal aging to Alzheimer's disease. Psychology and Aging, 13, 267276.Google Scholar
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, 626640.Google Scholar
Batting, W.F. & Montague, W.E. (1969). Category norms for verbal items in 56 categories: A replication and extension of the Connecticut category norms. Journal of Experimental Psychology Monograph, 80, 146.Google Scholar
Berr, C., Dufouil, C., Brousseau, T., Richard, F., Amouyel, P., Marceteau, E., & Alperovitch, A. (1996). Early effect of ApoE-E4 allele on cognitive results in a group of highly performing subjects: The EVA study. Neuroscience Letters, 218, 912.Google Scholar
Blacker, D., Haines, J.L., Rodes, L., Terwedow, H., Go, R.C.P., Harrell, L.E., Perry, R.T., Bassett, S.S., Chase, G., Meyers, D., Albert, M.S., & Tanzi, R. (1997). ApoE–4 and age of onset of Alzheimer's disease: The NIMH genetics initiative. Neurology, 48, 139147.Google Scholar
Blair, J.R. & Spreen, O. (1989). Predicting premorbid IQ: A revision of the National Adult Reading Test. Clinical Neuropsychologist, 3, 129136.Google Scholar
Bondi, M.W., Salmon, D.P., Monsch, A.U., Galasko, D., Butters, N., Klauber, M.R., Thal, L.J., & Saitoh, T. (1995). Episodic memory changes are associated with the APOE-E4 allele in nondemented older adults. Neurology, 45, 22032206.Google Scholar
Bondi, M.W., Salmon, D.P., Galasko, D., Thomas, R.G., & Thal, L.J. (1999). Neuropsychological function and apolipoprotein E genotype in the preclinical detection of Alzheimer's disease. Psychology and Aging, 14, 295303.CrossRefGoogle Scholar
Bondi, M.W., Lange, K.L., Salmon, D.P., & Delis, D.C. (2003). Verbal memory during the preclinical period of Alzheimer's disease: Influence of APOE genotype. Journal of the International Neuropsychological Society, 9, 153.Google Scholar
Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J., & Small, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. New England Journal of Medicine, 343, 450456.Google Scholar
Bozoki, A., Giordani, B., Heidebrink, J.L., Berent, S., & Foster, N.L. (2001). Mild cognitive impairments predict dementia in nondemented elderly patients with memory loss. Archives of Neurology, 58, 411416.Google Scholar
Braak, H. & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82, 239259.Google Scholar
Brainerd, C.J. & Reyna, V.F. (1990). Gist is the grist: Fuzzy-trace theory and the intuitionism. Developmental Review, 10, 347.Google Scholar
Budson, A.E., Daffner, K.R., Desikan, R., & Schacter, D.L. (2000). When false recognition is unopposed by true recognition: Gist-based memory distortion in Alzheimer's disease. Neuropsychology, 14, 277287.Google Scholar
Buschke, H. (1973). Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12, 4350.Google Scholar
Caselli, R.J., Graff-Radford, N.R., Reiman, E.M., Weaver, A., Osborne, D., Lucas, J., Uecker, A., & Thibodeau, S.N. (1999). Preclinical memory decline in cognitively normal apolipoprotein E-E4 homozygotes. Neurology, 53, 201207.CrossRefGoogle Scholar
Caselli, R.J., Osborne, D., Reiman, E.M., Hentz, J.G., Barbieri, C.J., Saunders, A.M., Hardy, J., Graff-Radford, N.R., Hall, G.R., & Alexander, G.E. (2001). Preclinical cognitive decline in late middle-aged asymptomatic apolipoprotein E-e4/4 homozygotes: A replication study. Journal of the Neurological Sciences, 189, 9398.Google Scholar
Chen, J.G., Edwards, C.L., Vidyarthi, S., Pitchumoni, S., Tabrizi, S., Barboriak, D., Charles, H.C., & Doraiswamy, P.M. (2002). Learning and recall in subjects at genetic risk for Alzheimer's disease. Journal of Neuropsychiatry and Clinical Neurosciences, 14, 5863.Google Scholar
Chen, P., Ratcliff, G., Belle, S.H., Cauley, J.A., DeKosky, S.T., & Ganguli, M. (2001). Patterns of cognitive decline in presymptomatic Alzheimer disease. Archives of General Psychiatry, 58, 853858.Google Scholar
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. (1993). Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science, 261, 921923.CrossRefGoogle Scholar
de Leon, M.J., Convit, A., Wolf, O.T., Tarshish, C.Y., DeSanti, S., Rusinek, H., Tsai, W., Kandil, E., Scherer, A.J., Roche, A., Imossi, A., Thorn, E., Bobinski, M., Caraos, C., Lesbre, P., Schlyer, D., Poirier, J., Reisberg, B., & Fowler, J. (2001). Prediction of cognitive decline in normal elderly subjects with 2-[18F]fluoro-2-deoxy-D-glucose/positron-emission tomography (FDG/PET). Proceedings of the National Academy of Sciences, 98, 1096610971.Google Scholar
De Santi, S., de Leon, M.J., Rusinek, H., Convit, A., Tarshish, C.Y., Roche, A., Tsai, W.H., Kandil, E., Boppana, M., Daisley, K., Wang, G.J., Schlyer, R., & Fowler, J. (2001). Hippocampal formation glucose metabolism and volume losses in MCI and AD. Neurobiology of Aging, 22, 529539.CrossRefGoogle Scholar
Dik, M.G., Jonker, C., Bouter, L.M., Geerlings, M.I., van Kamp, G.J., & Deeg, D.J.H. (2000). APOE-E4 is associated with memory decline in cognitively impaired elderly. Neurology, 54, 14921497.CrossRefGoogle Scholar
Elias, M.F., Beiser, A., Wolf, P.A., Au., R., White, R.F., & D'Agostino, R.B. (2000). The preclinical phase of Alzheimer disease: A 22-year prospective of the Framingham cohort. Archives of Neurology, 57, 808813.Google Scholar
Farrer, L.A., Cupples, A., Haines, J.L., Hyman, B., Kukull, W.A., Mayeux, R., Myers, R.H., Pericak-Vance, M.A., Risch, N., & van Duijn, C.M. (1997). Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. Journal of the American Medical Association, 278, 13491356.Google Scholar
Fernandez, G., Brewer, J.B., Zhao, Z., Glover, G.H., & Gabrieli, J.D.E. (1999). Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: A functional magnetic resonance imaging study with high acquisition rate. Hippocampus, 9, 3544.Google Scholar
Frank, L.M., Brown, E.N., & Wilson, M. (2000). Trajectory encoding in the hippocampus and entorhinal cortex. Neuron, 27, 169178.Google Scholar
Ghebremedhin, E., Schultz, C., Braak, E., & Braak, H. (1998). High frequency of apolipoprotein E E4 allele in young individuals with very mild Alzheimer's disease-related neurofibrillary changes. Experimental Neurology, 153, 152155.Google Scholar
Gilsky, E.L., Rubin, S.R., & Davidson, P.S.R. (2001). Source memory in older adults: An encoding or retrieval problem? Journal of Experimental Psychology: Learning, Memory, and Cognition, 27, 11311146.Google Scholar
Gomez-Isla, T., Price, J.L., McKeel Jr., D.W., Morris, J.C., Growdon, J.H., & Hyman, B.T. (1996). Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. Journal of Neuroscience, 16, 44914500.Google Scholar
Greenwood, P.M., Sunderland, T., Friz, J.L., & Parasuraman, R. (2000). Genetics and visual attention: Selective deficits in healthy adult carriers of the E4 allele of the apolipoprotein E gene. Proceedings of the National Academy of Sciences, 97, 1166111666.Google Scholar
Haist, F., Gore, J.B., & Mao, H. (2001). Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nature Neuroscience, 4, 11391145.Google Scholar
Helkala, E.-L., Kovisto, K., Hanninen, T., Vanhanen, M., Kervinen, K., Kuusisto, J., Mykkanen, L., Kesaniemi, Y.A., Laakso, M., & Riekkinen, P., Sr. (1995). The association of apolipoprotein E polymorphism with memory: A population based study. Neuroscience Letters, 191, 141144.Google Scholar
Helkala, E.-L., Kovisto, K., Hanninen, T., Vanhanen, M., Kervinen, K., Kuusisto, J., Mykkanen, L., Kesaniemi, Y.A., Laakso, M., & Riekkinan, P., Sr. (1996). Memory functions in human subjects with different apolipoprotein E phenotypes during a 3-year population-based follow-up study. Neuroscience Letters, 204, 177180.Google Scholar
Howieson, D.B., Dame, A., Camicioli, R., Sexton, G., Payami, H., & Kaye, J.A. (1997). Cognitive markers preceding Alzheimer's dementia in the healthy oldest old. Journal of the American Geriatric Society, 45, 584589.Google Scholar
Hyman, B.T., Van Hoesen, G.W., Damasio, A.R., & Barnes, C.L. (1984). Alzheimer's disease: Cell-specific pathology isolates the hippocampal formation. Science, 14, 11681170.Google Scholar
Hyman, B.T., Van Hoesen, G.W., Kromer, L.J., & Damasio, A.R. (1986). Preforant pathway changes and the memory impairment of Alzheimer's disease. Annals of Neurology, 20, 472481.CrossRefGoogle Scholar
Janowsky, J.S., Shimamura, A.P., & Squire, L.R. (1989). Source memory impairment in patients with frontal lobe lesions. Neuropsychologia, 27, 10431056Google Scholar
Johnson, D.K., Storandt, M., & Balota, D.A. (2003). A discourse analysis of logical memory recall in normal aging and dementia of the Alzheimer type. Neuropsychology, 17, 8292.Google Scholar
Juottonen, K., Lehtovirta, M., Helisalmi, S., Riekkinen, P.J., & Soininen, H. (1998). Major decrease in the volume of the entorhinal cortex in patients with Alzheimer's disease carrying the apolipoprotein E E4 allele. Journal of Neurology, Neurosurgery, and Psychiatry, 65, 322327.Google Scholar
Kantarci, K., Smith, G.E., Ivnik, R.J., Petersen, R.C., Boeve, B.F., Knopman, D.S., Tangalos, E.G., & Jack, C.R., Jr. (2002). 1H magnetic resonance spectroscopy, cognitive function, and apolipoprotein E genotype in normal aging, mild cognitive impairment and Alzheimer's disease. Journal of the International Neuropsychological Society, 8, 934942.Google Scholar
Kaplan, E.F., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test. Philadelphia, Pennsylvania: Lea & Febiger.
Killiany, R.J., Gomez-Isla, T., Moss, M., Kikinis, R., Sandor, T., Jolesz, F., Tanzi, R., Jones, K., Hyman, B.T., & Albert, M.S. (2000). Use of structural magnetic resonance imaging to predict who will get Alzheimer's disease. Annals of Neurology, 47, 430439.Google Scholar
Killiany, R.J., Hyman, B.T., Gomez-Isla, T., Moss, M.B., Kikinis, R., Jolesz, F., Tanzi, R., Jones, K., & Albert, M.S. (2002). MRI measures of entorhinal cortex vs. hippocampus in preclinical AD. Neurology, 58, 11881196.Google Scholar
Kordower, J.H., Chu, Y., Stebbins, G.T., DeKoksy, S.T., Cochran, E.J., Bennett, D., & Mufson, E.J. (2001). Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Annals of Neurology, 49, 202213.Google Scholar
Lange, K.L., Bondi, M.W., Salmon, D.P., Galasko, D., Delis, D.C., Thomas, R.G., & Thal, L.J. (2002). Decline in verbal memory during preclinical Alzheimer's disease: Examination of the effect of APOE genotype. Journal of the International Neuropsychological Society, 8, 943955.Google Scholar
Linn, R.T., Wolf, P.A., Bachman, D.L., Knoefel, J.E., Cobb, J.L., Belanger, A.J., Kaplan, E.F., & D'Agostino, R.B. (1995). The ‘preclinical phase’ of probable Alzheimer's disease: A 13-year prospective study of the Framingham cohort. Archives of Neurology, 52, 485490.Google Scholar
Marquis, S., Moore, M.M., Howieson, D.B., Sexton, G., Payami, H., Kaye, J.A., & Camicioli, R. (2002). Independent predictors of cognitive decline in healthy elderly persons. Archives of Neurology, 59, 601606.CrossRefGoogle Scholar
Mayeux, R., Small, S.A., Tang, M.-X., Tycko, B., & Stern, Y. (2001). Memory performance in healthy elderly without Alzheimer's disease: Effects of time and apolipoprotein-E. Neurobiology of Aging, 22, 683689.Google Scholar
Meyers, J. & Meyers, K. (1995). The Meyers Scoring System for the Rey Complex Figure and the recognition trial: Professional manual. Odessa, Florida: Psychological Assessment Resources.
O'Hara, R., Yesavage, J.A., Kraemer, H.C., Mauricio, M., Friedman, L.F., & Murphy, G.M. (1998). The APOE E4 allele is associated with decline on delayed recall performance in community-dwelling older adults. Journal of the American Geriatric Society, 46, 14931498.Google Scholar
Parasuraman, R., Greenwood, P.M., & Sunderland, T. (2002). The Apolipoprotein E gene, attention, and brain function. Neuropsychology, 16, 254274.Google Scholar
Reiman, E.M., Caselli, R.J., Yun, L.S., Chen, K., Bandy, D., Minoshima, S., Thibodeau, S.N., & Osborne, D. (1996). Preclinical evidence of Alzheimer's disease in persons homozygous for the ε4 allele for apolipoprotein E. New England Journal of Medicine, 334, 752758.Google Scholar
Reiman, E.M., Caselli, R.J., Chen, K., Alexander, G.E., Bandy, D., & Frost, J. (2001). Declining brain activity in cognitively normal apolipoprotein E ε4 heterozygotes: A foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proceedings of the National Academy of Sciences, 98, 33343339.CrossRefGoogle Scholar
Rosen, V.M., Bergeson, J.L., Putnam, K., Harwell, A., & Sunderland, T. (2002). Working memory and apolipoprotein E: What's the connection? Neuropsychologia, 40, 22262233.Google Scholar
Rubin, E.H., Storandt, M., Miller, J.P., Kinscherf, D.A., Grant, E.A., Morris, J.C., & Berg, L. (1998). A prospective study of cognitive function and onset of dementia in cognitively healthy elders. Archives of Neurology, 55, 395401.CrossRefGoogle Scholar
Saunders, A.M., Strittmatter, W.J., Schmechel, D., St. George-Hyslop, P.H., Pericak-Vance, M.A., Joo, S.H., Rosi, B.L., Gusella, J.F., Crapper-MacLachlan, D.R., Alberts, M.J., Hulette, C., Crain, B., Goldgaber, D., & Roses, A.D. (1993). Association of apolipoprotein E allele E4 with late-onset familial and sporadic Alzheimer's disease. Neurology, 43, 14671472.Google Scholar
Schiffman, S.S., Graham, B.G., Sattely-Miller, E.A., Zervakis, J., & Welsh-Bohmer, K. (2002). Taste, smell and neuropsychological performance of individuals at familial risk for Alzheimer's disease. Neurobiology of Aging, 23, 397404.Google Scholar
Schmidt, H., Schmidt, R., Fazekas, F., Semmler, J., Kapeller, P., Reinhart, B., & Kostner, G.M. (1996). Apolipoprotein E E4 allele in the normal elderly: Neuropsychologic and brain MRI correlates. Clinical Genetics, 50, 293299.Google Scholar
Simon, E., Leach, L., Winocur, G., & Moscovitch, M. (1994). Intact primary memory in mild to moderate Alzheimer disease: Indices from the California Verbal Learning Test. Journal of Clinical and Experimental Neuropsychology, 16, 414422.Google Scholar
Small, B.J., Basun, H., & Backman, L. (1998). Three-year changes in cognitive performance as a function of apolipoprotein E genotype: Evidence from very old adults without dementia. Psychology and Aging, 13, 8087.Google Scholar
Small, B.J., Dixon, R.A., Hultsch, D.F., & Hertzog, C. (1999). Longitudinal changes in quantitative and qualitative indicators of word and story recall in young-old and old-old adults. Journal of Gerontology: Psychological Sciences, 54B, P107P115.Google Scholar
Small, B.J., Graves, A.B., McEvoy, C.L., Crawford, F.C., Mullan, M., & Mortimer, J.A. (2000). Is APOE-ε4 a risk factor for cognitive impairment in normal aging? Neurology, 54, 20822088.Google Scholar
Small, B.J., Rosnick, C., Fratiglioni, L., & Backman, L. (2003). Apolipoprotein E genotype and cognitive performance in normal aging: A quantitative review. Journal of the International Neuropsychological Society, 9, 153.Google Scholar
Small, G.W., Ercoli, L.M., Silverman, D.H.S., Huang, S.-C., Komo, S., Bookheimer, S.Y., Lavrotsky, H., Miller, K., Siddarth, P., Rasgon, N.L., Mazziotta, J.C., Saxena, S., Wu, H.M., Mega, M.S., Cummings, J.L., Saunders, A.M., Pericak-Vance, M.A., Roses, A.D., Barrio, J.R., & Phelps, M.E. (2000). Cerebral metabolic and cognitive decline in persons at genetic risk for Alzheimer's disease. Proceedings of the National Academy of Sciences, 97, 60376042.Google Scholar
Smith, C.D., Anderson, A.H., Kryscio, R.J., Schmitt, F.A., Kindy, M.S., Blonder, L.X., & Avison, M.J. (1999). Altered brain activation in cognitively intact individuals at high risk for Alzheimer's disease. Neurology, 53, 13911396.Google Scholar
Smith, G.E., Bohac, D.L., Waring, S.C., Kokmen, E., Tangalos, E.G., Ivnik, R.J., & Petersen, R.C. (1998). Apolipoprotein E genotype influences cognitive ‘phenotype’ in patients with Alzheimer's disease but not in healthy control subjects. Neurology, 50, 355362.Google Scholar
Smith, J.A. & Knight, R.G. (2002). Memory processing in Alzheimer's disease. Neuropsychologia, 40, 666682.Google Scholar
Spencer, W.D. & Raz, N. (1995). Differential effects of aging on memory for content and context: A meta-analysis. Psychology and Aging, 10, 527539.Google Scholar
Storandt, M. & Hill, R.D. (1989). Very mild senile dementia of the Alzheimer type: II. Psychometric test performance. Archives of Neurology, 46, 383386.Google Scholar
Storandt, M., Botwinick, J., Danzinger, W.L., Berg, L., & Hughes, C.P. (1984). Psychometric differentiation of mild senile dementia of the Alzheimer type. Archives of Neurology, 41, 477499.Google Scholar
Strittmatter, W.J., Saunders, A.M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G.S., & Roses, A.D. (1993). Apolipoprotein E: High-avidity binding to B-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proceedings of the National Academy of Sciences, 90, 19771981.Google Scholar
Suzuki, W.A., Miller, E.K., & Desimone, R. (1997). Object and place memory in the macaque entorhinal cortex. Journal of Neurophysiology, 78, 10621081.Google Scholar
Tierney, M.C., Szalai, J.P., Snow, W.G., Fisher, R.H., Tsuda, T., Chi, H., MacLachlan, D.R., & St. George-Hyslop, P.H. (1996). A prospective study of the clinical utility of ApoE genotype in the prediction of outcome in patients with memory impairment. Neurology, 46, 149154.Google Scholar
Tun, P.A., Wingfield, A., Rosen, M.J., & Blanchard, C. (1998). Response latencies for false memories: Gist-based processes in normal aging. Psychology and Aging, 13, 230241.CrossRefGoogle Scholar
Van Petten, C., Senkfor, A.J., & Newberg, W.M. (2000). Memory for drawings in locations: Spatial source memory and event-related potentials. Psychophysiology, 37, 551564.Google Scholar
Wechsler, D. (1981). Wechsler Adult Intelligence Scale–Revised: Manual. New York: Psychological Corporation.
Wechsler, D. (1987). Wechsler Memory Scale–Revised: Manual. New York: Psychological Corporation.
Wilson, R.S., Schneider, J.A., Barnes, L.L., Beckett, L.A., Aggarwal, N.T., Cochran, E.J., Beiry-Kravis, E., Bach, J., Fox, J.H., Evans, D.A., & Bennett, D.A. (2002). The apolipoprotein E E4 allele and decline in different cognitive systems during a 6-year period. Archives of Neurology, 59, 11541160.Google Scholar
Winer, B.J. (1991). Statistical principles in experimental design (3rd ed.). New York: McGraw-Hill.
Wu, Y.-Y., Delgado, R., Costello, R., Sunderland, T., Dukoff, R., & Csako, G. (2000). Quantitative assessment of apolipoprotein E genotypes by image analysis of PCR-RFLP fragments. Clinica Chimica Acta, 293, 213221.CrossRefGoogle Scholar
Yaffe, K., Cauley, J., Sands, L., & Browner, W. (1997). Apolipoprotein E phenotype and cognitive decline in a prospective study of elderly community women. Archives of Neurology, 54, 11101114.Google Scholar