Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T06:59:23.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Machine Learning Amplifies the Effect of Parental Family History of Alzheimer's Disease on List Learning Strategy

Published online by Cambridge University Press:  10 February 2012

Timothy S. Chang ,
Michael H. Coen ,
Asenath La Rue ,
Erin Jonaitis ,
Rebecca L. Koscik ,
Bruce Hermann  and
Mark A. Sager
Timothy S. Chang*
Affiliation:
Department of Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
Michael H. Coen
Affiliation:
Department of Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin Department of Computer Science, University of Wisconsin-Madison, Madison, Wisconsin
Asenath La Rue
Affiliation:
Wisconsin Alzheimer's Institute, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
Erin Jonaitis
Affiliation:
Wisconsin Alzheimer's Institute, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
Rebecca L. Koscik
Affiliation:
Wisconsin Alzheimer's Institute, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
Bruce Hermann
Affiliation:
Wisconsin Alzheimer's Institute, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin Department of Neurology, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
Mark A. Sager
Affiliation:
Wisconsin Alzheimer's Institute, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin Section of Geriatrics and Gerontology, Department of Medicine, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, Wisconsin
*
Correspondence and reprint requests to: Timothy S. Chang, Biostatistics and Medical Informatics, School of Medicine and Public Health, University of Wisconsin-Madison, 6795 Medical Sciences Center, 1300 University Avenue, Madison, WI 53706. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Identification of preclinical Alzheimer's disease (AD) is an essential first step in developing interventions to prevent or delay disease onset. In this study, we examine the hypothesis that deeper analyses of traditional cognitive tests may be useful in identifying subtle but potentially important learning and memory differences in asymptomatic populations that differ in risk for developing Alzheimer's disease. Subjects included 879 asymptomatic higher-risk persons (middle-aged children of parents with AD) and 355 asymptotic lower-risk persons (middle-aged children of parents without AD). All were administered the Rey Auditory Verbal Learning Test at baseline. Using machine learning approaches, we constructed a new measure that exploited finer differences in memory strategy than previous work focused on serial position and subjective organization. The new measure, based on stochastic gradient descent, provides a greater degree of statistical separation (p = 1.44 × 10−5) than previously observed for asymptomatic family history and non-family history groups, while controlling for apolipoprotein epsilon 4, age, gender, and education level. The results of our machine learning approach support analyzing memory strategy in detail to probe potential disease onset. Such distinct differences may be exploited in asymptomatic middle-aged persons as a potential risk factor for AD. (JINS, 2012, 18, 428–439)

Keywords

Cohort studyMemoryNeuropsychological testsPre-symptomatic diseaseStatistical modelsMedical informatics
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 3 , May 2012 , pp. 428 - 439
Copyright
Copyright © The International Neuropsychological Society 2012

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

Bäckman, L., Jones, S., Berger, A.K., Laukka, E.J., Small, B.J. (2005). Cognitive impairment in preclinical Alzheimer's disease: A meta-analysis. Neuropsychology, 19(4), 520–531. doi:10.1037/0894-4105.19.4.520CrossRefGoogle ScholarPubMed
Barnes, D.E., Yaffe, K. (2011). The projected effect of risk factor reduction on Alzheimer's disease prevalence. The Lancet Neurology, 10(9), 819–828. doi:10.1016/S1474-4422(11)70072-2CrossRefGoogle ScholarPubMed
Bassett, S.S., Yousem, D.M., Cristinzio, C., Kusevic, I., Yassa, M.A., Caffo, B.S., Zeger, S.L. (2006). Familial risk for Alzheimer's disease alters fMRI activation patterns. Brain, 129(5), 1229–1239. doi:10.1093/brain/awl089CrossRefGoogle ScholarPubMed
Benton, A.L. (1994). Neuropsychological assessment. Annual Review of Psychology, 45, 1–23. doi:10.1146/annurev.ps.45.020194.000245CrossRefGoogle ScholarPubMed
Bertsekas, D., Nedic, A. (2003). Convex analysis and optimization. Nashua, NH: Athena Scientific.Google Scholar
Bousfield, A.K., Bousfield, W.A. (1966). Measurement of clustering and of sequential constancies in repeated free recall. Psychological Reports, 19(3), 935–942. doi:10.2466/pr0.1966.19.3.935CrossRefGoogle ScholarPubMed
Braak, H., Braak, E. (1990). Alzheimer's disease: Striatal amyloid deposits and neurofibrillary changes. Journal of Neuropathology and Experimental Neurology, 49(3), 215–224. Retrieved from http://journals.lww.com/jneuropath/pages/default.aspxCrossRefGoogle ScholarPubMed
Capitani, E., Della Sala, S., Logie, R.H., Spinnler, H. (1992). Recency, primacy, and memory: Reappraising and standardising the serial position curve. Cortex, 28(3), 315–342. Retrieved from http://www.cortexjournal.net/CrossRefGoogle ScholarPubMed
Carlesimo, G.A., Sabbadini, M., Fadda, L., Caltagirone, C. (1997). Word-list forgetting in young and elderly subjects: Evidence for age-related decline in transferring information from transitory to permanent memory condition. Cortex, 33(1), 155–166. Retrieved from http://www.cortexjournal.net/CrossRefGoogle Scholar
Coen, M.H., Selvaprakash, V., Dassow, A.M., Prudom, S., Colman, R., Kemnitz, J. 2009. Modeling the role of memory function in primate game play. Proceedings of the 38th Annual Conference of the Cognitive Science Society (pp. 2408–2413), Amsterdam, Netherlands. Retrieved from http://csjarchive.cogsci.rpi.edu/proceedings/2009/papers/556/paper556.pdfGoogle Scholar
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Erlbaum.Google Scholar
Corder, E.H., Caskey, J. (2009). Early intervention in Alzheimer disease: The importance of APOE4 plus family history. Neurology, 73(24), 2054–2055. doi:10.1212/WNL.0b013e3181c67870CrossRefGoogle ScholarPubMed
Cupples, L.A., Farrer, L.A., Sadovnick, A.D., Relkin, N., Whitehouse, P., Green, R.C. (2004). Estimating risk curves for first-degree relatives of patients with Alzheimer's disease: The REVEAL study. Genetics in Medicine, 6(4), 192–196. doi:10.1097/01.GIM.0000132679.92238.58Google Scholar
Debette, S., Wolf, P.A., Beiser, A., Au, R., Himali, J.J., Pikula, A., Seshadri, S. (2009). Association of parental dementia with cognitive and brain MRI measures in middle-aged adults. Neurology, 73(24), 2071–2078. doi:10.1212/WNL.0b013e3181c67833CrossRefGoogle ScholarPubMed
Dowling, N.M., Hermann, B., La Rue, A., Sager, M.A. (2010). Latent structure and factorial invariance of a neuropsychological test battery for the study of preclinical Alzheimer's disease. Neuropsychology, 24(6), 742–756. doi:10.1037/a0020176CrossRefGoogle Scholar
Drake, A.W. (1967). Fundamentals of applied probability theory. New York: McGraw-Hill College.Google Scholar
Durbin, R., Eddy, S., Krogh, A., Mitchison, G. (1998). Biological sequence analysis (1st ed.). New York, NY: Cambridge University Press.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 study of the Framingham Cohort. Archives of Neurology, 57(6), 808–813. doi:10.1001/archneur.57.6.808CrossRefGoogle ScholarPubMed
Foldi, N.S., Brickman, A.M., Schaefer, L.A., Knutelska, M.E. (2003). Distinct serial position profiles and neuropsychological measures differentiate late life depression from normal aging and Alzheimer's disease. Psychiatry Research, 120(1), 71–84. doi:10.1016/S0165-1781(03)00163-XCrossRefGoogle ScholarPubMed
Foldi, N.S., Kneutelska, M.E., Winnick, W., Dahlman, K.L., Andreeva-Cook, V. 2005. What happened to their middle region? Serial position effects (SPE) in late life depression, Alzheimer's disease, and normal elderly on the Rey Auditory Verbal Learning Test (RAVLT). Poster session presented at the 33rd Annual International Neuropsychological Society Conference, St. Louis, MO.Google Scholar
Greenwood, P.M., Lambert, C., Sunderland, T., Parasuraman, R. (2005). Effects of apolipoprotein E genotype on spatial attention, working memory, and their interaction in healthy, middle-aged adults: Results from the National Institute of Mental Health's BIOCARD study. Neuropsychology, 19(2), 199–211. doi:10.1037/0894-4105.19.2.199CrossRefGoogle ScholarPubMed
Grundman, M., Petersen, R.C., Ferris, S.H., Thomas, R.G., Aisen, P.S., Bennett, D.A., Thal, L.J. (2004). Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. Archives of Neurology, 61(1), 59–66. doi:10.1001/archneur.61.1.59CrossRefGoogle ScholarPubMed
Guyon, I., Elisseeff, A. (2003). An introduction to variable and feature selection. The Journal of Machine Learning Research, 3, 1157–1182. Retrieved from http://jmlr.csail.mit.edu/Google Scholar
Hampstead, B.M., Sathian, K., Moore, A.B., Nalisnick, C., Stringer, A.Y. (2008). Explicit memory training leads to improved memory for face–name pairs in patients with mild cognitive impairment: Results of a pilot investigation. Journal of the International Neuropsychological Society, 14(05), 883–889. doi:10.1017/S1355617708081009CrossRefGoogle ScholarPubMed
Hayden, K.M., Zandi, P.P., West, N.A., Tschanz, J.T., Norton, M.C., Corcoran, C., Welsh-Bohmer, K.A. (2009). Effects of family history and apolipoprotein E epsilon4 status on cognitive decline in the absence of Alzheimer dementia: The Cache County Study. Archives of Neurology, 66(11), 1378–1383. doi:10.1001/archneurol.2009.237CrossRefGoogle ScholarPubMed
Hendrie, H.C., Albert, M.S., Butters, M.A., Gao, S., Knopman, D.S., Launer, L.J., Wagster, M.V. (2006). The NIH Cognitive and Emotional Health Project. Report of the Critical Evaluation Study Committee. Alzheimer's & Dementia, 2(1), 12–32. doi:10.1016/j.jalz.2005.11.004CrossRefGoogle ScholarPubMed
Hermann, B.P., Seidenberg, M., Wyler, A., Davies, K., Christeson, J., Moran, M., Stroup, E. (1996). The effects of human hippocampal resection on the serial position curve. Cortex, 32(2), 323–334. Retrieved from http://www.cortexjournal.net/CrossRefGoogle ScholarPubMed
Howieson, D.B., Mattek, N., Seeyle, A.M., Dodge, H.H., Wasserman, D., Zitzelberger, T., Jeffrey, K. (2010). Serial position effects in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 1–8. doi:10.1080/13803395.2010.516742Google Scholar
Jack, C.R., Petersen, R.C., Xu, Y.C., O'Brien, P.C., Smith, G.E., Ivnik, R.J., Kokmen, E. (1999). Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology, 52(7), 1397–1403. Retrieved from http://www.neurology.org/CrossRefGoogle ScholarPubMed
Jarvik, L., LaRue, A., Blacker, D., Gatz, M., Kawas, C., McArdle, J.J., Zonderman, A.B. (2008). Children of persons with Alzheimer disease: What does the future hold? Alzheimer Disease and Associated Disorders, 22(1), 6–20. doi:10.1097/WAD.0b013e31816653acCrossRefGoogle ScholarPubMed
Johnson, S.C., Schmitz, T.W., Trivedi, M.A., Ries, M.L., Torgerson, B.M., Carlsson, C.M., Sager, M.A. (2006). The influence of Alzheimer disease family history and apolipoprotein E epsilon4 on mesial temporal lobe activation. The Journal of Neuroscience, 26(22), 6069–6076. doi:10.1523/JNEUROSCI.0959-06.2006CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., Weintraub, S. (1983). The Boston Naming Test (2nd ed.). Philadelphia, PA: Lea & Febiger.Google Scholar
Kawas, C.H., Corrada, M.M., Brookmeyer, R., Morrison, A., Resnick, S.M., Zonderman, A.B., Arenberg, D. (2003). Visual memory predicts Alzheimer's disease more than a decade before diagnosis. Neurology, 60(7), 1089–1093. doi:10.1212/01.WNL.0000055813.36504.BFCrossRefGoogle ScholarPubMed
Killiany, R.J., Gomez-Isla, T., Moss, M., Kikinis, R., Sandor, T., Jolesz, F., Albert, M.S. (2000). Use of structural magnetic resonance imaging to predict who will get Alzheimer's disease. Annals of Neurology, 47(4), 430–439. doi:10.1002/1531-8249(200004)47:4<430::AID-ANA5>3.3.CO;2-93.0.CO;2-I>CrossRefGoogle ScholarPubMed
La Rue, A., Hermann, B., Jones, J.E., Johnson, S., Asthana, S., Sager, M.A. (2008). Effect of parental family history of Alzheimer's disease on serial position profiles. Alzheimer's & Dementia, 4(4), 285–290. doi:10.1016/j.jalz.2008.03.009.CrossRefGoogle ScholarPubMed
Lautenschlager, N.T., Cupples, L.A., Rao, V.S., Auerbach, S.A., Becker, R., Burke, J., Farrer, L.A. (1996). Risk of dementia among relatives of Alzheimer's disease patients in the MIRAGE study: What is in store for the oldest old? Neurology, 46(3), 641–650. Retrieved from http://www.neurology.org/CrossRefGoogle Scholar
Lezak, M.D., Howieson, D.B., Loring, D.W. (2004). Neuropsychological assessment (4th ed.). New York, NY: Oxford University Press.Google Scholar
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology, 34(7), 939–944. Retrieved from http://www.neurology.org/CrossRefGoogle ScholarPubMed
Mosconi, L., Brys, M., Switalski, R., Mistur, R., Glodzik, L., Pirraglia, E., de Leon, M.J. (2007). Maternal family history of Alzheimer's disease predisposes to reduced brain glucose metabolism. Proceedings of the National Academy of Sciences of the United States of America, 104(48), 19067–19072. doi:10.1073/pnas.0705036104CrossRefGoogle ScholarPubMed
Ott, R.L., Longnecker, M.T. (2001). An introduction to statistical methods and data analysis (5th ed.). Pacific Grove, CA: Duxbury Press.Google Scholar
Ramakers, I.H., Visser, P.J., Aalten, P., Bekers, O., Sleegers, K., van Broeckhoven, C.L., Verhey, F.R. (2008). The association between APOE genotype and memory dysfunction in subjects with mild cognitive impairment is related to age and Alzheimer pathology. Dementia and Geriatric Cognitive Disorders, 26, 101–108. doi:10.1159/000144072CrossRefGoogle ScholarPubMed
Ramakers, I.H., Visser, P.J., Aalten, P., Maes, H.L., Lansdaal, H.G., Meijs, C.J., Verhey, F.R. (2010). The predictive value of memory strategies for Alzheimer's disease in subjects with mild cognitive impairment. Archives of Clinical Neuropsychology, 25(1), 71–77. doi:10.1093/arclin/acp093CrossRefGoogle ScholarPubMed
Reitan, R.M., Wolfson, D. (1993). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation (2nd ed.). Tucson, AZ: Neuropsychology Press.Google Scholar
Rey, A. (1964). L'examen clinique en psychologie [The clinical examination in psychology]. Paris, France: Presses Universitaires de France.Google Scholar
Sager, M.A., Hermann, B., La Rue, A. (2005). Middle-aged children of persons with Alzheimer's disease: APOE genotypes and cognitive function in the Wisconsin Registry for Alzheimer's Prevention. Journal of Geriatric Psychiatry and Neurology, 18(4), 245–249. doi:10.1177/0891988705281882CrossRefGoogle ScholarPubMed
Snowdon, D.A., Kemper, S.J., Mortimer, J.A., Greiner, L.H., Wekstein, D.R., Markesbery, W.R. (1996). Linguistic ability in early life and cognitive function and Alzheimer's disease in late life. Findings from the Nun Study. Journal of the American Medical Association, 275(7), 528–532. doi:10.1001/jama.1996.03530310034029CrossRefGoogle ScholarPubMed
Sperling, R.A., Aisen, P.S., Beckett, L.A., Bennett, D.A., Craft, S., Fagan, A.M., Phelps, C.H. (2011). Toward defining the preclinical stages of Alzheimer's disease: Recommendations from the National Institute on Aging and the Alzheimer's Association workgroup. Alzheimer's and Dementia, 7(3), 1–13. doi:10.1016/j.jalz.2011.03.003CrossRefGoogle Scholar
Trenerry, M., Crosson, B., DeBoe, J., Leber, L. (1989). Stroop neuropsychological screening test. Odessa, FL: Psychological Assessment Resource.Google Scholar
Tulving, E. (1962). Subjective organization in free recall of “unrelated” words. Psychological Review, 69(4), 344–354. doi:10.1037/h0043150CrossRefGoogle ScholarPubMed
van Exel, E., Eikelenboom, P., Comijs, H., Frölich, M., Smit, J.H., Stek, M.L., Westendorp, R.G. (2009). Vascular factors and markers of inflammation in offspring with a parental history of late-onset Alzheimer disease. Archives of General Psychiatry, 66(11), 1263–1270. doi:10.1001/archgenpsychiatry.2009.146CrossRefGoogle Scholar
van Vliet, P., Westendorp, R.G., Eikelenboom, P., Comijs, H.C., Frolich, M., Bakker, E., van Exel, E. (2009). Parental history of Alzheimer disease associated with lower plasma apolipoprotein E levels. Neurology, 73(9), 681–687. doi:10.1212/WNL.0b013e3181b59c2eCrossRefGoogle ScholarPubMed
Verhaeghen, P., Marcoen, A., Goossens, L. (1992). Improving memory performance in the aged through mnemonic training: A meta-analytic study. Psychology and Aging, 7(2), 242–251. doi:10.1037/0882-7974.7.2.242CrossRefGoogle ScholarPubMed
Wasserman, L. (2004). All of statistics: A concise course in statistical inference. New York, NY: Springer Verlag.CrossRefGoogle Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Intelligence Scale. San Antonio, TX: The Psychological Corporation.Google Scholar
Welsh, K., Butters, N., Hughes, J., Mohs, R., Heyman, A. (1991). Detection of abnormal memory decline in mild cases of Alzheimer's disease using CERAD neuropsychological measures. Archives of Neurology, 48(3), 278–281. doi:10.1001/archneur.1991.00530150046016CrossRefGoogle ScholarPubMed
Wilkinson, G.S. (1993). Wide range achievement test (WRAT3) administrative manual. Wilmington, DE: Wide Range.Google Scholar
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(1), 63–74. doi:10.1016/j.neurobiolaging.2009.02.003CrossRefGoogle ScholarPubMed
Wolk, D., Dickerson, B., Alzheimer's Disease Neuroimaging Initiative (2011). Fractionating verbal episodic memory in Alzheimer's disease. Neuroimage, 54(2), 1530–1539. doi:10.1016/j.neuroimage.2010.09.005CrossRefGoogle ScholarPubMed
Xu, G., McLaren, D.G., Ries, M.L., Fitzgerald, M.E., Bendlin, B.B., Rowley, H.A., Johnson, S.C. (2009). The influence of parental history of Alzheimer's disease and apolipoprotein E epsilon4 on the BOLD signal during recognition memory. Brain, 132(2), 383–391. doi:10.1093/brain/awn254Google Scholar