Hostname: page-component-7479d7b7d-q6k6v Total loading time: 0 Render date: 2024-07-14T12:19:11.609Z Has data issue: false hasContentIssue false

Comparison of Semantic and Episodic Memory BOLD fMRI Activation in Predicting Cognitive Decline in Older Adults

Published online by Cambridge University Press:  30 November 2012

Nathan Hantke
Affiliation:
Department of Psychology, Marquette University, Milwaukee, Wisconsin
Kristy A. Nielson
Affiliation:
Department of Psychology, Marquette University, Milwaukee, Wisconsin Department of Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin
John L. Woodard
Affiliation:
Department of Psychology, Wayne State University, Detroit, Michigan
Leslie M. Guidotti Breting
Affiliation:
Department of Psychology, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois
Alissa Butts
Affiliation:
Department of Psychology, Marquette University, Milwaukee, Wisconsin
Michael Seidenberg
Affiliation:
Department of Psychology, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois
J. Carson Smith
Affiliation:
Department of Kinesiology, University of Maryland, College Park, Maryland
Sally Durgerian
Affiliation:
Department of Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin
Melissa Lancaster
Affiliation:
Department of Psychology, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois
Monica Matthews
Affiliation:
Department of Psychology, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois
Michael A. Sugarman
Affiliation:
Department of Psychology, Wayne State University, Detroit, Michigan
Stephen M. Rao*
Affiliation:
Neurological Institute, Cleveland Clinic, Cleveland, Ohio
*
Correspondence and reprint requests to: Stephen M. Rao, Schey Center for Cognitive Neuroimaging, Neurological Institute, Cleveland Clinic, 9500 Euclid Avenue/U10, Cleveland, OH 44195. E-mail: raos2@ccf.org

Abstract

Previous studies suggest that task-activated functional magnetic resonance imaging (fMRI) can predict future cognitive decline among healthy older adults. The present fMRI study examined the relative sensitivity of semantic memory (SM) versus episodic memory (EM) activation tasks for predicting cognitive decline. Seventy-eight cognitively intact elders underwent neuropsychological testing at entry and after an 18-month interval, with participants classified as cognitively “Stable” or “Declining” based on ≥1.0 SD decline in performance. Baseline fMRI scanning involved SM (famous name discrimination) and EM (name recognition) tasks. SM and EM fMRI activation, along with Apolipoprotein E (APOE) ε4 status, served as predictors of cognitive outcome using a logistic regression analysis. Twenty-seven (34.6%) participants were classified as Declining and 51 (65.4%) as Stable. APOE ε4 status alone significantly predicted cognitive decline (R2 = .106; C index = .642). Addition of SM activation significantly improved prediction accuracy (R2 = .285; C index = .787), whereas the addition of EM did not (R2 = .212; C index = .711). In combination with APOE status, SM task activation predicts future cognitive decline better than EM activation. These results have implications for use of fMRI in prevention clinical trials involving the identification of persons at-risk for age-associated memory loss and Alzheimer's disease. (JINS, 2012, 18, 1–11)

Type
Research Articles
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

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(Pt 5), 12291239. doi:129/5/1229 [pii], 10.1093/brain/awl089 [doi]CrossRefGoogle ScholarPubMed
Binder, J.R., Desai, R.H., Graves, W.W., Conant, L.L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex, 19(12), 27672796. doi:bhp055 [pii], 10.1093/cercor/bhp055 [doi]CrossRefGoogle ScholarPubMed
Bondi, M.W., Houston, W.S., Eyler, L.T., Brown, G.G. (2005). fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology, 64(3), 501508. doi:64/3/501 [pii], 10.1212/01.WNL.0000150885.00929.7E [doi]CrossRefGoogle ScholarPubMed
Bondi, M.W., Kaszniak, A.W. (1991). Implicit and explicit memory in Alzheimer's disease and Parkinson's disease. Journal of Clinical and Experimental Neuropsychology, 13(2), 339358. doi:10.1080/01688639108401048 [doi]CrossRefGoogle ScholarPubMed
Bondi, M.W., Salmon, D.P., Glasako, D., Thomas, R.G., Thal, L.J. (1999). Neuropsychological function and apolipoprotein E genotype in preclinical detection of Alzheimer's disease. Psychology and Aging, 14(2), 195303.CrossRefGoogle ScholarPubMed
Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., Small, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. New England Journal of Medicine, 343(7), 450456. doi:10.1056/NEJM200008173430701 [doi]CrossRefGoogle ScholarPubMed
Buckner, R.L., Snyder, A.Z., Shannon, B.J., LaRossa, G., Sachs, R., Fotenos, A.F., Mintun, M.A. (2005). Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory. Journal of Neuroscience, 25(34), 77097717. doi:25/34/7709 [pii], 10.1523/JNEUROSCI.2177-05.2005 [doi]CrossRefGoogle ScholarPubMed
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychology and Aging, 17(1), 85100.CrossRefGoogle ScholarPubMed
Cansino, S. (2009). Episodic memory decay along the adult lifespan: A review of behavioral and neurophysiological evidence. International Journal of Psychophysiology, 71(1), 6469. doi:S0167-8760(08)00756-3 [pii], 10.1016/j.ijpsycho.2008.07.005 [doi]CrossRefGoogle ScholarPubMed
Caselli, R.J., Graff-Radford, N.R., Reiman, E.M., Weaver, A., Osborne, D., Lucas, J., Thibodeau, S.N. (1999). Preclinical memory decline in cognitively normal apolipoprotein E-epsilon4 homozygotes. Neurology, 53(1), 201207.CrossRefGoogle ScholarPubMed
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162173. doi:S0010480996900142 [pii]CrossRefGoogle ScholarPubMed
Douville, K., Woodard, J.L., Seidenberg, M., Miller, S.K., Leveroni, C.L., Nielson, K.A., Rao, S.M. (2005). Medial temporal lobe activity for recognition of recent and remote famous names: An event-related fMRI study. Neuropsychologia, 43(5), 693703. doi:S0028-3932(04)00238-6 [pii], 10.1016/j.neuropsychologia.2004.09.005 [doi]CrossRefGoogle ScholarPubMed
Farrer, L.A., Cupples, L.A., Haines, J.L., Hyman, B., Kukull, W.A., Mayeux, R., van Duijn, C.M. (1997). 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. The Journal of the American Medical Association, 278(16), 13491356.CrossRefGoogle ScholarPubMed
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(3), 189198. doi:0022-3956(75)90026-6 [pii]CrossRefGoogle ScholarPubMed
Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., Noll, D.C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33(5), 636647.CrossRefGoogle ScholarPubMed
Han, S.D., Bangen, K.J., Bondi, M.W. (2009). Functional magnetic resonance imaging of compensatory neural recruitment in aging and risk for Alzheimer's disease: Review and recommendations. Dementia and Geriatric Cognitive Disorders, 27(1), 110. doi:000182420 [pii], 10.1159/000182420 [doi]CrossRefGoogle ScholarPubMed
Harrell, F.E. (2001). Regression modeling strategies: With applications to linear models, logistic regression, and survival analysis. New York: Springer.CrossRefGoogle Scholar
Hodges, J.R., Patterson, K. (1995). Is semantic memory consistently impaired early in the course of Alzheimer's disease? Neuroanatomical and diagnostic implications. Neuropsychologia, 33(4), 441459. doi:0028-3932(94)00127-B [pii]CrossRefGoogle 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), 60696076. doi:26/22/6069 [pii], 10.1523/JNEUROSCI.0959-06.2006 [doi]CrossRefGoogle ScholarPubMed
Jurica, P.J., Leitten, C.L., Mattis, S. (2001). Dementia Rating Scale-2 professional manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Kukolja, J., Thiel, C.M., Eggermann, T., Zerres, K., Fink, G.R. (2010). Medial temporal lobe dysfunction during encoding and retrieval of episodic memory in non-demented APOE epsilon4 carriers. Neuroscience, 168(2), 487497. doi:S0306-4522(10)00437-9 [pii], 10.1016/j.neuroscience.2010.03.044 [doi]CrossRefGoogle ScholarPubMed
Lawton, M.P., Brody, E.M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9(3), 179186.CrossRefGoogle ScholarPubMed
Lind, J., Ingvar, M., Persson, J., Sleegers, K., Van Broeckhoven, C., Adolfsson, R., Nyberg, L. (2006). Parietal cortex activation predicts memory decline in apolipoprotein E-epsilon4 carriers. Neuroreport, 17(16), 16831686. doi:10.1097/01.wnr.0000239954.60695.c6 [doi], 00001756-200611060-00005 [pii]CrossRefGoogle ScholarPubMed
Machulda, M.M., Ward, H.A., Borowski, B., Gunter, J.L., Cha, R.H., O'Brien, P.C., Jack, C.R. Jr. (2003). Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients. Neurology, 61(4), 500506.CrossRefGoogle ScholarPubMed
Mattis, S. (1988). Dementia Rating Scale professional manual. Odessa, FL: Psychological Assessment Resources.Google Scholar
Mickes, L., Wixted, J.T., Fennema-Notestine, C., Galasko, D., Bondi, M.W., Thal, L.J., Salmon, D.P. (2007). Progressive impairment on neuropsychological tasks in a longitudinal study of preclinical Alzheimer's disease. Neuropsychology, 21(6), 696705. doi:2007-15625-007 [pii], 10.1037/0894-4105.21.6.696 [doi]CrossRefGoogle Scholar
Miller, S.L., Fenstermacher, E., Bates, J., Blacker, D., Sperling, R.A., Dickerson, B.C. (2008). Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. Journal of Neurolology, Neurosurgery, & Psychiatry, 79(6), 630635. doi:jnnp.2007.124149 [pii], 10.1136/jnnp.2007.124149 [doi]CrossRefGoogle ScholarPubMed
Nagelkerke, N.J.D. (1991). A note on a general definition of the coefficient of determination. Biometrika, 78, 691692.CrossRefGoogle Scholar
Nielson, K.A., Douville, K.L., Seidenberg, M., Woodard, J.L., Miller, S.K., Franczak, M., Rao, S.M. (2006). Age-related functional recruitment for famous name recognition: An event-related fMRI study. Neurobiology of Aging, 27(10), 14941504. doi:S0197-4580(05)00226-5 [pii], 10.1016/j.neurobiolaging.2005.08.022CrossRefGoogle ScholarPubMed
Nielson, K.A., Langenecker, S.A., Garavan, H. (2002). Differences in the functional neuroanatomy of inhibitory control across the adult life span. Psychology and Aging, 17(1), 5671.CrossRefGoogle ScholarPubMed
Nilsson, L.G. (2003). Memory function in normal aging. Acta Neurologica Scandinavica. Supplementum, 179, 713.CrossRefGoogle ScholarPubMed
O'Brien, J.L., O'Keefe, K.M., LaViolette, P.S., DeLuca, A.N., Blacker, D., Dickerson, B.C., Sperling, R.A. (2010). Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology, 74(24), 19691976. doi:WNL.0b013e3181e3966e [pii], 10.1212/WNL.0b013e3181e3966e [doi]CrossRefGoogle ScholarPubMed
Oldfield, R.C. (1971). The assessment of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97111.CrossRefGoogle ScholarPubMed
Park, D.C., Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173196. doi:10.1146/annurev.psych.59.103006.093656 [doi]CrossRefGoogle ScholarPubMed
Persson, J., Nyberg, L., Lind, J., Larsson, A., Nilsson, L.G., Ingvar, M., Buckner, R.L. (2006). Structure-function correlates of cognitive decline in aging. Cerebral Cortex, 16(7), 907915. doi:bhj036 [pii], 10.1093/cercor/bhj036 [doi]CrossRefGoogle ScholarPubMed
Petersen, R.C. (2000). Mild cognitive impairment: Transition between aging and Alzheimer's disease. Neurologia, 15(3), 93101.Google ScholarPubMed
Pihlajamaki, M., Sperling, R.A. (2009). Functional MRI assessment of task-induced deactivation of the default mode network in Alzheimer's disease and at-risk older individuals. Behavioural Neurology, 21(1), 7791. doi:R6331×54T779523W [pii], 10.3233/BEN-2009-0231 [doi]CrossRefGoogle ScholarPubMed
Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676682. doi:10.1073/pnas.98.2.676 [doi], 98/2/676 [pii]CrossRefGoogle ScholarPubMed
Rey, A. (1958). L'examen clinique en psychologie. Paris: Presses Universitaires de France.Google Scholar
Rombouts, S., Scheltens, P. (2005). Functional connectivity in elderly controls and AD patients using resting state fMRI: A pilot study. Current Alzheimer Research, 2(2), 115116.CrossRefGoogle Scholar
Saunders, A.M., Hulette, O., Welsh-Bohmer, K.A., Schmechel, D.E., Crain, B., Burke, J.R., Rosenberg, C. (1996). Specificity, sensitivity, and predictive value of apolipoprotein-E genotyping for sporadic Alzheimer's disease. Lancet, 348(9020), 9093. doi:S0140673696012512 [pii]CrossRefGoogle ScholarPubMed
Schmidt, K.S. (2004). DRS-2: Alternate form professional manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Schmidt, K.S., Mattis, P.J., Adams, J., Nestor, P. (2005). Alternate-form reliability of the Dementia Rating Scale-2. Archives of Clinical Neuropsychology, 20(4), 435441. doi:S0887-6177(04)00145-3 [pii], 10.1016/j.acn.2004.09.011 [doi]CrossRefGoogle ScholarPubMed
Schmidt, M. (1996). Rey Auditory and Verbal Learning Test: A handbook. Los Angeles, CA: Western Psychological Services.Google Scholar
Seidenberg, M., Guidotti, L., Nielson, K.A., Woodard, J.L., Durgerian, S., Antuono, P., Rao, S.M. (2009). Semantic memory activation in individuals at risk for developing Alzheimer disease. Neurology, 73(8), 612620. doi:73/8/612 [pii], 10.1212/WNL.0b013e3181b389ad [doi]CrossRefGoogle ScholarPubMed
Smith, C.D., Kryscio, R.J., Schmitt, F.A., Lovell, M.A., Blonder, L.X., Rayens, W.S., Andersen, A.H. (2005). Longitudinal functional alterations in asymptomatic women at risk for Alzheimer's disease. Journal of Neuroimaging, 15(3), 271277. doi:15/3/271 [pii], 10.1177/1051228405277340 [doi]CrossRefGoogle ScholarPubMed
Sperling, R.A., Dickerson, B.C., Pihlajamaki, M., Vannini, P., LaViolette, P.S., Vitolo, O.V., Johnson, K.A. (2010). Functional alterations in memory networks in early Alzheimer's disease. Neuromolecular Medicine, 12(1), 2743. doi:10.1007/s12017-009-8109-7 [doi]CrossRefGoogle ScholarPubMed
Sugarman, M.A., Woodard, J.L., Nielson, K.A., Seidenberg, M., Smith, J.C., Durgerian, S., Rao, S.M. (2012). Functional magnetic resonance imaging of semantic memory as a presymptomatic biomarker of Alzheimer's disease is. Biochimica et Biophysica Acta, 1822(3), 442456.CrossRefGoogle Scholar
Swan, G.E., Lessov-Schlaggar, C.N., Carmelli, D., Schellenberg, G.D., La Rue, A. (2005). Apolipoprotein E epsilon4 and change in cognitive functioning in community-dwelling older adults. Journal of Geriatric Psychiatry and Neurology, 18(4), 196201. doi:18/4/196 [pii], 10.1177/0891988705281864 [doi]CrossRefGoogle ScholarPubMed
Talairach, J., Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.Google Scholar
Trivedi, M.A., Schmitz, T.W., Ries, M.L., Hess, T.M., Fitzgerald, M.E., Atwood, C.S., Johnson, S.C. (2008). fMRI activation during episodic encoding and metacognitive appraisal across the lifespan: Risk factors for Alzheimer's disease. Neuropsychologia, 46(6), 16671678. doi:S0028-3932(07)00429-0 [pii], 10.1016/j.neuropsychologia.2007.11.035 [doi]CrossRefGoogle ScholarPubMed
Twamley, E.W., Ropacki, S.A., Bondi, M.W. (2006). Neuropsychological and neuroimaging changes in preclinical Alzheimer's disease. Journal of the International Neuropsychological Association, 12(5), 707735. doi:S1355617706060863 [pii], 10.1017/S1355617706060863CrossRefGoogle ScholarPubMed
Wierenga, C.E., Bondi, M.W. (2007). Use of functional magnetic resonance imaging in the early identification of Alzheimer's disease. Neuropsychology Review, 17(2), 127143. doi:10.1007/s11065-007-9025-y [doi]CrossRefGoogle ScholarPubMed
Wolk D.A., Dickerson B.C., Alzheimer's Disease Neuroimaging Initiative. (2011). Fractioning verbal episodic memory in Alzheimer's disease. Neuroimage, 54(2), 15301539.CrossRefGoogle Scholar
Woodard, J.L., Seidenberg, M., Nielson, K.A., Antuono, P., Guidotti, L., Durgerian, S., Rao, S.M. (2009). Semantic memory activation in amnestic mild cognitive impairment. Brain, 132(Pt 8), 20682078. doi:awp157 [pii], 10.1093/brain/awp157 [doi]CrossRefGoogle ScholarPubMed
Woodard, J.L., Seidenberg, M., Nielson, K.A., Miller, S.K., Franczak, M., Antuono, P., Rao, S.M. (2007). Temporally graded activation of neocortical regions in response to memories of different ages. Journal of Cognitive Neuroscience, 19(7), 11131124. doi:10.1162/jocn.2007.19.7.1113 [doi]CrossRefGoogle ScholarPubMed
Woodard, J.L., Seidenberg, M., Nielson, K.A., Smith, J.C., Antuono, P., Durgerian, S., Rao, S.M. (2010). Prediction of cognitive decline in healthy older adults using fMRI. Journal of Alzheimers Disease, 21(3), 871885. doi:M27677251202372G [pii], 10.3233/JAD-2010-091693 [doi]CrossRefGoogle ScholarPubMed
Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., Leirer, V.O. (1982). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research, 17(1), 3749.CrossRefGoogle Scholar