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

  • Nathan Hantke (a1), Kristy A. Nielson (a1) (a2), John L. Woodard (a3), Leslie M. Guidotti Breting (a4), Alissa Butts (a1), Michael Seidenberg (a4), J. Carson Smith (a5), Sally Durgerian (a2), Melissa Lancaster (a4), Monica Matthews (a4), Michael A. Sugarman (a3) and Stephen M. Rao (a6)...

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)

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Copyright

Corresponding author

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

References

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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]
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]
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]
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]
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.
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]
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]
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychology and Aging, 17(1), 85100.
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]
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.
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]
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]
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.
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]
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.
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]
Harrell, F.E. (2001). Regression modeling strategies: With applications to linear models, logistic regression, and survival analysis. New York: Springer.
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]
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]
Jurica, P.J., Leitten, C.L., Mattis, S. (2001). Dementia Rating Scale-2 professional manual. Lutz, FL: Psychological Assessment Resources.
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]
Lawton, M.P., Brody, E.M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist, 9(3), 179186.
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]
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.
Mattis, S. (1988). Dementia Rating Scale professional manual. Odessa, FL: Psychological Assessment Resources.
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]
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]
Nagelkerke, N.J.D. (1991). A note on a general definition of the coefficient of determination. Biometrika, 78, 691692.
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.2005.08.022
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.
Nilsson, L.G. (2003). Memory function in normal aging. Acta Neurologica Scandinavica. Supplementum, 179, 713.
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]
Oldfield, R.C. (1971). The assessment of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97111.
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]
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]
Petersen, R.C. (2000). Mild cognitive impairment: Transition between aging and Alzheimer's disease. Neurologia, 15(3), 93101.
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]
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]
Rey, A. (1958). L'examen clinique en psychologie. Paris: Presses Universitaires de France.
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.
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]
Schmidt, K.S. (2004). DRS-2: Alternate form professional manual. Lutz, FL: Psychological Assessment Resources.
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]
Schmidt, M. (1996). Rey Auditory and Verbal Learning Test: A handbook. Los Angeles, CA: Western Psychological Services.
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]
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]
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]
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.
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]
Talairach, J., Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme Medical Publishers.
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]
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/S1355617706060863
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]
Wolk D.A., Dickerson B.C., Alzheimer's Disease Neuroimaging Initiative. (2011). Fractioning verbal episodic memory in Alzheimer's disease. Neuroimage, 54(2), 15301539.
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]
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]
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]
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.

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