Skip to main content
×
×
Home

Evidence for Reduced Autobiographical Memory Episodic Specificity in Cognitively Normal Middle-Aged and Older Individuals at Increased Risk for Alzheimer’s Disease Dementia

  • Matthew D. Grilli (a1) (a2) (a3), Aubrey A. Wank (a1), John J. Bercel (a1) and Lee Ryan (a1) (a2) (a3)
Abstract

Objectives: Alzheimer’s disease (AD) typically eludes clinical detection for years, if not decades. The identification of subtle cognitive decline associated with preclinical AD would not only advance understanding of the disease, but also provide clinical targets to assess preventative and early intervention treatments. Disrupted retrieval of detailed episodic autobiographical memories may be a sensitive indicator of subtle cognitive decline, because this type of memory taxes a core neural network affected by preclinical AD neuropathology. Methods: To begin to address this idea, we assessed the episodic specificity of autobiographical memories retrieved by cognitively normal middle-aged and older individuals who are carriers of the apolipoprotein E ε4 allele – a population at increased risk for subtle cognitive decline related to neuropathological risk factors for AD. We compared the ε4 carriers to non-carriers of ε4 similar in age, education, and gender. Results: The ε4 carriers did not perform worse than the non-carriers on a comprehensive battery of neuropsychological tests. In contrast, as a group, the ε4 carriers generated autobiographical memories that were reduced in “internal” or episodic details relative to non-carriers. Conclusions: These findings support the notion that reduced autobiographical episodic detail generation may be a marker of subtle cognitive decline associated with AD. (JINS, 2018, 24, 1073–1183)

Copyright
Corresponding author
Correspondence and reprint requests to: Matthew D. Grilli, 1503 E. University Blvd., PO Box 210068, Tucson, Arizona 85721. E-mail: mdgrilli@email.arizona.edu
References
Hide All
Addis, D.R., Moloney, E.E., Tippett, L.J., P. Roberts, R., & Hach, S. (2016). Characterizing cerebellar activity during autobiographical memory retrieval: ALE and functional connectivity investigations. Neuropsychologia, 90, 8093. doi:10.1016/j.neuropsychologia.2016.05.025
Addis, D.R., & Tippett, L. (2004). Memory of myself: Autobiographical memory and identity in Alzheimer’s disease. Memory, 12, 5674. doi:10.1080/09658210244000423
Addis, D.R., Wong, A.T., & Schacter, D.L. (2008). Age-related changes in the episodic simulation of future events. Psychological Science, 19(1), 3341. doi:10.1111/j.1467-9280.2008.02043.x
Barnabe, A., Whitehead, V., Pilon, R., Arsenault-Lapierre, G., & Chertkow, H. (2012). Autobiographical memory in mild cognitive impairment and Alzheimer’s disease: A comparison between the Levine and Kopelman interview methodologies. Hippocampus, 22, 18091825. doi:10.1002/hipo.22015
Bastin, C., Feyers, D., Jedidi, H., Bahri, M.A., Degueldre, C., Lemaire, C., & Salmon, E. (2013). Episodic autobiographical memory in amnestic mild cognitive impairment: What are the neural correlates? Human Brain Mapping, 34, 18111825. doi:10.1002/hbm.22032
Benjamin, M.J., Cifelli, A., Garrard, P., Caine, D., & Jones, F.W. (2015). The role of working memory and verbal fluency in autobiographical memory in early Alzheimer’s disease and matched controls. Neuropsychologia, 78, 115121. doi:10.1016/j.neuropsychologia.2015.10.006
Benton, A.L. (1969). Development of a multilingual aphasia battery: Progress and problems. Journal of the Neurological Sciences, 9, 3948.
Berryhill, M.E., Phuong, L., Picasso, L., Cabeza, R., & Olson, I.R. (2007). Parietal lobe and episodic memory: Bilateral damage causes impaired free recall of autobiographical memory. Journal of Neuroscience, 27(52), 1441514423. doi:10.1523/JNEUROSCI.4163-07.2007
Bertossi, E., Tesini, C., Cappelli, A., & Ciaramelli, E. (2016). Ventromedial prefrontal damage causes a pervasive impairment of episodic memory and future thinking. Neuropsychologia, 90, 1224. doi:10.1016/j.neuropsychologia.2016.01.034
Bondi, M.W., Edmonds, E.C., Jak, A.J., Clark, L.R., Delano-Wood, L., McDonald, C.R., & Salmon, D.P. (2014). Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations, and progression rates. Journal of Alzheimers Disease, 42(1), 275289. doi:10.3233/JAD-140276
Bondi, M.W., Jak, A.J., Delano-Wood, L., Jacobson, M.W., Delis, D.C., & Salmon, D.P. (2008). Neuropsychological contributions to the early identification of Alzheimer’s disease. Neuropsychology Review, 18(1), 7390. doi:10.1007/s11065-008-9054-1
Buckley, R.F., Saling, M.M., Irish, M., Ames, D., Rowe, C.C., & Villemagne, V.L., Australian Imaging Biomarkers and Lifestyle Study of Ageing (AIBL) Research Group. (2014). Autobiographical narratives relate to Alzheimer’s disease biomarkers in older adults. International Psychogeriatrics, 26(10), 17371746. doi:10.1017/S1041610214001136
Buckley, R.F., Saling, M.M., Irish, M., Ames, D., Rowe, C.C., Lautenschlager, N.T., & Ellis, K.A. (2014). Personal memory function in mild cognitive impairment and subjective memory complaints: Results from the Australian Imaging, Biomarkers, and Lifestyle (AIBL) Study of Ageing. Journal of Alzheimers Disease, 40(3), 551561. doi:10.3233/JAD-131820
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:10.1523/JNEUROSCI.2177-05.2005
Caselli, R.J., Dueck, A.C., Osborne, D., Sabbagh, M.N., Connor, D.J., Ahern, G.L., & Reiman, E.M. (2009). Longitudinal modeling of age-related memory decline and the APOE epsilon4 effect. New England Journal of Medicine, 361(3), 255263. doi:10.1056/NEJMoa0809437
Caselli, R.J., & Reiman, E.M. (2013). Characterizing the preclinical stages of Alzheimer’s disease and the prospect of presymptomatic intervention. Journal of Alzheimers Disease, 33(Suppl 1), S405S416. doi:10.3233/JAD-2012-129026
Cermak, L.S., & O’Connor, M. (1983). The anterograde and retrograde retrieval ability of a patient with amnesia due to encephalitis. Neuropsychologia, 21(3), 213234.
Chen, H.Y., Gilmore, A.W., Nelson, S.M., & McDermott, K.B. (2017). Are there multiple kinds of episodic memory? An fMRI investigation comparing autobiographical and recognition memory tasks. Journal of Neuroscience, 37(10), 27642775. doi:10.1523/JNEUROSCI.1534-16.2017
Chételat, G., Villemagne, V.L., Bourgeat, P., Pike, K.E., Jones, G., & Ames, D., Australian Imaging Biomarkers and Lifestyle Research Group. (2010). Relationship between atrophy and beta-amyloid deposition in Alzheimer disease. Annals of Neurology, 67(3), 317324. doi:10.1002/ana.21955
Cohen, N.J., & Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system. Cambridge, MA: MIT Press.
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). The California Verbal Learning Test (CVLT-II). New York, NY: The Psychological Corporation.
den Heijer, T., Oudkerk, M., Launer, L.J., van Duijn, C.M., Hofman, A., & Breteler, M.M. (2002). Hippocampal, amygdalar, and global brain atrophy in different apolipoprotein E genotypes. Neurology, 59(5), 746748.
Edmonds, E.C., Delano-Wood, L., Galasko, D.R., Salmon, D.P., & Bondi, M.W. (2015). Subtle cognitive decline and biomarker staging in preclinical Alzheimer’s disease. Journal of Alzheimer’s Disease, 47, 231242.
El Haj, M., Antoine, P., Amouyel, P., Lambert, J.C., Pasquier, F., & Kapogiannis, D. (2016). Apolipoprotein E (APOE) e4 and episodic memory decline in Alzheimer’s disease: A review. Ageing Research Reviews, 27, 1522. doi:10.1016/j.arr.2016.02.002
El Haj, M., Antoine, P., Nandrino, J.L., & Kapogiannis, D. (2015). Autobiographical memory decline in Alzheimer’s disease, a theoretical and clinical overview. Ageing Research Reviews, 23, 183192. doi:10.1016/j.arr.2015.07.001
Fastenau, P.S., Denburg, N.L., & Hufford, B.J. (1999). Adult norms for the Rey-Osterrieth Complex Figure Test and for supplemental recognition and matching trials from the extended complex figure test. The Clinical Neuropsychologist, 13(1), 3047. doi/abs/10.1076/clin.13.1.30.1976
Gamboz, N., De Vito, S., Brandimonte, M.A., Pappalardo, S., Galeone, F., Iavarone, A., &Della Sala, S. (2010). Episodic future thinking in amnestic mild cognitive impairment. Neuropsychologia, 48, 20912097. doi:10.1016/j.neuropsychologia.2010.03.030
Gilboa, A. (2004). Autobiographical and episodic memory--One and the same? Evidence from prefrontal activation in neuroimaging studies. Neuropsychologia, 42(10), 13361349. doi:10.1016/j.neuropsychologia.2004.02.014
Goodglass, H., Kaplan, E., & Barresi, B. (2001). Boston diagnostic aphasia examination (3rd ed.). Philadelphia: Lippincott Williams & Wilkins.
Grilli, M.D., Wank, A.A., & Verfaellie, M. (2018). The life stories of adults with amnesia: Insights into the contribution of the medial temporal lobes to the organization of autobiographical memory. Neuropsychologia, 110, 8491. doi:10.1016/j.neuropsychologia.2017.03.013
Grilli, M.D., & Verfaellie, M. (2015). Supporting the self-concept with memory: Insight from amnesia. Social Cognitive and Affective Neuroscience, 16841692. doi:10.1093/scan/nsv056
Grilli, M.D., & Verfaellie, M. (2014). Personal semantic memory: Insights from neuropsychological research on amnesia. Neuropsychologia, 61, 5664. doi:10.1016/j.neuropsychologia.2014.06.012
Han, D.S., Nguyen, C.P., Stricker, N.H., & Nation, D.A. (2017). Detectable neuropsychological differences in early preclinical Alzheimer’s disease: A meta-analysis. Neuropsychology Review, 27, 305325. doi:10.1007/s11065-017-9345-5
Hassabis, D., Kumaran, D., Vann, S.D., & Maguire, E.A. (2007). Patients with hippocampal amnesia cannot imagine new experiences. Proceedings of the National Academy of Sciences of the United States of America, 104(5), 17261731. doi:10.1073/pnas.0610561104
Heaton, R.K., Miller, S.W., Taylor, M.J., & Grant, I. (2004). Revised comprehensive norms for an expanded Halstead-Reitan Battery: Demographically adjusted neuropsychological norms for African American and Caucasian adults. Lutz, FL: Psychological Assessment Resources.
Hodgetts, C.J., Postans, M., Warne, N., Varnava, A., Lawrence, A.D., & Graham, K.S. (2017). Distinct contributions of the fornix and inferior longitudinal fasciculus to episodic and semantic autobiographical memory. Cortex, 94, 114. doi:10.1016/j.cortex.2017.05.010
Irish, M., Landin-Romero, R., Mothakunnel, A., Ramanan, S., Hseih, S., Hodges, J.R., &Piguet, O. (2018). Evolution of autobiographical memory impairments in Alzheimer’s disease and frontotemporal dementia: A longitudinal neuroimaging study. Neuropsychologia, 1110, 1425.
Irish, M., Halena, S., Kamminga, J., Tu, S., Hornberger, M., & Hodges, J.R. (2015). Scene construction impairments in Alzheimer’s disease – A unique role for the posterior cingulate cortex. Cortex, 73, 1023. doi:10.1016/j.cortex.2015.08.004
Irish, M., Addis, D.R., Hodges, J.R., & Piguet, O. (2012). Considering the role of semantic memory in episodic future thinking: Evidence from semantic dementia. Brain, 135, 21782191. doi:10.1093/brain/aws119
Irish, M., Hornberger, M., Lah, S., Miller, L., Pengas, G., Nestor, P.J., & Piguet, O. (2011). Profiles of recent autobiographical memory retrieval in semantic dementia, behavioural-variant frontotemporal dementia, and Alzheimer’s disease. Neuropsychologia, 49, 26942702. doi:10.1016/j.neuropsychologia.2011.05.017
Irish, M., Lawlor, B.A., O’Mara, S.M., & Coen, R.F. (2010). Exploring the recollective experience during autobiographical memory retrieval in amnestic mild cognitive impairment. Journal of the International Neurpsychological Society, 16(3), 546555. doi:10.1017/S1355617710000172
Jack, C.R., Knopman, D.S., Jagust, W.J., Petersen, R.C., Weiner, M.W., Aisen, P.S., & Trojanowski, J.Q. (2013). Tracking pathophysiological processes in Alzheimer’s disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurology, 12(2), 207216. doi:10.1016/S1474-4422(12)70291-0
Jack, C.R., Knopman, D.S., Jagust, W.J., Shaw, L.M., Aisen, P.S., Weiner, M.W., & Trojanowski, J.Q. (2010). Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade. Lancet Neurology, 9(1), 119128. doi:10.1016/S1474-4422(09)70299-6
Jack, C.R., Wiste, H.J., Weigand, S.D., Therneau, T.M., Knopman, D.S., Lowe, V., & Petersen, R.C. (2017). Age-specific and sex-specific prevalence of cerebral β-amyloidosis, tauopathy, and neurodegeneration in cognitively unimpaired individuals aged 50-95 years: A cross-sectional study. Lancet Neurology, 16(6), 435444. doi:10.1016/S1474-4422(17)30077-7
Levine, B. (2004). Autobiographical memory and the self in time: Brain lesion effects, functional neuroanatomy, and lifespan development. Brain & Cognition, 55, 5468.
Levine, B., Svoboda, E., Hay, J.F., Winocur, G., & Moscovitch, M. (2002). Aging and autobiographical memory: Dissociating episodic from semantic retrieval. Psychology and Aging, 17(4), 677689.
Maguire, E.A., & Mullally, S.L. (2013). The hippocampus: A manifesto for change. Journal of Experimental Psychology. General, 142(4), 11801189. doi:10.1037/a0033650
Martinelli, P., Sperduti, M., & Piolino, P. (2013). Neural substrates of the self-memory system: New insights from a meta-analysis. Human Brain Mapping, 34(7), 15151529. doi:10.1002/hbm.22008
Masters, C.L., Bateman, R., Blennow, K., Rowe, C.C., Sperling, R.A., & Cummings, J.L. (2015). Alzheimer’s disease. Nature Reviews . Disease Primers, 1, 15056. doi:10.1038/nrdp.2015.56
McCormick, C., St-Laurent, M., Ty, A., Valiante, T.A., & McAndrews, M.P. (2015). Functional and effective hippocampal-neocortical connectivity during construction and elaboration of autobiographical memory retrieval. Cerebral Cortex, 25(5), 12971305. doi:10.1093/cercor/bht324
Miller, T.D., Chong, T.T.J., Aimola Davies, A.M., Ng, T.W.C., Johnson, M.R., Irani, S.R., & Rosenthal, C.R. (2017). Focal CA3 hippocampal subfield atrophy following LGII VGKC-complex antibody limbic encephalitis. Brain, 140, 12121219. doi:10.1093/brain/awx070
Monge, Z.A., Wing, E.A., Stokes, J., & Cabeza, R. (2018). Search and recovery of autobiographical and laboratory memories: Shared and distinct neural components. Neuropsychologia, 110, 4454. doi:10.1016/j.neuropsychologia.2017.07.030
Murphy, K.J., Troyer, A.K., Levine, B., & Moscovitch, M. (2008). Episodic, but not semantic, autobiographical memory is reduced in amnestic mild cognitive impairment. Neuropsychologia, 46(13), 31163123. doi:10.1016/j.neuropsychologia.2008.07.004
Palombo, D.J., Hayes, S.M., Peterson, K.M., Keane, M.M., & Verfaellie, M. (2018). Medial temporal lobe contributions to episodic future thinking: Scene construction or future projection? Cerebral Cortex, 28, 447458. doi.org/ 10.1093/cercor/bhw381
Palombo, D.J., Bacopulos, A., Amaral, R.S.C., Olsen, R.K., Todd, R.M., Anderson, A.K., & Levine, B. (2018). Episodic autobiographical memory is associated with variation in the size of hippocampal subregions. Hippocampus, 28, 6975. doi:10.1002/hipo.22818
Parra, M.A., Abrahams, S., Logie, R.H., Méndez, L.G., Lopera, F., & Della Sala, S. (2010). Visual short-term memory binding deficits in familial Alzheimer’s disease. Brain, 133(9), 27022713. doi:10.1093/brain/awq148
Price, J.L., & Morris, J.C. (1999). Tangles and plaques in nondemented aging and “preclinical” Alzheimer’s disease. Annals of Neurology, 45(3), 358368.
Radloff, L.S. (1977). The CES-D scale: A self-report depression scale for research in the general population. Applied Psychological Measurements, 1, 385401.
Reiman, E.M., Chen, K., Alexander, G.E., Caselli, R.J., Bandy, D., Osborne, D., & Hardy, J. (2005). Correlations between apolipoprotein E epsilon4 gene dose and brain-imaging measurements of regional hypometabolism. Proceedings of the National Academy of Sciences of the United States of America, 102(23), 82998302. doi:10.1073/pnas.0500579102
Reitan, R.M., & Wolfson, D. (1993). The Haldstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation. Tucson: Neuropsychology Press.
Rentz, D.M., Amariglio, R.E., Becker, J.A., Frey, M., Olson, L.E., Frishe, K., & Sperling, R.A. (2011). Face-name associative memory performance is related to amyloid burden in normal elderly. Neuropsychologia, 49(9), 27762783. doi:10.1016/j.neuropsychologia.2011.06.006
Rey, A. (1941). L’examen psychologique dans les cas d’encephalopathie traumatique. Archives de Psychologie, 28, 286340.
Roberts, R.P., Schacter, D.L., & Addis, D.R. (2018). Scene construction and relational processing: Separable constructs? Cerebral Cortex, 28, 17291732. doi:10.1093/cercor/bhx081
Rugg, M.D., & Vilberg, K.L. (2013). Brain networks underlying episodic memory retrieval. Current Opinion in Neurobiology, 23(2), 255260. doi:10.1016/j.conb.2012.11.005
Ryan, L., Walther, K., Bendlin, B.B., Lue, L.F., Walker, D.G., & Glisky, E.L. (2011). Age-related differences in white matter integrity and cognitive function are related to APOE status. NeuroImage, 54(2), 15651577. doi:10.1016/j.neuroimage.2010.08.052
Schacter, D.L., & Addis, D.R. (2007). The cognitive neuroscience of constructive memory: Remembering the past and imagining the future. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 362(1481), 773786. doi: 10.1098/rstb.2007.2087
Schmitt, F.A., Davis, D.G., Wekstein, D.R., Smith, C.D., Ashford, J.W., & Markesbery, W.R. (2000). “Preclinical” AD revisited: Neuropathology of cognitively normal older adults. Neurology, 55(3), 370376.
Sheldon, S., Farb, N., Palombo, D.J., & Levine, B. (2016). Intrinsic medial temporal lobe connectivity relates to individual differences in episodic autobiographical remembering. Cortex, 74, 206216. doi:10.1016/j.cortex.2015.11.005
Sheldon, S., Vandermorris, S., Al-Haj, M., Cohen, S., Winocur, G., & Moscovitch, M. (2015). Ill-defined problem solving in amnestic mild cognitive impairment: Linking episodic memory to effective solution generation. Neuropsychologia, 68, 168175. doi:10.1016/j.neuropsychologia.2015.01.005
Sheline, Y.I., Raichle, M.E., Snyder, A.Z., Morris, J.C., Head, D., Wang, S., &Mintun, M.A. (2010). Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biological Psychiatry, 67(6), 584587. doi: 10.1016/j.biopsych.2009.08.024
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-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers & Dementia, 7(3), 280292. doi:10.1016/j.jalz.2011.03.003
Spreng, R.N., Lockrow, A.W., DuPre, E., Setton, R., Spreng, K.A.P., & Turner, G.R. (2018). Semanticized autobiographical memory and the default-executive coupling hypothesis of aging. Neuropsychologia, 1110, 3743. doi:10.1016/j.neuropsychologia.2017.06.009
St. Jacques, P.L., & Levine, B. (2007). Ageing and autobiographical memory for emotional and neutral events. Memory, 15, 129144.
Summerfield, J.J., Hassabis, D., & Maguire, E.A. (2010). Differential engagement of brain regions within a ‘core’ network during scene construction. Neuropsychologia, 48(5), 15011509. doi: 10.1016/j.neuropsychologia.2010.01.022
Svoboda, E., McKinnon, M.C., & Levine, B. (2006). The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia, 44(12), 21892208. doi:10.1016/j.neuropsychologia.2006.05.023
Trachtenberg, A.J., Filippini, N., & Mackay, C.E. (2012). The effects of APOE-ε4 on the BOLD response. Neurobiology of Aging, 33(2), 323334. doi:10.1016/j.neurobiolaging.2010.03.009
Tramoni, E., Felician, O., Koric, L., Balzamo, M., Joubert, S., & Ceccaldi, M. (2012). Alteration of autobiographical memory in amnestic mild cognitive impairment. Cortex, 48, 13101319. doi: 10.1016/j.cortex.2011.09.002
Tulving, E. (1985). Memory and consciousness. Canadian Psychology, 26, 112.
van der Flier, W.M., Schoonenboom, S.N., Pijnenburg, Y.A., Fox, N.C., & Sheltens, P. (2006). The effect of APOE genotype on clinical phenotype in Alzheimer’s disease. Neurology, 67, 526527. doi:10.1212/01.wnl.0000228222.17111.2a
van der Vlies, A.E., Pijneburg, Y.A.L., Koene, T., Klein, M., Kok, A., Sheltens, P., &van der Flier, W.M. (2007). Cognitive impairment in Alzheimer’s disease is modified by APOE genotype. Dementia and Geriatric Cognitive Disorders, 24, 98103. doi:10.1159/000104467
Verfaellie, M., Bousquet, K., & Keane, M.M. (2014). Medial temporal and neocortical contributions to remote memory for semantic narratives: Evidence from amnesia. Neuropsychologia, 61, 105112. doi:10.1016/j.neuropsychologia.2014.06.018
Wechsler, D. (2008). WAIS-IV Manual. New York, NY: Psychological Corporation.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the International Neuropsychological Society
  • ISSN: 1355-6177
  • EISSN: 1469-7661
  • URL: /core/journals/journal-of-the-international-neuropsychological-society
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed