Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T05:22:04.443Z Has data issue: false hasContentIssue false

Association Between Visual Memory and In Vivo Amyloid and Tau Pathology in Preclinical Autosomal Dominant Alzheimer’s Disease

Published online by Cambridge University Press:  07 August 2020

Yamile Bocanegra
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Calle 62 No. 52-59, Medellín, Colombia
Joshua T. Fox-Fuller
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA Department of Psychological and Brain Sciences, Boston University, 900 Commonwealth Ave., 2nd Floor, Boston, MA02125, USA
Ana Baena
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Calle 62 No. 52-59, Medellín, Colombia
Edmarie Guzmán-Vélez
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA
Clara Vila-Castelar
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA
Jairo Martínez
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA
Heirangi Torrico-Teave
Affiliation:
Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA
Francisco Lopera
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Calle 62 No. 52-59, Medellín, Colombia
Yakeel T. Quiroz*
Affiliation:
Grupo de Neurociencias de Antioquia, Universidad de Antioquia, Calle 62 No. 52-59, Medellín, Colombia Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA
*
*Correspondence and reprint requests to: Yakeel T. Quiroz, PhD, Associate Professor, Harvard Medical School, Departments of Psychiatry and Neurology, Massachusetts General Hospital, 100 1st Ave, Building 39, Suite 101, Charlestown, MA02129, USA. Phone: +(617) 643-5944, Fax: +(617) 726-5760. E-mail: [email protected]

Abstract

Objective:

Visual memory (ViM) declines early in Alzheimer’s disease (AD). However, it is unclear whether ViM impairment is evident in the preclinical stage and relates to markers of AD pathology. We examined the relationship between ViM performance and in vivo markers of brain pathology in individuals with autosomal dominant AD (ADAD).

Methods:

Forty-five cognitively unimpaired individuals from a Colombian kindred with the Presenilin 1 (PSEN1) E280A ADAD mutation (19 carriers and 26 noncarriers) completed the Rey–Osterrieth Complex Figure immediate recall test, a measure of ViM. Cortical amyloid burden and regional tau deposition in the entorhinal cortex (EC) and inferior temporal cortex (IT) were measured using 11C-Pittsburgh compound B positron emission tomography (PET) and 11F-flortaucipir PET, respectively.

Results:

Cognitively unimpaired carriers and noncarriers did not differ on ViM performance. Compared to noncarriers, carriers had higher levels of cortical amyloid and regional tau in both the EC and IT. In cognitively unimpaired carriers, greater cortical amyloid burden, higher levels of regional tau, and greater age were associated with worse ViM performance. Only a moderate correlation between regional tau and ViM performance remained after adjusting for verbal memory scores. None of these correlations were observed in noncarriers.

Conclusions:

Results suggest that AD pathology and greater age are associated with worse ViM performance in ADAD before the onset of clinical symptoms. Further investigation with larger samples and longitudinal follow-up is needed to examine the utility of ViM measures for identifying individuals at high risk of developing dementia later in life.

Type
Regular Research
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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

Acosta-Baena, N., Sepulveda-Falla, D., Lopera-Gómez, C.M., Jaramillo-Elorza, M.C., Moreno, S., Aguirre-Acevedo, D.C., … Lopera, F. (2011). Pre-dementia clinical stages in presenilin 1 E280A familial early-onset Alzheimer’s disease: a retrospective cohort study. Lancet Neurology, 10(3), 213220. doi: 10.1016/S1474-4422(10)70323-9.CrossRefGoogle ScholarPubMed
Aguirre-Acevedo, D.C., Gómez, R.D., Moreno, S., Henao-Arboleda, E., Motta, M., Muñoz, C., … Lopera, F. (2007). Validity and reliability of the CERAD-Col neuropsychological battery. Revue Neurologique, 45(11), 655660.Google ScholarPubMed
Aguirre-Acevedo, D.C., Lopera, F., Henao, E., Tirado, V., Muñoz, C., Giraldo, M., … Jaimes, F. (2016). Cognitive decline in a Colombian kindred with autosomal dominant Alzheimer disease: a retrospective cohort study. JAMA Neurology, 73(4), 431438. doi: 10.1001/jamaneurol.2015.4851.CrossRefGoogle Scholar
Barbeau, E.J., Pariente, J., Felician, O., & Puel, M. (2011). Visual recognition memory: a double anatomo-functional dissociation. Hippocampus, 21(9), 929934. doi: 10.1002/hipo.20848.Google ScholarPubMed
Bateman, R.J., Xiong, C., Benzinger, T.L., Fagan, A.M., Goate, A., Fox, N.C., … Network, D.I.A. (2012). Clinical and biomarker changes in dominantly inherited Alzheimer’s disease. The New England Journal of Medicine, 367(9), 795804. doi: 10.1056/NEJMoa1202753.CrossRefGoogle ScholarPubMed
Berry, D.T.R., Allen, R.S., & Schmitt, F. A. (1991). Rey-Osterrieth complex figure: psychometric characteristics in a geriatric sample. Clinical Neuropsychologist, 5(2), 143153. doi: 10.1080/13854049108403298.CrossRefGoogle Scholar
Boone, K.B., Lesser, I.M., Hill-gutierrez, E., Berman, N.G., & D’Elia, L.F. (1993). Rey-Osterrieth complex figure performance in healthy, older adults: relationship to age, education, sex, and IQ. Clinical Neuropsychologist, 7(1), 2228. doi: 10.1080/13854049308401884.CrossRefGoogle Scholar
Braskie, M.N., Small, G.W., & Bookheimer, S.Y. (2009). Entorhinal cortex structure and functional MRI response during an associative verbal memory task. Human Brain Mapping, 30(12), 39813992. doi: 10.1002/hbm.20823.CrossRefGoogle ScholarPubMed
Fiebach, C.J., Rissman, J., & D’Esposito, M. (2006). Modulation of inferotemporal cortex activation during verbal working memory maintenance. Neuron, 51(2), 251261. doi: 10.1016/j.neuron.2006.06.007.CrossRefGoogle ScholarPubMed
Fleisher, A.S., Chen, K., Quiroz, Y.T., Jakimovich, L.J., Gomez, M.G., Langois, C.M., … Reiman, E.M. (2012). Florbetapir PET analysis of amyloid-β deposition in the presenilin 1 E280A autosomal dominant Alzheimer’s disease kindred: a cross-sectional study. The Lancet Neurology, 11(12), 10571065. doi: 10.1016/S1474-4422(12)70227-2.CrossRefGoogle ScholarPubMed
Fleisher, A.S., Chen, K., Quiroz, Y.T., Jakimovich, L.J., Gutierrez Gomez, M., Langois, C.M., … Reiman, E.M. (2015). Associations between biomarkers and age in the presenilin 1 E280A autosomal dominant Alzheimer disease kindred: a cross-sectional study. JAMA Neurology, 72(3), 316324. doi: 10.1001/jamaneurol.2014.3314.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: 10.1016/0022-3956(75)90026-6.CrossRefGoogle ScholarPubMed
Fuller, J.T., Cronin-Golomb, A., Gatchel, J.R., Norton, D.J., Guzmán-Vélez, E., Jacobs, H.I.L., … Quiroz, Y.T. (2019). Biological and cognitive markers of presenilin1 E280A autosomal dominant Alzheimer’s disease: a comprehensive review of the Colombian kindred. The Journal of Prevention of Alzheimers Disease, 6(2), 112120. doi: 10.14283/jpad.2019.6.Google ScholarPubMed
Gordon, B.A., Blazey, T.M., Christensen, J., Dincer, A., Flores, S., Keefe, S., … Benzinger, T.L.S. (2019). Tau PET in autosomal dominant Alzheimer’s disease: relationship with cognition, dementia and other biomarkers. Brain, 142(4), 10631076. doi: 10.1093/brain/awz019.CrossRefGoogle ScholarPubMed
Hollands, S., Lim, Y.Y., Buckley, R., Pietrzak, R.H., Snyder, P.J., Ames, D., … Maruff, P. (2015). Amyloid-β related memory decline is not associated with subjective or informant rated cognitive impairment in healthy adults. Journal of Alzheimers Disease, 43(2), 677686. doi: 10.3233/JAD-140678.CrossRefGoogle ScholarPubMed
IBM. (2016). IBM SPSS Statistics for Windows, Version 24.0. Armonk, NY: IBM Corp.Google Scholar
Jack, C.R., Bennett, D.A., Blennow, K., Carrillo, M.C., Dunn, B., Haeberlein, S.B., … Contributors. (2018). NIA-AA research framework: Toward a biological definition of Alzheimer’s disease. Alzheimers Dement, 14(4), 535562. doi: 10.1016/j.jalz.2018.02.018.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Jansen, W.J., Ossenkoppele, R., Tijms, B.M., Fagan, A.M., Hansson, O., Klunk, W.E., … Group, A.B.S. (2018). Association of cerebral amyloid-β aggregation with cognitive functioning in persons without dementia. JAMA Psychiatry, 75(1), 8495. doi: 10.1001/jamapsychiatry.2017.3391.CrossRefGoogle ScholarPubMed
Johnson, S.C., Christian, B.T., Okonkwo, O.C., Oh, J.M., Harding, S., Xu, G., … Sager, M.A. (2014). Amyloid burden and neural function in people at risk for Alzheimer’s disease. Neurobiology of Aging, 35(3), 576584. doi: 10.1016/j.neurobiolaging.2013.09.028.CrossRefGoogle ScholarPubMed
Kravitz, D.J., Saleem, K.S., Baker, C.I., Ungerleider, L.G., & Mishkin, M. (2013). The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends in Cognitive Sciences, 17(1), 2649. doi: 10.1016/j.tics.2012.10.011.CrossRefGoogle ScholarPubMed
Lekeu, F., Magis, D., Marique, P., Delbeuck, X., Bechet, S., Guillaume, B., … Salmon, E. (2010). The California verbal learning test and other standard clinical neuropsychological tests to predict conversion from mild memory impairment to dementia. Journal of Clinical and Experimental Neuropsychology, 32(2), 164173. doi: 10.1080/13803390902889606.CrossRefGoogle Scholar
Lim, Y.Y., Kalinowski, P., Pietrzak, R.H., Laws, S.M., Burnham, S.C., Ames, D., … Maruff, P.T. (2018). Association of β-amyloid and apolipoprotein E ϵ4 with memory decline in preclinical Alzheimer disease. JAMA Neurology, 75(4), 488494. doi: 10.1001/jamaneurol.2017.4325.CrossRefGoogle ScholarPubMed
Lim, Y.Y., Maruff, P., Pietrzak, R.H., Ames, D., Ellis, K.A., Harrington, K., … Group, A.R. (2014). Effect of amyloid on memory and non-memory decline from preclinical to clinical Alzheimer’s disease. Brain, 137(Pt 1), 221231. doi: 10.1093/brain/awt286.CrossRefGoogle ScholarPubMed
Mormino, E.C., Papp, K.V., Rentz, D.M., Donohue, M.C., Amariglio, R., Quiroz, Y.T., … Sperling, R.A. (2017). Early and late change on the preclinical Alzheimer’s cognitive composite in clinically normal older individuals with elevated amyloid β. Alzheimers Dement, 13(9), 10041012. doi: 10.1016/j.jalz.2017.01.018.CrossRefGoogle ScholarPubMed
Morris, J.C. (1993). The clinical dementia rating (CDR): current version and scoring rules. Neurology, 43(11), 24122414. doi: 10.1212/wnl.43.11.2412-a.CrossRefGoogle ScholarPubMed
Ossenkoppele, R., Madison, C., Oh, H., Wirth, M., van Berckel, B.N., & Jagust, W.J. (2014). Is verbal episodic memory in elderly with amyloid deposits preserved through altered neuronal function? Cerebral Cortex, 24(8), 22102218. doi: 10.1093/cercor/bht076.CrossRefGoogle ScholarPubMed
Papp, K.V., Rentz, D.M., Orlovsky, I., Sperling, R.A., & Mormino, E.C. (2017). Optimizing the preclinical Alzheimer’s cognitive composite with semantic processing: the PACC5. Alzheimers Dement (N Y), 3(4), 668677. doi: 10.1016/j.trci.2017.10.004.CrossRefGoogle ScholarPubMed
Peter, J., Sandkamp, R., Minkova, L., Schumacher, L.V., Kaller, C.P., Abdulkadir, A., & Klöppel, S. (2018). Real-world navigation in amnestic mild cognitive impairment: the relation to visuospatial memory and volume of hippocampal subregions. Neuropsychologia, 109, 8694. doi: 10.1016/j.neuropsychologia.2017.12.014.CrossRefGoogle ScholarPubMed
Petersen, R.C., Wiste, H.J., Weigand, S.D., Rocca, W.A., Roberts, R.O., Mielke, M.M., … Jack, C.R. (2016). Association of elevated amyloid levels with cognition and biomarkers in cognitively normal people from the community. JAMA Neurology, 73(1), 8592. doi: 10.1001/jamaneurol.2015.3098.CrossRefGoogle ScholarPubMed
Pike, K.E., Savage, G., Villemagne, V.L., Ng, S., Moss, S.A., Maruff, P., … Rowe, C. C. (2007). Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer’s disease. Brain, 130(Pt 11), 28372844. doi: 10.1093/brain/awm238.CrossRefGoogle ScholarPubMed
Pontecorvo, M.J., Devous, M.D., Navitsky, M., Lu, M., Salloway, S., Schaerf, F.W., … 18F-AV-1451-A05 investigators (2017). Relationships between flortaucipir PET tau binding and amyloid burden, clinical diagnosis, age and cognition. Brain, 140(3), 748763. doi: 10.1093/brain/aww334.Google ScholarPubMed
Quiroz, Y.T., Sperling, R.A., Norton, D.J., Baena, A., Arboleda-Velasquez, J.F., Cosio, D., … Johnson, K.A. (2018). Association between amyloid and tau accumulation in young adults with autosomal dominant Alzheimer disease. JAMA Neurology, 75(5), 548556. doi: 10.1001/jamaneurol.2017.4907.CrossRefGoogle ScholarPubMed
Ranganath, C., Cohen, M.X., Dam, C., & D’Esposito, M. (2004). Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. The Journal of Neuroscience, 24(16), 39173925. doi: 10.1523/JNEUROSCI.5053-03.2004.CrossRefGoogle ScholarPubMed
Reisberg, B. (1988). Functional assessment staging (FAST). Psychopharmacology Bulletin, 24(4), 653659.Google Scholar
Rey, A. (2003). Rey, Test de Copia y Reproducción de Memoria de Figuras Geométricas Complejas. Madrid, Spain: TEA ediciones.Google Scholar
Salimi, S., Irish, M., Foxe, D., Hodges, J. R., Piguet, O., & Burrell, J.R. (2018). Can visuospatial measures improve the diagnosis of Alzheimer’s disease? Alzheimers Dement (Amst), 10, 6674. doi: 10.1016/j.dadm.2017.10.004.CrossRefGoogle ScholarPubMed
Schoenberg, M.R., Duff, K., Beglinger, L.J., Moser, D.J., Bayless, J.D., Mold, J., … Adams, R.L. (2008). Retention rates on RBANS memory subtests in elderly adults. Journal of Geriatric Psychiatry and Neurology, 21(1), 2633. doi: 10.1177/0891988707311030.CrossRefGoogle ScholarPubMed
Schultz, S.A., Gordon, B.A., Mishra, S., Su, Y., Perrin, R.J., Cairns, N.J., … Benzinger, T.L.S. (2018). Widespread distribution of tauopathy in preclinical Alzheimer’s disease. Neurobiology of Aging, 72, 177185. doi: 10.1016/j.neurobiolaging.2018.08.022.CrossRefGoogle ScholarPubMed
Sperling, R.A., Johnson, K.A., Doraiswamy, P.M., Reiman, E.M., Fleisher, A.S., Sabbagh, M.N., … Group, A.-A.S. (2013). Amyloid deposition detected with florbetapir F 18 ((18)F-AV-45) is related to lower episodic memory performance in clinically normal older individuals. Neurobiology of Aging, 34(3), 822831. doi: 10.1016/j.neurobiolaging.2012.06.014.CrossRefGoogle ScholarPubMed
Sperling, R.A., Mormino, E.C., Schultz, A.P., Betensky, R.A., Papp, K.V., Amariglio, R.E., … Johnson, K.A. (2019). The impact of amyloid-beta and tau on prospective cognitive decline in older individuals. Annals of Neurology, 85(2), 181193. doi: 10.1002/ana.25395.Google ScholarPubMed
Storandt, M., Balota, D.A., Aschenbrenner, A.J., & Morris, J.C. (2014). Clinical and psychological characteristics of the initial cohort of the Dominantly Inherited Alzheimer Network (DIAN). Neuropsychology, 28(1), 1929. doi: 10.1037/neu0000030.CrossRefGoogle Scholar
Tariot, P.N., Lopera, F., Langbaum, J.B., Thomas, R.G., Hendrix, S., Schneider, L.S., … Initiative, A.S.P. (2018). The Alzheimer’s prevention initiative autosomal-dominant Alzheimer’s disease trial: a study of crenezumab versus placebo in preclinical. Alzheimers Dement (N Y), 4, 150160. doi: 10.1016/j.trci.2018.02.002.CrossRefGoogle ScholarPubMed
Torres, V.L., Vila-Castelar, C., Bocanegra, Y., Baena, A., Guzmán-Vélez, E., Aguirre-Acevedo, D.C., … Lopera, F. (2019). Normative data stratified by age and education for a Spanish neuropsychological test battery: results from the Colombian Alzheimer’s prevention initiative registry. Applied Neuropsychology: Adult, 115. doi: 10.1080/23279095.2019.1627357.Google ScholarPubMed
Tupler, L.A., Welsh, K.A., Asare-Aboagye, Y., & Dawson, D.V. (1995). Reliability of the Rey-Osterrieth Complex Figure in use with memory-impaired patients. J Clin Exp Neuropsychol, 17(4), 566579. doi: 10.1080/01688639508405146.CrossRefGoogle ScholarPubMed
Wang, F., Gordon, B.A., Ryman, D.C., Ma, S., Xiong, C., Hassenstab, J., … Network, D.I.A. (2015). Cerebral amyloidosis associated with cognitive decline in autosomal dominant Alzheimer disease. Neurology, 85(9), 790798. doi: 10.1212/WNL.0000000000001903.CrossRefGoogle ScholarPubMed
Zhao, Y., Tudorascu, D.L., Lopez, O.L., Cohen, A.D., Mathis, C.A., Aizenstein, H.J., … Snitz, B.E. (2018). Amyloid β deposition and suspected Non-Alzheimer Pathophysiology and Cognitive Decline Patterns for 12 years in oldest old participants without dementia. JAMA Neurology, 75(1), 8896. doi: 10.1001/jamaneurol.2017.3029.CrossRefGoogle ScholarPubMed