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February 09, 2021; 96 (6) Article

Memory Resilience in Alzheimer Disease With Primary Progressive Aphasia

M.-Marsel Mesulam, View ORCID ProfileChristina Coventry, Alan Kuang, Eileen H. Bigio, Qinwen Mao, Margaret E. Flanagan, Tamar Gefen, Jaiashre Sridhar, Changiz Geula, Hui Zhang, Sandra Weintraub, Emily J. Rogalski
First published January 13, 2021, DOI: https://doi.org/10.1212/WNL.0000000000011397
M.-Marsel Mesulam
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Christina Coventry
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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  • ORCID record for Christina Coventry
Alan Kuang
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Eileen H. Bigio
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Qinwen Mao
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Margaret E. Flanagan
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Tamar Gefen
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Jaiashre Sridhar
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Changiz Geula
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Hui Zhang
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Sandra Weintraub
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Emily J. Rogalski
From the Mesulam Center for Cognitive Neurology and Alzheimer's Disease (M.-M.M., C.C., E.H.B., Q.M., M.E.F., T.G., J.S., C.G., H.Z., S.W., E.J.R.), Department of Preventive Medicine (A.K., H.Z.), Department of Pathology (E.H.B., Q.M., M.E.F.), and Department of Psychiatry and Behavioral Sciences (T.G., S.W., E.J.R.), Northwestern University Feinberg School of Medicine, Chicago. IL.
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Citation
Memory Resilience in Alzheimer Disease With Primary Progressive Aphasia
M.-Marsel Mesulam, Christina Coventry, Alan Kuang, Eileen H. Bigio, Qinwen Mao, Margaret E. Flanagan, Tamar Gefen, Jaiashre Sridhar, Changiz Geula, Hui Zhang, Sandra Weintraub, Emily J. Rogalski
Neurology Feb 2021, 96 (6) e916-e925; DOI: 10.1212/WNL.0000000000011397

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Abstract

Objective To determine whether memory is preserved longitudinally in primary progressive aphasia (PPA) associated with Alzheimer disease (AD) and to identify potential factors that maintain memory despite underlying neurofibrillary degeneration of mediotemporal memory areas.

Methods Longitudinal memory assessment was done in 17 patients with PPA with autopsy or biomarker evidence of AD (PPA-AD) and 14 patients with amnestic dementia of the Alzheimer type with AD at autopsy (DAT-AD).

Results In PPA-AD, episodic memory, tested with nonverbal items, was preserved at the initial testing and showed no decline at retesting 2.35 ± 0.78 years later, at which time symptoms had been present for 6.26 ± 2.21 years. In contrast, language functions declined significantly during the same period. In DAT-AD, both verbal memory and language declined with equal severity. Although imaging showed asymmetric left-sided mediotemporal atrophy in PPA-AD, autopsy revealed bilateral hippocampo-entorhinal neurofibrillary degeneration at Braak stages V and VI. Compared to DAT-AD, however, the PPA-AD group had lower incidence of APOE ε4 and of mediotemporal TAR DNA-binding protein 43 (TDP-43) pathology.

Conclusions Memory preservation in PPA is not just an incidental finding at onset but a core feature that persists for years despite the hippocampo-entorhinal AD neuropathology that is as severe as that of DAT-AD. Asymmetry of mediotemporal atrophy and a lesser impact of APOE ε4 and of TDP-43 on the integrity of memory circuitry may constitute some of the factors underlying this resilience. Our results also suggest that current controversies on memory in PPA-AD reflect inconsistencies in the diagnosis of logopenic PPA, the clinical variant most frequently associated with AD.

ClinicalTrials.gov Identifier NCT00537004 and NCT03371706.

Glossary

Aβ=
β-amyloid;
AD=
Alzheimer disease;
AQ=
Aphasia Quotient;
BNT=
Boston Naming Test;
CDR=
Clinical Dementia Rating;
DAT-AD=
amnestic dementia of the Alzheimer type with AD;
LPA=
logopenic progressive aphasia;
NFT=
neurofibrillary tangle;
PPA=
primary progressive aphasia;
RBMT=
Rivermead Behavioral Memory Test;
TDP-43=
TAR DNA-binding protein 43

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Editorial, page 243

  • Received July 1, 2020.
  • Accepted in final form September 25, 2020.
  • © 2021 American Academy of Neurology
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