Neocortical origin and progression of gray matter atrophy in nonamnestic Alzheimer's disease
Open accessAbstract
Amnestic Alzheimer's disease (AD) is characterized by early atrophy of the hippocampus and medial temporal lobes before spreading to the neocortex. In contrast, nonamnestic Alzheimer's patients have relative sparing of the hippocampus, but the pattern in which the disease spreads is unclear. We examined spreading disease in nonamnestic AD using a novel magnetic resonance imaging-based analysis adapted from pathologic staging studies, applied here to cross-sectional imaging data. We selected 240 T1-weighted scans from 129 patients with pathology confirmed by autopsy or cerebrospinal fluid, and atrophy maps were computed relative to 238 scans from 115 elderly controls. For each phenotype, the frequency of atrophy in 116 brain regions was used to infer the anatomical origin of disease and its progression across 4 phases of atrophy. Results from the amnestic cohort were used to determine appropriate parameter settings for the phase assignment algorithm, based on correspondence to Braak pathology staging. Phase 1 regions, which represent the origin of disease, included the hippocampus for the amnestic group (comprising 33 scans); left lateral temporal lobe for logopenic-variant primary progressive aphasia (88 scans); occipitoparietal cortex for posterior cortical atrophy (51 scans); temporoparietal cortex for corticobasal syndrome (31 scans); and frontotemporal cortex for behavioral/dysexecutive variant AD (37 scans). In nonamnestic patients, atrophy spread to other neocortical areas in later phases, but the hippocampus exhibited only late-phase atrophy in posterior cortical atrophy and corticobasal syndrome. Region-specific phase values were also associated with regional measures of tau, beta amyloid, neuronal loss, and gliosis for the subset of patients (n = 17) with neuropathology findings; this comparison represented a first validation of the phase assignment algorithm. We subsequently assigned a phase to each patient scan based on the similarity of regional atrophy patterns with atrophy predicted for the corresponding phenotype at each phase. Scan-specific phases were correlated with disease duration as well as global and domain-specific cognition, supporting these phase values as global estimates of patients' disease progression. Logistic regression models based on spatial overlap with model-predicted atrophy patterns reliably discriminated nonamnestic phenotypes from each other and from amnestic AD. The frequency-based phase assignment algorithm used in the present study thus represents a promising approach for studying the neocortical origin and spread of disease in nonamnestic AD.
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Patients with LOAD often branch into distinct groups including slow versus rapid cognitive decliners, amnestic versus nonamnestic AD, executive versus cortical visual defect versus dysphasia-predominant AD, psychosis and depression-associated AD, and metabolic dysfunction-associated AD.
“For instance, patients with LOAD often branch into distinct groups including (i) slow versus rapid cognitive decliners (7), (ii) amnestic versus nonamnestic AD (8), (iii) executive versus cortical visual defect versus dysphasia-predominant AD (9), (iv) psychosis and depression-associated AD (10–12), and (v) metabolic dysfunction–associated AD modulated by abnormalities in insulin resistance, Hormo”
From Molecular subtyping of Alzheimer’s disease using RNA sequencing data reveals novel mechanisms and targets (2021) · cites this paper as [9]
The Methods (section 2.1) distinguish amnestic from nonamnestic AD, supporting the portion of the citing sentence attached to this source, citation (8). But the Limitations (section 4.6) say the amnestic reference group had a relatively young age of onset and caution against generalizing to typical late-onset AD (LOAD). The source therefore does not fully support the claim as framed specifically about LOAD. (LLM, conf=0.87)
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Neff, R. A., Wang, M., Vatansever, S., Guo, L., Ming, C., Wang, Q., Wang, E., Horgusluoglu-Moloch, E., Song, W.-M., Li, A., et al. (2021) · Science Advances · doi:10.1126/sciadv.abb5398 · Cited by 306 · see citing works
“For instance, patients with LOAD often branch into distinct groups including (i) slow versus rapid cognitive decliners (7), (ii) amnestic versus nonamnestic AD (8), (iii) executive versus cortical visual defect versus dysphasia-predominant AD (9), (iv) psychosis and depression-associated AD (10–12), and (v) metabolic…”
BackgroundFalgàs, N., Sánchez-Valle, R., Bargalló, N., Balasa, M., Fernández-Villullas, G., Bosch, B., Olives, J., Tort-Merino, A., Antonell, A., Muñoz-García, C., et al. (2019) · NeuroImage: Clinical · doi:10.1016/j.nicl.2019.101927 · Cited by 47 · see citing works
- Authors
- Phillips, J. S., Da Re, F., Dratch, L., Xie, S. X., Irwin, D. J., McMillan, C. T., Vaishnavi, S. N., Ferrarese, C., Lee, E. B., Shaw, L. M., Trojanowski, J. Q., Wolk, D. A., & Grossman, M.
- Affiliations
- University of Pennsylvania (US)
- University of Milano-Bicocca (IT)
- Corresponding author
- Phillips, Jeffrey S.
- ORCID
- Venue
- Neurobiology of Aging
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 63
- Pages
- 75-87
- ISSN
- 0197-4580 (ISSN-L)
- PMC
- PMC5801003
- OpenAlex
- W2769426437
- Cited by
- 74
- References
- 72
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 6 · 2023: 7 · 2022: 11 · 2021: 11 · 2020: 18 · 2019: 12 · 2018: 2 · 2016: 1
- FWCI
- 7.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neurobiology of Aging (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Funders
- Alzheimer's Association (AARF-16-443681)
- National Institutes of Health (AG017586, AG010124, AG043503, NS088341)
- BrightFocus Foundation (A2016244S))
- Dana Foundation
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- gray matter atrophy, disease progression, hippocampal sparing, posterior cortical atrophy, corticobasal syndrome, logopenic variant primary progressive aphasia, Braak staging, tau protein, amyloid-beta
- MeSH terms
- Aged, Alzheimer Disease, Atrophy, Female, Hippocampus, Humans, Male, Middle Aged, Retrospective Studies, Logistic Models, Disease Progression, Neocortex, Diffusion Magnetic Resonance Imaging, Gray Matter
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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