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Cited by 243Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsFunctional Brain Connectivity Studies

Atrophy patterns in early clinical stages across distinct phenotypes of A lzheimer's disease

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Ossenkoppele, Rik, Cohn‐Sheehy, Brendan I., La Joie, Renaud, Vogel, Jacob W., Möller, Christiane, Lehmann, Manja, van Berckel, Bart N.M., Seeley, William W. +10 more·2015·Human Brain Mapping
DOI 10.1002/hbm.22927PMC PMC4692964
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Abstract

Alzheimer's disease (AD) can present with distinct clinical variants. Identifying the earliest neurodegenerative changes associated with each variant has implications for early diagnosis, and for understanding the mechanisms that underlie regional vulnerability and disease progression in AD. We performed voxel‐based morphometry to detect atrophy patterns in early clinical stages of four AD phenotypes: Posterior cortical atrophy (PCA, “visual variant,” n = 93), logopenic variant primary progressive aphasia (lvPPA, “language variant,” n = 74), and memory‐predominant AD categorized as early age‐of‐onset (EOAD, <65 years, n = 114) and late age‐of‐onset (LOAD, >65 years, n = 114). Patients with each syndrome were stratified based on: (1) degree of functional impairment, as measured by the clinical dementia rating (CDR) scale, and (2) overall extent of brain atrophy, as measured by a neuroimaging approach that sums the number of brain voxels showing significantly lower gray matter volume than cognitively normal controls ( n = 80). Even at the earliest clinical stage (CDR = 0.5 or bottom quartile of overall atrophy), patients with each syndrome showed both common and variant‐specific atrophy. Common atrophy across variants was found in temporoparietal regions that comprise the posterior default mode network (DMN). Early syndrome‐specific atrophy mirrored functional brain networks underlying functions that are uniquely affected in each variant: Language network in lvPPA, posterior cingulate cortex‐hippocampal circuit in amnestic EOAD and LOAD, and visual networks in PCA. At more advanced stages, atrophy patterns largely converged across AD variants. These findings support a model in which neurodegeneration selectively targets both the DMN and syndrome‐specific vulnerable networks at the earliest clinical stages of AD. Hum Brain Mapp 36:4421–4437, 2015 . © 2015 Wiley Periodicals, Inc .

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  • Studies have demonstrated that executive or behavioral dysfunction typically develop after memory deficits in fvAD.

    “While not apparent in our cases, studies have demonstrated that executive or behavioral dysfunction typically develop after memory deficits in fvAD [1, 22, 23].”

    From Diagnosing the frontal variant of Alzheimer’s disease: a clinician’s yellow brick road (2017) · cites this paper as [23]

    The Results (Participants and Neuropsychological Scores; page unavailable) describe memory-predominant profiles in early- and late-onset AD. The Discussion (Neuropsychological Features and Atrophy Patterns; page unavailable) reports later decline in non-memory functions, particularly in early-onset AD. The paper does not study fvAD or establish that executive or behavioral dysfunction typically follows memory deficits in that phenotype. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • In fvAD, memory impairment is the first abnormality in up to 85% of patients, with the remainder developing memory impairment within 3 years from symptom onset.

    “Conversely, in fvAD memory impairment is the first abnormality in up to 85% of patients (Fig. 4), with the remainder developing memory impairment within 3 years from symptom onset [1, 22, 23].”

    From Diagnosing the frontal variant of Alzheimer’s disease: a clinician’s yellow brick road (2017) · cites this paper as [23]

    The Introduction says amnesia is the most common presenting symptom of Alzheimer’s disease generally, but the paper studies PCA, lvPPA, EOAD and LOAD—not fvAD. Searches for fvAD, the 85% figure and memory impairment within three years found no passage addressing those claims in our copy; section pages were not provided. (LLM, conf=0.75)

    Experimental — accuracy not yet measured

  • In fvAD there is greater temporal than frontal atrophy, particularly in the perisylvian area compared to bvFTD.

    “In fvAD there is greater temporal than frontal atrophy, particularly in the perisylvian area compared to bvFTD [21, 33].”

    From Diagnosing the frontal variant of Alzheimer’s disease: a clinician’s yellow brick road (2017) · cites this paper as [33]

    The Results (Voxel Based Morphometry: AD Variants Versus Controls; page unavailable) describe temporal and temporoparietal atrophy in the AD phenotypes studied, but do not examine frontal-variant AD (fvAD) or compare it with bvFTD. Searches for fvAD, bvFTD, perisylvian atrophy, and the frontal-versus-temporal comparison found no passage addressing the cited claim. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

  • In bvFTD, frontal regions are more affected, particularly the anterior cingulate, orbitofrontal cortex, middle and superior frontal gyrus.

    “In bvFTD, frontal regions are more affected, particularly the anterior cingulate, orbitofrontal cortex, middle and superior frontal gyrus [21, 33].”

    From Diagnosing the frontal variant of Alzheimer’s disease: a clinician’s yellow brick road (2017) · cites this paper as [33]

    The Results (Voxel Based Morphometry: AD Variants Versus Controls; page unavailable) describe atrophy in Alzheimer’s disease variants, not bvFTD. Searches for bvFTD and the named frontal regions found no passage reporting the claimed pattern; a bvFTD study appears only in the References. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

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Authors
Ossenkoppele, R., Cohn‐Sheehy, B. I., La Joie, R., Vogel, J. W., Möller, C., Lehmann, M., van Berckel, B. N. M., Seeley, W. W., Pijnenburg, Y. A., Gorno‐Tempini, M. L., Kramer, J. H., Barkhof, F., Rosen, H. J., van der Flier, W. M., Jagust, W. J., Miller, B. L., Scheltens, P., & Rabinovici, G. D.
Affiliations
  • University of California, San Francisco (US)
  • Helen Wills Neuroscience Institute, University of California Berkeley Berkeley California
  • University of California, Berkeley (US)
  • Amsterdam Neuroscience (NL)
  • Gemeente Amsterdam (NL)
  • Department of Neurology &amp; Alzheimer Center Neuroscience Campus Amsterdam, VU University Medical Center Amsterdam The Netherlands
ORCID
Venue
Human Brain Mapping
Publisher
Wiley
Published
2015-08-11
Volume
36
Issue
11
Pages
4421-4437
ISSN
  • 1065-9471 (ISSN-L)
  • 1097-0193
DOI
10.1002/hbm.22927
PMC
PMC4692964
OpenAlex
W1935126539
Cited by
243
References
70
Citations by year
2026: 14 · 2025: 18 · 2024: 19 · 2023: 18 · 2022: 21 · 2021: 21 · 2020: 34 · 2019: 32 · 2018: 27 · 2017: 24 · 2016: 12 · 2015: 2 · 2014: 1
FWCI
17.60
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Human Brain Mapping (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • Pure Amsterdam UMC (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Funders
  • Marie Curie FP7 International Outgoing Fellowship (628812)
  • The donors of [Alzheimer's Disease Research], a program of BrightFocus Foundation
  • National Institute on Aging grants (R01-AG045611, P01-AG1792403, P50-AG023501, R01-AG034570)
  • Tau Consortium
  • Consortium for Frontotemporal Dementia Research
  • John Douglas French Alzheimer's Foundation
  • State of California Department of Health Services Alzheimer's Disease Research Centre of California (04-33516)
  • Netherlands Initiative Brain and Cognition (NIHC), a part of the Netherlands Organization for Scientific Research (NWO) (056-13-001)
  • Alzheimer Nederland and Stichting VUMC funds and Stichting Dioraphte
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
Alzheimer's disease, brain atrophy patterns, posterior cortical atrophy, logopenic variant primary progressive aphasia, posterior default mode network, language network, visual network, gray matter volume, Clinical Dementia Rating, early diagnosis, regional vulnerability
MeSH terms
Aged, Alzheimer Disease, Animals, Atrophy, Cerebral Cortex, Female, Humans, Male, Middle Aged, Nerve Net, Phenotype, Syndrome, Age of Onset, Aphasia, Primary Progressive

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