The DOI matches its Crossref record; 30 of the 30 references it cites were found in a registry or an index.
Synaptic and neuritic alterations during the progression of Alzheimer's disease
Abstract
Extensive synaptic and neuritic alterations in the neocortex and limbic system are characteristically found in Alzheimer's disease (AD). However, it is not known how early in the development of the disease these alterations occur. For the present study, we compared the synaptic and neuritic alterations among cases classified clinically and neuropathologically as early, mild and advanced AD. In early AD there was a 20% loss of synaptophysin-immunoreactive presynaptic terminals in the outer molecular layer of the hippocampal dentate gyrus (but not in the neocortex and entorhinal cortex), accompanied by increased amyloid precursor protein (APP) and Alz50 immunoreactivity in hippocampal and entorhinal cortex pyramidal neurons. These results suggest that abnormal neuronal expression of APP and cytoskeletal proteins in early stages might be involved in the mechanisms of synaptic pathology in AD.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“which may be a result of our focus on the earliest stages of pathology and/or a dissociation between plaque load and function, which has been observed in other settings.21,60,62”
From Microglial INPP5D limits plaque formation and glial reactivity in the PSAPP mouse model of Alzheimer's disease (2023) · cites this paper as [21]
In the citing paper
“Remarkably, APP mutant neurons showed differential alterations in synaptic proteins [3] that resembled those that have been described in AD brain, such as early loss of the pre-synaptic protein synaptophysin [113, 163, 192] and the post-synaptic protein PSD-95 [63].”
From Intraneuronal β-amyloid accumulation and synapse pathology in Alzheimer’s disease (2010) · cites this paper as [113]
Citations
Cites
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123
Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., & Katzman, R. (1991) · Annals of Neurology · doi:10.1002/ana.410300410 · Cited by 4,397
Self-citationNeurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease
Arriagada, P. V., Growdon, J. H., Hedley-Whyte, E. T., & Hyman, B. T. (1992) · Neurology · doi:10.1212/wnl.42.3.631 · Cited by 2,668
Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity
DeKosky, S. T., & Scheff, S. W. (1990) · Annals of Neurology · doi:10.1002/ana.410270502 · Cited by 2,376
Milliken, G. A., & Johnson, D. E. (1992) · Thammasat University Digital Collections · Cited by 1,469
Some morphometric aspects of the brain in senile dementia of the alzheimer type
Terry, R. D., Peck, A., DeTeresa, R., Schechter, R., & Horoupian, D. S. (1981) · Annals of Neurology · doi:10.1002/ana.410100209 · Cited by 801
Self-citationPerforant pathway changes and the memory impairment of Alzheimer's disease
Hyman, B. T., Van Hoesen, G. W., Kromer, L. J., & Damasio, A. R. (1986) · Annals of Neurology · doi:10.1002/ana.410200406 · Cited by 672
Identification of normal and pathological aging in prospectively studied nondemented elderly humans
Dickson, D. W., Crystal, H. A., Mattiace, L. A., Masur, D. M., Blau, A. D., Davies, P., Yen, S.-H., & Aronson, M. K. (1992) · Neurobiology of Aging · doi:10.1016/0197-4580(92)90027-u · Cited by 643
Arriagada, P. V., Marzloff, K., & Hyman, B. T. (1992) · Neurology · doi:10.1212/wnl.42.9.1681 · Cited by 638
Crystal, H., Dickson, D., Fuld, P., Masur, D., Scott, R., Mehler, M., Masdeu, J., Kawas, C., Aronson, M., & Wolfson, L. (1988) · Neurology · doi:10.1212/wnl.38.11.1682 · Cited by 586
Cited by
Sorted by citations
Items 301–374 of 374
Brain Protein Oxidation and Modification for Good or for Bad in Alzheimer’s Disease
Rukhsana Sultana, A., & Butterfield, D. A. (2010) · Advances in neurobiology · doi:10.1007/978-1-4419-7104-3_17 · Cited by 4
Long‐term synaptic alteration in the rat hippocampal CA3 field following an entorhinal cortex lesion
Miwa, C., Ueki, A., Shinjo, H., Shimode, H., & Morita, Y. (2001) · Psychiatry and Clinical Neurosciences · doi:10.1046/j.1440-1819.2001.00908.x · Cited by 4
Compilation of all known protein changes in the human Alzheimer’s disease brainPreprint
Askenazi, M., Kavanagh, T., Pires, G., Ueberheide, B. M., Wısnıewskı, T., & Drummond, E. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.13.536828 · Cited by 4
Insights to develop tau‐directed therapeutics to protect the synaptic integrity for tauopathies
Cha, E., Kim, H. J., & Lim, S. M. (2023) · Bulletin of the Korean Chemical Society · doi:10.1002/bkcs.12792 · Cited by 4
Price, D. L., Borchelt, D., & Wong, P. C. (2005) · Elsevier eBooks · doi:10.1016/b978-012738903-5/50028-x · Cited by 3
Alzheimer disease and neuroplasticity: New approaches and new targets in pharmacotherapy
Uzbay, T. I. (2012) · MARMARA PHARMACEUTCAL JOURNAL · doi:10.12991/201216404 · Cited by 3
Jasmin, S. B. (2011) · eScholarship@McGill (McGill) · doi:10.82308/52384 · Cited by 3
Chapter 4. Emerging themes in Alzheimer's disease research: Paradigm shift in drug discovery
Morgan, T. E., & Krafft, G. A. (2002) · Annual reports in medicinal chemistry · doi:10.1016/s0065-7743(02)37005-2 · Cited by 3
Protein Carbonylation in Brains of Subjects with Selected Neurodegenerative Disorders
Reed, T. T., & Butterfield, D. A. (2017) · Wiley eBooks · doi:10.1002/9781119374947.ch8 · Cited by 3
Sarantseva, S. V., Kislik, G., Tkachenko, N., Vasiliev, A. N., & Schwarzman, A. L. (2012) · Cell and Tissue Biology · doi:10.1134/s1990519x12040104 · Cited by 2
Neural Regeneration as a Disease-Modifying Therapeutic Strategy for Alzheimer’s Disease
Kazim, S. F., & Iqbal, K. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803690-7.00002-8 · Cited by 2
ten Donkelaar, H. J. (2011) · Springer eBooks · doi:10.1007/978-3-642-19134-3_14 · Cited by 2
An Individualized Approach to Treatment for Alzheimer’s Disease, Pick’s Disease, and Other Dementias
Lippa, C. F. (2006) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317506292372 · Cited by 2
Autophagic and Lysosomal Disorders
Chandra, S., & Pahan, K. (2024) · Springer eBooks · doi:10.1007/978-3-031-68237-7_11 · Cited by 1
Amyloid β–dependent neuronal silencing through synaptic decoupling
Zhang, Y., Chen-Engerer, H.-J., Zhang, K., Zott, B., Varga, Z., Chen, Y., Chen, X., Hongbo, J., Sakmann, B. J., Nelken, I., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2515113122 · Cited by 2
Choline Modulation of the Aβ P1-40 Channel Reconstituted into a Model Lipid Membrane
Meleleo, D., Notarachille, G., & Micelli, S. (2010) · International Journal of Alzheimer s Disease · doi:10.4061/2010/752804 · Cited by 1
Alzheimer’s Disease and Mechanism-Based Attempts to Enhance Cognition
Draffin, J. E., Knafo, S., & Heneka, M. T. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-417042-1.00009-7 · Cited by 1
Butterfield, D. A., Rukhsana Sultana, A., & Poon, H. F. (2005) · Oxidative stress and disease · doi:10.1201/9781420026559.ch1 · Cited by 1
Treatment of Alzheimer's Disease (With or Without Cerebrovascular Disease)
Schneider, L. S., Qizilbash, N., Sano, M. C., Massoud, F., Kaye, J. A., Olin, J. T., Laake, K., Øksengaard, A. R., Oken, B., Yaffe, K. S., et al. (2003) · Wiley eBooks · doi:10.1002/9780470752340.ch34
Modeling Amyloid Diseases in Fruit Fly Drosophila Melanogaster
Sarantseva, S. V., & Schwarzm, A. (2011) · InTech eBooks · doi:10.5772/20102
Brain sterol metabolism : modulating Alzheimer’s disease
Vanmierlo, T. (2010) · Research Publications (Maastricht University) · doi:10.26481/dis.20100930tv
Swarowsky, A. (2009) · Americanae (AECID Library)
Memory, genes, and brain imaging : relating the APOE gene to brain function and structure
Lind, J. (2007) · Figshare
Hvoslef‐Eide, M. (2012) · ORCA Online Research @Cardiff (Cardiff University)
Ferreira, A. F. B. (2011) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2011.tde-04102011-161054
Drugs of Abuse and NeuroAIDS: Opiates
Rogers, T. J. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1071-7_22
TRAFFICKING OF α-SECRETASE ADAM10: NEW INSIGHTS INTO THE MOLECULAR MECHANISM OF MODULATION
Farmacologiche, S., Farmacia, F. D., Farmacotossicologiche, S., & Ciclo, X. (2011)
TRAFFICKING OF ALPHA SECRETASE ADAM10: NEW INSIGHTS INTO THE MOLECULAR MECHANISM OF MODULATION
Saraceno, C. (2012) · Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) · doi:10.13130/saraceno-claudia_phd2012-02-08
Hansson, K. (2018) · Gothenburg University Publications Electronic Archive (Gothenburg University)
Neurofilaments as biomarkers of neuronal damage
Pujol-Calderón, F. (2019)
Genetic and functional studies of genes involved in the pathogenesis of Alzheimer's disease
Natunen, T. (2014) · UEF eRepo (University of Eastern Finland)
Huang, Y. H., Jia, H., & Bao, W. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816475-4.00013-6
Kashani, A. (2006) · OpenGrey (Institut de l'Information Scientifique et Technique)
Studies on the use of glycosaminoglycans for the treatment of Alzheimer's Disease
Cui, H. (2012) · UTAS Research Repository · doi:10.25959/23206211
The role of N-truncated Aβ peptides in Alzheimer’s Disease
López‐Noguerola, J. S. (2018) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6949
Rujescu, D., & Jung, M. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.725966450.793557761
Zampar, S. (2021) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9004
Proteomics Analysis in Alzheimer's Disease: New Insights into Mechanisms of Neurodegeneration
Butterfield, D. A., & Rukhsana Sultana, A. (2007) · Springer eBooks · doi:10.1007/978-0-387-30377-2_13
Willis, M. A., & Haines, D. E. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-0294-1.00031-4
Exploring the ATN classification system using Brain MorphologyPreprint
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2022) · medRxiv · doi:10.1101/2022.06.01.22275839
Modelling the contributions to hyperexcitability in a mouse model of Alzheimer’s diseasePreprint
Mittag, M., Mediavilla, L., Remy, S., Cuntz, H., & Jedlička, P. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.29.494500
Cannabinoid-basierte Therapie in einem Modell für die sporadische Alzheimer-Erkrankung
Sichler, M. E. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9445
Horkulak, N. (2023) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-10060
Nussbaumer, J., Barve, A., Zufferey, V., Espourteille, J., Kirabali, T., Konietzko, U., Razansky, D., Rominger, A., Nordberg, A. K., Buée, L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.21.634009
Neurological aging and neurodegenerative disease in humans and great apes
Edler, M. K., Hearn, C. J., Guevara, E. E., Mhatre‐Winters, I., Varghese, M., Freire‐Cobo, C., Sherwood, C. C., Richardson, J. R., Raghanti, M. A., & Hof, P. R. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00074-9
Dietrich, K. (2015) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4863
Li, J.-Q., Bi, Y.-L., Shen, X.-N., Wang, H.-F., Xu, W., Tan, C.-C., Dong, Q., Wang, Y.-J., Tan, L., & Yu, J.-T. (2020) · Figshare · doi:10.6084/m9.figshare.13279377
Li, J.-Q., Bi, Y.-L., Shen, X.-N., Wang, H.-F., Xu, W., Tan, C.-C., Dong, Q., Wang, Y.-J., Tan, L., & Yu, J.-T. (2020) · Figshare · doi:10.6084/m9.figshare.13279368
Li, J.-Q., Bi, Y.-L., Shen, X.-N., Wang, H.-F., Xu, W., Tan, C., Dong, Q., Wang, Y.-J., Tan, L., & Yu, J.-T. (2020) · Figshare · doi:10.6084/m9.figshare.13279380
Additional file 4 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574865
Additional file 5 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574868
Li, J.-Q., Bi, Y.-L., Shen, X.-N., Wang, H.-F., Xu, W., Tan, C., Dong, Q., Wang, Y.-J., Tan, L., & Yu, J.-T. (2020) · Figshare · doi:10.6084/m9.figshare.13279374
Additional file 3 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maass, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.26574862
O’Dell, R. S., Mecca, A. P., Chen, M.-K., Naganawa, M., Toyonaga, T., Lu, Y., Godek, T. A., Harris, J. E., Bartlett, H. H., Banks, E. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13525170
Additional file 6 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574871
Additional file 10 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maass, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574883
O’Dell, R. S., Mecca, A. P., Chen, M.-K., Naganawa, M., Toyonaga, T., Lu, Y., Godek, T. A., Harris, J. E., Bartlett, H. H., Banks, E. R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.13525173
Additional file 8 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574877
Additional file 1 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574856
Additional file 2 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maass, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574859
Additional file 9 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574880
Additional file 7 of Exploring the ATN classification system using brain morphology
Heinzinger, N., Maaß, A., Berron, D., Yakupov, R., Peters, O., Fiebach, J. B., Villringer, K., Preis, L., Priller, J., Spruth, E. J., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26574874
Li, J.-Q., Bi, Y.-L., Shen, X.-N., Wang, H.-F., Xu, W., Tan, C.-C., Dong, Q., Wang, Y.-J., Tan, L., & Yu, J.-T. (2020) · Figshare · doi:10.6084/m9.figshare.13279371
Fatigue life of Malaysian hot mix asphalt mixes
Hainin, . R., Yaacob, H., & Haron, Z. (2013) · UTM Institutional Repository
Sepulveda-Diaz, J. E. (2013) · theses.fr (ABES) · doi:10.70675/56c42bcbz41dfz432bzbb78z77110b373285
Auboyer, L. (2018) · theses.fr (ABES) · doi:10.70675/07243ef7zb974z4ad8z97d9zd046801798b1
Physiological and pathological roles of the amyloid precursor protein at the presynapse
Jordá-Siquier, T. (2021) · theses.fr (ABES) · doi:10.70675/3bff9a77z3935z4d28zb02bz5b454bcbc77e
Identification et caractérisation fonctionnelle de nouveaux sites de clivage de la protéine Tau
Derisbourg, M. J. (2015) · theses.fr (ABES) · doi:10.70675/ef5f45b0zf4e8z433fz9beaz8d2cc6de65bc
Transcriptomic signatures of synaptic loss in Alzheimer’s disease
Sun, L., Yang, X., Xu, X., Kang, L., Zheng, Y., Huang, Q., Xu, W., Guan, Y., Shen, Y., Liu, J. S., et al. (2026) · iScience · doi:10.1016/j.isci.2026.116336
Friedman (2000) · doi:10.1002/1097-0029(20001001)51:1
Metadata
- Authors
- Masliah, E., Mallory, M., Hansen, L., Richard, D., Alford, M., & Terry, R.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Masliah, Eliezer
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 1994-06
- Volume
- 174
- Issue
- 1
- Pages
- 67-72
- ISSN
- 0304-3940 (ISSN-L)
- OpenAlex
- W2073518622
- Cited by
- 370
- References
- 30
- Citations by year
- 2026: 1 · 2025: 10 · 2024: 10 · 2023: 17 · 2022: 12 · 2021: 15 · 2020: 19 · 2019: 15 · 2018: 15 · 2017: 11 · 2016: 10 · 2015: 14 · 2014: 11 · 2013: 15 · 2012: 18
- FWCI
- 4.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ag008205-08, 5r01ag008201-05)
- National Institute on Aging (AG 08205, AG05131, P50AG005131, AG08201)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Alzheimer's disease, synaptic pathology, synaptophysin, presynaptic terminals, amyloid precursor protein, amyloid plaques, dentate gyrus, entorhinal cortex, hippocampus, pyramidal neurons, cytoskeletal proteins, disease progression
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Amyloid, Cerebral Cortex, Cytoskeleton, Hippocampus, Humans, Nerve Tissue Proteins, Synapses, Neurites, Synaptophysin, Pyramidal Cells, Entorhinal Cortex
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review