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The Topographical and Neuroanatomical Distribution of Neurofibrillary Tangles and Neuritic Plaques in the Cerebral Cortex of Patients with Alzheimer's Disease
Abstract
The distribution of neurofibrillary tangles (NFTs) and neuritic plaques (NPs) was mapped in 39 cortical areas of 11 brains of patients with Alzheimer's disease (AD). Whole hemisphere blocks were embedded in polyethylene glycol (Carbowax), sectioned coronally, and stained with thioflavin S and thionin. The densities of NFTs and NPs were assessed using a numerical rating scale for each area. Scores were grouped by type of cortex and by lobe for statistical analysis. Highly significant differences were obtained. For example, limbic periallocortex and allocortex had more NFTs than any other type of cortex. In descending order, the density of NFTs was as follows: periallocortex (area 28) greater than allocortex (subiculum/CA1 zones of hippocampal formation, area 51) greater than corticoid areas (accessory basal nucleus of amygdala, nucleus basalis of Meynert) greater than proisocortex (areas 11, 12, 24, 23, anterior insula, 38, 35) greater than nonprimary association cortex (32, 46, superior temporal sulcus, 40, 39, posterior parahippocampal cortex, 37, 36) greater than primary sensory association cortex (7, 18, 19, 22, 21, 20) greater than agranular cortex (44-5, 8, 6, 4) greater than primary sensory cortex (41-2, 3-1-2, 17). The laminar distribution of NFTs tended to be selective, involving primarily layers III and V of association areas and layers II and IV of limbic periallocortex. There were far more NFTs in both limbic and temporal lobes than in frontal, parietal, and occipital lobes. In general, NPs were more evenly distributed throughout the cortex, with the exceptions of limbic periallocortex and allocortex, which had notably fewer NPs than other cortical areas. Temporal and occipital lobes had the highest NP densities, limbic and frontal lobes had the lowest, and parietal lobe was intermediate. No significant left-right hemispheric differences for NFT or NP densities were found across the population, and there was no relationship between duration of illness and densities of NFTs or NPs. The regional and laminar distribution of NFTs (and, to a lesser degree, that of NPs) suggests a consistent pattern of vulnerability within the cerebral cortices that seems correlated to the hierarchies of cortico-cortical connections. The higher-order association cortices, especially those in the anterior and ventromedial sectors of temporal lobe, are the most vulnerable, while other cortices appear less vulnerable to a degree commensurate with their connectional "distance" (i.e., synapses removed) from the limbic areas.
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In the citing paper
“The EC is affected severely in Alzheimer disease (AD), likely contributing to memory impairment.”
From Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease (1996) · cites this paper as Arnold et al., 1991
In the citing paper
“The EC was chosen because it is highly selectively vulnerable in AD (Hyman et al., 1984(Hyman et al., , 1986;;Arnold et al., 1991;Braak and Braak, 1991;Price et al., 1991;Arriagada et al., 1992a;Fukutani et al., 1995;Solodkin and Van Hoesen, 1996).”
From Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease (1996) · cites this paper as Arnold et al., 1991
In the citing paper
“The midfrontal gyrus cortex (corresponding predominantly to Brodmann area 46) was chosen for semi-quantitative image analyses of AD pathology, cellular and synaptic markers because of its important role in complex cognition and its common neuropathological involvement in the spectrum of AD (Arnold, et al., 1991).”
From Cellular, synaptic, and biochemical features of resilient cognition in Alzheimer’s disease (2013) · cites this paper as Arnold, et al., 1991
In the citing paper
“as this region is the first area of the brain involved by the neurofibrillary pathology of AD(4, 5).”
From Rates of hippocampal atrophy correlate with change in clinical status in aging and AD (2000) · cites this paper as [5]
In the citing paper
“We consider it to be an important clue that most brains from elderly human subjects show abnormalities that fall somewhere along particular continua of pathologic severity (60, 96-100).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [100]
In the citing paper
“In the early stages of Alzheimer’s disease (AD), the most common form of age-related dementia, clinical symptoms (such as memory loss) are caused by the selective degeneration of principal neurons of the entorhinal cortex layer II (ECII), followed by CA1 pyramidal cells in the hippocampus, and pyramidal neurons in neocortical association areas.”
From Selective Neuronal Vulnerability in Alzheimer’s Disease: A Network-Based Analysis (2020) · cites this paper as Arnold et al., 1991
In the citing paper
“In contrast, other brain regions, such as the primary sensory cortices, are relatively resistant to degeneration until later stages of the disease (Arnold et al., 1991; Bussière et al., 2003; Fukutani et al., 2000; Gómez-Isla et al., 1996; Hof and Morrison, 1990; Hyman et al., 1984; Morrison and Hof, 1997; West et al., 1994).”
From Selective Neuronal Vulnerability in Alzheimer’s Disease: A Network-Based Analysis (2020) · cites this paper as Arnold et al., 1991
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Delayed ischaemia after subarachnoid haemorrhage: a role for small vessel changes.
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α2‐Macroglobulin Receptor/Low Density Lipoprotein Receptor—Related Protein
Hyman, B. T., Strickland, D. K., & Rebeck, G. W. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb44303.x · Cited by 10
Self-citationTherapeutic potential and microRNA regulating properties of phytochemicals in Alzheimer’s disease
Kumari, A., Rahaman, A., Zeng, X., & Baloch, Z. (2024) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2024.102439 · Cited by 9
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Whatever Happened to Pittsburgh Compound-A?
Klunk, W. E., & Mathis, C. A. (2008) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0b013e318188c0c8 · Cited by 9
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Metadata
- Authors
- Arnold, S. E., Hyman, B. T., Flory, J., Damasio, A. R., & Van Hoesen, G. W.
- Affiliations
- University of Iowa (US)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 1991-01-01
- Volume
- 1
- Issue
- 1
- Pages
- 103-116
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2029923284
- Cited by
- 1,380
- References
- 0
- Citations by year
- 2026: 15 · 2025: 32 · 2024: 32 · 2023: 34 · 2022: 31 · 2021: 45 · 2020: 36 · 2019: 41 · 2018: 47 · 2017: 43 · 2016: 42 · 2015: 40 · 2014: 42 · 2013: 54 · 2012: 42
- FWCI
- 19.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service (P019632)
- National Institute on Aging (AG-08487)
- National Institute of Neurological Disorders and Stroke (R01NS014944, NS-14944)
- 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 › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, neurofibrillary tangles, neuritic plaques, cortical topography, neuroanatomy, allocortex, temporal lobe, occipital lobe, frontal lobe, parietal lobe, laminar distribution, thioflavin S, thionin, amygdala, nucleus basalis of Meynert
- MeSH terms
- Aged, Alzheimer Disease, Brain Mapping, Cerebral Cortex, Female, Histocytochemistry, Humans, Male, Middle Aged, Neurites, Tissue Embedding, Neurofibrillary Tangles
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