Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship

Nelson, Peter T.; Braak, Heiko; Markesbery, William R.

doi:10.1097/nen.0b013e3181919a48

Cited by 643Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship

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Nelson, Peter T., Braak, Heiko, Markesbery, William R.·2009·Journal of Neuropathology & Experimental Neurology

DOI 10.1097/nen.0b013e3181919a48PMC PMC2692822

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Abstract

Amyloid plaques and neurofibrillary tangles (NFTs) are the pathological hallmarks of Alzheimer disease (AD). There is controversy regarding the use of current diagnostic criteria for AD and whether amyloid plaques and NFTs contribute to cognitive impairment. Because AD is specific to humans, rigorous and comprehensiveclinicopathologic studies are necessary to test and refine hypotheses of AD diagnosis and pathogenesis. Neither the clinical nor the pathological aspects of AD evolve in a linear manner, but thepredictable sequence of AD pathology allows for stage-based correlations with cognitive deterioration. We discuss subsets of patients with clinical dementia who lack amyloid plaques and NFTs and, conversely, whether individuals without antemortem cognitive impairment can harbor severe AD-type pathological findings at autopsy. There are many medical, technical, and anatomical challenges to clinicopathologic studies in AD. For example, at least two thirds of persons older than 80 years have non-AD brain diseases that can effect on cognitive function. We argue that existing data strongly support the hypothesis that both amyloid plaques and NFTs contribute to cognitive impairment.

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The accumulation of senile plaques and neurofibrillary tangles causes synaptic dysfunction, synapse loss, and eventual neuronal death.
“leading to dysfunction and loss of synapses and eventual neuronal death1,2.”
From Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease (2019) · cites this paper as [1]
In “The Neuritic Plaque: A Pathological Entity With Strong Mechanistic Implications” (page unavailable), the paper says neuritic plaques involve degenerating nerve-cell processes and that amyloid plaque pathology induces neurofibrillary pathology and apparent structural and functional disruption. In “Nonlinear clinicopathological correlations” (page unavailable), it suggests these changes may impair function before cell death. It does not establish the claimed sequence of synaptic dysfunction, synapse loss, and eventual neuronal death as a definite consequence of plaque and tangle accumulation. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Alzheimer disease is characterized by brain accumulation of senile plaques, composed mainly of fibrillary amyloid beta-peptide and dystrophic neurites, and neurofibrillary tangles, composed of hyperphosphorylated tau.
“AD is characterized by an accumulation of senile plaques (SP) [composed mostly of fibrillary amyloid beta-peptide (Aβ) and dystrophic neurites] and neurofibrillary tangles (NFT) [composed of hyperphosphorylated tau protein] in the brain”
From Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease (2019) · cites this paper as [1]
Table 1 and the Figure 1 caption (both indexed under Summary and Conclusions; page unavailable) describe AD amyloid plaques as having a fibrillary amyloid-peptide core and neuritic plaques as surrounded by degenerating neurites. The caption says neurofibrillary tangles are composed of tau fibrils, but the available passages do not specify that the tau is hyperphosphorylated. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Alzheimer disease clinically involves progressive cognitive decline with memory loss and impaired higher executive function.
“Clinically, AD is characterized by several features, notably a progressive cognitive decline involving loss of memory and higher executive functioning1.”
From Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease (2019) · cites this paper as [1]
Evaluation of AD status was conducted using National Institute on Aging Reagan Institute guidelines including evaluation of neurofibrillary tangles and neuritic senile plaques.
“Evaluation of AD status was conducted by the AD Center Neuropathology and Clinical Cores using guidelines set forth by the National Institute on Aging Reagan Institute that included evaluation of neurofibrillary tangles and neuritic senile plaques [36–38].”
From Predominant expression of Alzheimer’s disease-associated BIN1 in mature oligodendrocytes and localization to white matter tracts (2016) · cites this paper as [37]
The earliest pathological damage to neurons in Alzheimer disease and amnestic mild cognitive impairment occurs at pre- and post-synaptic membranes.
“Indeed, the first pathological insults to neurons in AD and aMCI occur at pre- and post-synaptic membranes1,3.”
From Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease (2019) · cites this paper as [1]
The discussion of early Alzheimer pathology describes where plaques and neurofibrillary tangles appear in the brain, but does not identify pre- or postsynaptic membranes as the sites of the first neuronal insults. Searches for synapses, synaptic membranes, and early damage in Alzheimer disease and mild cognitive impairment found no passage in our copy establishing that claim. (LLM, conf=0.72)
Experimental — accuracy not yet measured

This modeled expectation is precisely the observation reported by one of the largest autopsy series to date and is well supported by AD biomarker studies.
“Indeed, this is precisely the observation reported by one of the largest autopsy series to date (142) and is well supported by AD biomarker studies (143-145).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
It is expected that many persons die with brains that exhibit AD neuropathologic change in the preclinical phase of AD; data support the modeled expectations.
“It is expected that many persons die with brains that exhibit AD neuropathologic change in the preclinical phase of AD; indeed, data support the modeled expectations (44, 142).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
Among thousands of cases from dozens of clinicopathologic studies worldwide, there has never been a report of a thoroughly documented individual with truly end-stage neocortical neurofibrillary tangle pathology who lacked antemortem cognitive impairment proximal to death.
“It is important to emphasize that, among thousands of cases from dozens of CPC studies worldwide, there never has been a report of a thoroughly documented individual with truly “end-stage” neocortical NFT pathology who lacked antemortem cognitive impairment proximal to death (142, 151).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
Among 555 subjects without dementia from 11 studies, 12 brains (2.2%) were assessed as Braak stage V.
“In a review of 11 different studies comprising 555 subjects without dementia, a total of 12 brains were assessed as Braak stage V (2.2%); 3 were assessed as Braak stage VI (0.5%) (142).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
There was significant variation in neurofibrillary tangle burden among Braak stage VI cases.
“However, not all Braak stage VI brains were the same; there was significant variation in NFT burden in these cases (142, 151).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
Among 555 subjects without dementia from 11 studies, 3 brains (0.5%) were assessed as Braak stage VI.
“In a review of 11 different studies comprising 555 subjects without dementia, a total of 12 brains were assessed as Braak stage V (2.2%); 3 were assessed as Braak stage VI (0.5%) (142).”
From Correlation of Alzheimer Disease Neuropathologic Changes With Cognitive Status: A Review of the Literature (2012) · cites this paper as [142]
Many clinicopathological studies have correlated amyloid plaques with cognitive deficits in AD, with the strongest correlation in the earliest stages of the disease and this association greatly weakens as NFTs and neocortical degeneration become more widespread.
“There have been many clinicopathological studies that have correlated amyloid plaques with cognitive deficits in AD, with an emerging picture that the strongest correlation exists in the earliest stages of the disease and this association greatly weakens as NFTs and neocortical degeneration become more widespread [9, 102, 103, 157, 160, 169].”
From Alzheimer's disease: experimental models and reality (2017) · cites this paper as [103]

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Braak H, Braak E. Staging of Alzheimer's diseaseYrelated neuro- fibrillary changes. Neurobiol Aging 1995;16:271Y8;[discussion 8-84]
Centers for Disease Control and Prevention. Prevalence of strokeV United States, 2005. MMWR Morb Mortal Wkly Rep 2007;56: 469Y74

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Authors: Nelson, P. T., Braak, H., & Markesbery, W. R.
Affiliations: University of Kentucky HealthCare (US)
University of Kentucky (US)
Corresponding author: Nelson, Peter T.
ORCID: Nelson, Peter T.
Braak, Heiko
Venue: Journal of Neuropathology & Experimental Neurology
Publisher: Oxford University Press (OUP)
Published: 2009-01
Volume: 68
Issue: 1
Pages: 1-14
ISSN: 0022-3069 (ISSN-L)
1554-6578
DOI: 10.1097/nen.0b013e3181919a48
PMC: PMC2692822
OpenAlex: W1985747467
Cited by: 643
References: 155
Citations by year: 2026: 21 · 2025: 43 · 2024: 48 · 2023: 46 · 2022: 33 · 2021: 45 · 2020: 44 · 2019: 33 · 2018: 32 · 2017: 32 · 2016: 37 · 2015: 32 · 2014: 35 · 2013: 42 · 2012: 41
FWCI: 2.81
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuropathology & Experimental Neurology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Deutsche Forschungsgemeinschaft
National Institutes of Health (AG028 383)
National Institute on Aging (P30AG028383)
National Institute of Neurological Disorders and Stroke (R01NS061933, K08NS050110)
Topics: Health Sciences › Medicine › Physiology › 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, amyloid plaques, neurofibrillary tangles, cognitive impairment, clinicopathological correlation, Alzheimer's disease diagnosis, Alzheimer disease pathogenesis, autopsy findings
MeSH terms: Alzheimer Disease, Cognition Disorders, Humans, Neurofibrillary Tangles, Plaque, Amyloid

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Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship

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