Neuroinflammation and Functional Connectivity in Alzheimer's Disease: Interactive Influences on Cognitive Performance
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Abstract
Neuroinflammation is a key part of the etio-pathogenesis of Alzheimer9s disease (AD). We tested the relationship between neuroinflammation and the disruption of functional connectivity in large-scale networks, and their joint influence on cognitive impairment. We combined [11C]PK11195 positron emission tomography (PET) and resting-state functional magnetic resonance imaging (rs-fMRI) in 28 patients (12 females/16 males) with clinical diagnosis of probable AD or mild cognitive impairment with positive PET biomarker for amyloid, and 14 age-, sex-, and education-matched healthy controls (8 females/6 males). Source-based “inflammetry” was used to extract principal components of [11C]PK11195 PET signal variance across all participants. rs-fMRI data were preprocessed via independent component analyses to classify neuronal and non-neuronal signals. Multiple linear regression models identified sources of signal covariance between neuroinflammation and brain connectivity profiles, in relation to the diagnostic group (patients, controls) and cognitive status. Patients showed significantly higher [11C]PK11195 binding relative to controls, in a distributed spatial pattern including the hippocampus, frontal, and inferior temporal cortex. Patients with enhanced loading on this [11C]PK11195 binding distribution displayed diffuse abnormal functional connectivity. The expression of a stronger association between such abnormal connectivity and higher levels of neuroinflammation correlated with worse cognitive deficits. Our study suggests that neuroinflammation relates to the pathophysiological changes in network function that underlie cognitive deficits in Alzheimer9s disease. Neuroinflammation, and its association with functionally-relevant reorganization of brain networks, is proposed as a target for emerging immunotherapeutic strategies aimed at preventing or slowing the emergence of dementia. SIGNIFICANCE STATEMENT Neuroinflammation is an important aspect of Alzheimer9s disease (AD), but it was not known whether the influence of neuroinflammation on brain network function in humans was important for cognitive deficit. Our study provides clear evidence that in vivo neuroinflammation in AD impairs large-scale network connectivity; and that the link between neuro inflammation and functional network connectivity is relevant to cognitive impairment. We suggest that future studies should address how neuroinflammation relates to network function as AD progresses, and whether the neuroinflammation in AD is reversible, as the basis of immunotherapeutic strategies to slow the progression of AD.
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AD patients show significantly increased regional TSPO ligand binding in the cortices compared to controls using TSPO-specific radiotracers.
“AD patients all showed significantly increased regional TSPO ligand binding in the cortices compared to controls.”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [134]
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“In association with cognitive deficits, by regulating large-scale brain networks, neuroinflammation is indicated to be correlated with the progression of AD [73].”
Background
- Authors
- Passamonti, L., Tsvetanov, K. A., Jones, P. S., Bevan-Jones, W. R., Arnold, R., Borchert, R. J., Mak, E., Su, L., O'Brien, J. T., & Rowe, J. B.
- Affiliations
- University of Cambridge (GB)
- MRC Cognition and Brain Sciences Unit (GB)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2019-07-18
- Volume
- 39
- Issue
- 36
- Pages
- 7218-7226
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6733539
- OpenAlex
- W2962369126
- Cited by
- 220
- References
- 55
- Citations by year
- 2026: 16 · 2025: 24 · 2024: 40 · 2023: 39 · 2022: 32 · 2021: 34 · 2020: 31 · 2019: 4
- FWCI
- 11.45
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- Eli Lilly and Company
- Wellcome Trust (103838/Z/14/Z, JBR 103838, 103838, 088324/Z/09/Z)
- National Institute for Health and Care Research (RG64473, 103838)
- British Academy (PF160048)
- Cambridge University Hospitals (146281)
- Medical Research Council (MR/P01271X/1, RG91365)
- NIHR Cambridge Biomedical Research Centre (RG64473)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- neuroinflammation, Alzheimer's disease, functional connectivity, large-scale brain networks, [11C]PK11195 PET, microglial activation, cognitive impairment, mild cognitive impairment, resting-state fMRI, network reorganization, immunotherapy
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Amides, Cerebral Cortex, Cognition, Female, Hippocampus, Humans, Inflammation, Isoquinolines, Magnetic Resonance Imaging, Male, Middle Aged, Radiopharmaceuticals, Positron-Emission Tomography, Connectome
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