Principal component analysis of synaptic density measured with [11C]UCB-J PET in early Alzheimer’s disease

•This is the first application of PCA to synaptic density PET in Alzheimer’s disease.•Principal components reflect spatial patterns of covariance in synaptic density.•Principal components are correlated with unique characteristics in Alzheimer’s disease.•These findings support synaptic density as a...

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Published in:NeuroImage clinical Vol. 39; p. 103457
Main Authors: O'Dell, Ryan S., Higgins-Chen, Albert, Gupta, Dhruva, Chen, Ming-Kai, Naganawa, Mika, Toyonaga, Takuya, Lu, Yihuan, Ni, Gessica, Chupak, Anna, Zhao, Wenzhen, Salardini, Elaheh, Nabulsi, Nabeel B., Huang, Yiyun, Arnsten, Amy F.T., Carson, Richard E., van Dyck, Christopher H., Mecca, Adam P.
Format: Journal Article
Language:English
Published: Netherlands Elsevier Inc 01.01.2023
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ISSN:2213-1582, 2213-1582
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Abstract •This is the first application of PCA to synaptic density PET in Alzheimer’s disease.•Principal components reflect spatial patterns of covariance in synaptic density.•Principal components are correlated with unique characteristics in Alzheimer’s disease.•These findings support synaptic density as a robust biomarker of disease severity. Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer’s disease (AD). We used principal component analysis (PCA) to identify regional patterns of covariance in synaptic density using [11C]UCB-J PET and assessed the association between principal components (PC) subject scores with cognitive performance. [11C]UCB-J binding was measured in 45 amyloid + participants with AD and 19 amyloid– cognitively normal participants aged 55–85. A validated neuropsychological battery assessed performance across five cognitive domains. PCA was applied to the pooled sample using distribution volume ratios (DVR) standardized (z-scored) by region from 42 bilateral regions of interest (ROI). Parallel analysis determined three significant PCs explaining 70.2% of the total variance. PC1 was characterized by positive loadings with similar contributions across the majority of ROIs. PC2 was characterized by positive and negative loadings with strongest contributions from subcortical and parietooccipital cortical regions, respectively, while PC3 was characterized by positive and negative loadings with strongest contributions from rostral and caudal cortical regions, respectively. Within the AD group, PC1 subject scores were positively correlated with performance across all cognitive domains (Pearson r = 0.24–0.40, P = 0.06–0.006), PC2 subject scores were inversely correlated with age (Pearson r = -0.45, P = 0.002) and PC3 subject scores were significantly correlated with CDR-sb (Pearson r = 0.46, P = 0.04). No significant correlations were observed between cognitive performance and PC subject scores in CN participants. This data-driven approach defined specific spatial patterns of synaptic density correlated with unique participant characteristics within the AD group. Our findings reinforce synaptic density as a robust biomarker of disease presence and severity in the early stages of AD.
AbstractList Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer's disease (AD). We used principal component analysis (PCA) to identify regional patterns of covariance in synaptic density using [ C]UCB-J PET and assessed the association between principal components (PC) subject scores with cognitive performance. [ C]UCB-J binding was measured in 45 amyloid + participants with AD and 19 amyloid- cognitively normal participants aged 55-85. A validated neuropsychological battery assessed performance across five cognitive domains. PCA was applied to the pooled sample using distribution volume ratios (DVR) standardized (z-scored) by region from 42 bilateral regions of interest (ROI). Parallel analysis determined three significant PCs explaining 70.2% of the total variance. PC1 was characterized by positive loadings with similar contributions across the majority of ROIs. PC2 was characterized by positive and negative loadings with strongest contributions from subcortical and parietooccipital cortical regions, respectively, while PC3 was characterized by positive and negative loadings with strongest contributions from rostral and caudal cortical regions, respectively. Within the AD group, PC1 subject scores were positively correlated with performance across all cognitive domains (Pearson r = 0.24-0.40, P = 0.06-0.006), PC2 subject scores were inversely correlated with age (Pearson r = -0.45, P = 0.002) and PC3 subject scores were significantly correlated with CDR-sb (Pearson r = 0.46, P = 0.04). No significant correlations were observed between cognitive performance and PC subject scores in CN participants. This data-driven approach defined specific spatial patterns of synaptic density correlated with unique participant characteristics within the AD group. Our findings reinforce synaptic density as a robust biomarker of disease presence and severity in the early stages of AD.
Background: Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer’s disease (AD). We used principal component analysis (PCA) to identify regional patterns of covariance in synaptic density using [11C]UCB-J PET and assessed the association between principal components (PC) subject scores with cognitive performance. Methods: [11C]UCB-J binding was measured in 45 amyloid + participants with AD and 19 amyloid– cognitively normal participants aged 55–85. A validated neuropsychological battery assessed performance across five cognitive domains. PCA was applied to the pooled sample using distribution volume ratios (DVR) standardized (z-scored) by region from 42 bilateral regions of interest (ROI). Results: Parallel analysis determined three significant PCs explaining 70.2% of the total variance. PC1 was characterized by positive loadings with similar contributions across the majority of ROIs. PC2 was characterized by positive and negative loadings with strongest contributions from subcortical and parietooccipital cortical regions, respectively, while PC3 was characterized by positive and negative loadings with strongest contributions from rostral and caudal cortical regions, respectively. Within the AD group, PC1 subject scores were positively correlated with performance across all cognitive domains (Pearson r = 0.24–0.40, P = 0.06–0.006), PC2 subject scores were inversely correlated with age (Pearson r = -0.45, P = 0.002) and PC3 subject scores were significantly correlated with CDR-sb (Pearson r = 0.46, P = 0.04). No significant correlations were observed between cognitive performance and PC subject scores in CN participants. Conclusions: This data-driven approach defined specific spatial patterns of synaptic density correlated with unique participant characteristics within the AD group. Our findings reinforce synaptic density as a robust biomarker of disease presence and severity in the early stages of AD.
Highlights•This is the first application of PCA to synaptic density PET in Alzheimer’s disease. •Principal components reflect spatial patterns of covariance in synaptic density. •Principal components are correlated with unique characteristics in Alzheimer’s disease. •These findings support synaptic density as a robust biomarker of disease severity.
• This is the first application of PCA to synaptic density PET in Alzheimer’s disease. • Principal components reflect spatial patterns of covariance in synaptic density. • Principal components are correlated with unique characteristics in Alzheimer’s disease. • These findings support synaptic density as a robust biomarker of disease severity.
•This is the first application of PCA to synaptic density PET in Alzheimer’s disease.•Principal components reflect spatial patterns of covariance in synaptic density.•Principal components are correlated with unique characteristics in Alzheimer’s disease.•These findings support synaptic density as a robust biomarker of disease severity. Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer’s disease (AD). We used principal component analysis (PCA) to identify regional patterns of covariance in synaptic density using [11C]UCB-J PET and assessed the association between principal components (PC) subject scores with cognitive performance. [11C]UCB-J binding was measured in 45 amyloid + participants with AD and 19 amyloid– cognitively normal participants aged 55–85. A validated neuropsychological battery assessed performance across five cognitive domains. PCA was applied to the pooled sample using distribution volume ratios (DVR) standardized (z-scored) by region from 42 bilateral regions of interest (ROI). Parallel analysis determined three significant PCs explaining 70.2% of the total variance. PC1 was characterized by positive loadings with similar contributions across the majority of ROIs. PC2 was characterized by positive and negative loadings with strongest contributions from subcortical and parietooccipital cortical regions, respectively, while PC3 was characterized by positive and negative loadings with strongest contributions from rostral and caudal cortical regions, respectively. Within the AD group, PC1 subject scores were positively correlated with performance across all cognitive domains (Pearson r = 0.24–0.40, P = 0.06–0.006), PC2 subject scores were inversely correlated with age (Pearson r = -0.45, P = 0.002) and PC3 subject scores were significantly correlated with CDR-sb (Pearson r = 0.46, P = 0.04). No significant correlations were observed between cognitive performance and PC subject scores in CN participants. This data-driven approach defined specific spatial patterns of synaptic density correlated with unique participant characteristics within the AD group. Our findings reinforce synaptic density as a robust biomarker of disease presence and severity in the early stages of AD.
ArticleNumber 103457
Author Lu, Yihuan
Nabulsi, Nabeel B.
Salardini, Elaheh
Zhao, Wenzhen
Toyonaga, Takuya
Arnsten, Amy F.T.
Gupta, Dhruva
Naganawa, Mika
Ni, Gessica
Chen, Ming-Kai
Carson, Richard E.
Chupak, Anna
van Dyck, Christopher H.
Huang, Yiyun
Higgins-Chen, Albert
Mecca, Adam P.
O'Dell, Ryan S.
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  surname: O'Dell
  fullname: O'Dell, Ryan S.
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  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
– sequence: 2
  givenname: Albert
  surname: Higgins-Chen
  fullname: Higgins-Chen, Albert
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Dhruva
  surname: Gupta
  fullname: Gupta, Dhruva
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Ming-Kai
  surname: Chen
  fullname: Chen, Ming-Kai
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
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  givenname: Mika
  surname: Naganawa
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  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
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  givenname: Takuya
  surname: Toyonaga
  fullname: Toyonaga, Takuya
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
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  givenname: Yihuan
  surname: Lu
  fullname: Lu, Yihuan
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
– sequence: 8
  givenname: Gessica
  surname: Ni
  fullname: Ni, Gessica
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Anna
  surname: Chupak
  fullname: Chupak, Anna
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Wenzhen
  surname: Zhao
  fullname: Zhao, Wenzhen
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Elaheh
  surname: Salardini
  fullname: Salardini, Elaheh
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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  givenname: Nabeel B.
  surname: Nabulsi
  fullname: Nabulsi, Nabeel B.
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
– sequence: 13
  givenname: Yiyun
  surname: Huang
  fullname: Huang, Yiyun
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
– sequence: 14
  givenname: Amy F.T.
  surname: Arnsten
  fullname: Arnsten, Amy F.T.
  organization: Department of Neuroscience, Yale University School of Medicine, P.O. Box 208001, New Haven, CT 06520, USA
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  givenname: Richard E.
  surname: Carson
  fullname: Carson, Richard E.
  organization: Department of Radiology and Biomedical Imaging, Yale University School of Medicine, P.O. Box 208048, New Haven, CT 06520, USA
– sequence: 16
  givenname: Christopher H.
  surname: van Dyck
  fullname: van Dyck, Christopher H.
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
– sequence: 17
  givenname: Adam P.
  surname: Mecca
  fullname: Mecca, Adam P.
  email: adam.mecca@yale.edu
  organization: Alzheimer’s Disease Research Unit, Yale University School of Medicine, One Church Street, 8th Floor, New Haven, CT 06510, USA
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Keywords DVR
LMII
MRI
PiB
Synaptic density
CDR

SD
[11C]UCB-J
SV2A
MMSE
GDS
APOE
BPND
WAIS
aMCI
1TC
SRTM2
AD
Alzheimer’s disease
GM
CN
RAVLT
ROI
PCA
CS
IY
PCC
CDR-SB
PC
FWHM
PVC
Positron emission tomography
PET
VT
Principal component analysis
Cb
V T
principal component
BP ND
synaptic vesicle glycoprotein 2A
full width half maximum
Wechsler Adult Intelligence Scale
Geriatric depression scale
partial volume correction
amyloid-β
Iterative Yang
apolipoprotein E
Clinical Dementia Rating Scale
Mini-Mental Status Exam
[ 11C]UCB-J
standard deviation
magnetic resonance imaging
cerebellum
simplified reference tissue model – 2 step
1 tissue compartment
Pittsburgh Compound B
posterior cingulate cortex
distribution volume ratio
Rey Auditory Verbal Learning Test
centrum semiovale
CDR-sum of boxes
Logical Memory II
binding potential non-displaceable
gray matter
region of interest
volume of distribution (total)
cognitively normal
amnestic mild cognitive impairment
[C]UCB-J
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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PublicationTitle NeuroImage clinical
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Snippet •This is the first application of PCA to synaptic density PET in Alzheimer’s disease.•Principal components reflect spatial patterns of covariance in synaptic...
Highlights•This is the first application of PCA to synaptic density PET in Alzheimer’s disease. •Principal components reflect spatial patterns of covariance in...
Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer's disease (AD). We used principal...
• This is the first application of PCA to synaptic density PET in Alzheimer’s disease. • Principal components reflect spatial patterns of covariance in...
Background: Synaptic loss is considered an early pathological event and major structural correlate of cognitive impairment in Alzheimer’s disease (AD). We used...
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SubjectTerms [11C]UCB-J
Alzheimer Disease - pathology
Alzheimer’s disease
Amyloid - metabolism
Amyloidogenic Proteins - metabolism
Brain - pathology
Cognitive Dysfunction - pathology
Humans
Positron emission tomography
Principal Component Analysis
Radiology
Regular
SV2A
Synaptic density
Title Principal component analysis of synaptic density measured with [11C]UCB-J PET in early Alzheimer’s disease
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https://dx.doi.org/10.1016/j.nicl.2023.103457
https://www.ncbi.nlm.nih.gov/pubmed/37422964
https://pubmed.ncbi.nlm.nih.gov/PMC10338149
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Volume 39
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