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Global brain activity and its coupling with cerebrospinal fluid flow is related to tau pathology

INTRODUCTION Factors responsible for the deposition of pathological tau in the brain are incompletely understood. This study links macroscale tau deposition in the human brain to cerebrospinal fluid (CSF) flow dynamics using resting‐state functional magnetic resonance imaging (rsfMRI). METHODS Low‐f...

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Published in:Alzheimer's & dementia 2024-12, Vol.20 (12), p.8541-8555
Main Authors: Han, Feng, Lee, JiaQie, Chen, Xi, Ziontz, Jacob, Ward, Tyler, Landau, Susan M., Baker, Suzanne L., Harrison, Theresa M., Jagust, William J.
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container_end_page 8555
container_issue 12
container_start_page 8541
container_title Alzheimer's & dementia
container_volume 20
creator Han, Feng
Lee, JiaQie
Chen, Xi
Ziontz, Jacob
Ward, Tyler
Landau, Susan M.
Baker, Suzanne L.
Harrison, Theresa M.
Jagust, William J.
description INTRODUCTION Factors responsible for the deposition of pathological tau in the brain are incompletely understood. This study links macroscale tau deposition in the human brain to cerebrospinal fluid (CSF) flow dynamics using resting‐state functional magnetic resonance imaging (rsfMRI). METHODS Low‐frequency (
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This study links macroscale tau deposition in the human brain to cerebrospinal fluid (CSF) flow dynamics using resting‐state functional magnetic resonance imaging (rsfMRI). METHODS Low‐frequency (&lt; 0.1 Hz) resting‐state global brain activity is coupled with CSF flow and potentially reflects CSF dynamics‐related clearance. We examined the correlation between rsfMRI measures of CSF inflow and global activity (gBOLD–CSF coupling) as a predictor, interacting with amyloid beta (Aβ), of tau and cortical thickness (dependent variables) across Alzheimer's Disease Neuroimaging Initiative (ADNI) participants from cognitively unimpaired through mild cognitive impairment (MCI) and Alzheimer's disease (AD). RESULTS Tau deposition in Aβ+ participants, accompanied by cortical thinning and cognitive decline, is associated with decreased gBOLD–CSF coupling. Tau mediates the relationship between coupling and thickness. DISCUSSION Findings suggest that resting‐state global brain activity and CSF movements comodulate Alzheimer's tau deposition, presumably related to CSF clearance. Highlights A non‐invasive functional magnetic resonance imaging (fMRI) assessment of a CSF clearance‐related process is carried out. Global brain activity is coupled with CSF inflow in human fMRI during resting state. Global fMRI–CSF coupling is correlated with tau in Alzheimer's disease (AD). This coupling measure is also associated with cortical thickness, mediated by tau.</description><identifier>ISSN: 1552-5260</identifier><identifier>ISSN: 1552-5279</identifier><identifier>EISSN: 1552-5279</identifier><identifier>DOI: 10.1002/alz.14296</identifier><identifier>PMID: 39508716</identifier><language>eng</language><publisher>United States: John Wiley and Sons Inc</publisher><subject>Aged ; Aged, 80 and over ; Alzheimer Disease - cerebrospinal fluid ; Alzheimer Disease - diagnostic imaging ; Alzheimer Disease - physiopathology ; Alzheimer's disease pathology ; Amyloid beta-Peptides - cerebrospinal fluid ; Brain - diagnostic imaging ; Brain - pathology ; brain atrophy ; cerebrospinal fluid (CSF) flow ; Cerebrospinal Fluid - physiology ; Cognitive Dysfunction - cerebrospinal fluid ; Cognitive Dysfunction - physiopathology ; CSF dynamics‐related clearance ; Female ; global resting‐state fMRI signal ; Humans ; Magnetic Resonance Imaging ; Male ; tau deposition ; tau Proteins - cerebrospinal fluid</subject><ispartof>Alzheimer's &amp; dementia, 2024-12, Vol.20 (12), p.8541-8555</ispartof><rights>2024 The Author(s). published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><rights>2024 The Author(s). Alzheimer's &amp; Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3066-839d27e636ccaabca64f24d7059ba81396235762aec2d83cc040d0124e87d70e3</cites><orcidid>0000-0003-3561-4304</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11667553/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11667553/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,11561,27923,27924,37012,46051,46475,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39508716$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Han, Feng</creatorcontrib><creatorcontrib>Lee, JiaQie</creatorcontrib><creatorcontrib>Chen, Xi</creatorcontrib><creatorcontrib>Ziontz, Jacob</creatorcontrib><creatorcontrib>Ward, Tyler</creatorcontrib><creatorcontrib>Landau, Susan M.</creatorcontrib><creatorcontrib>Baker, Suzanne L.</creatorcontrib><creatorcontrib>Harrison, Theresa M.</creatorcontrib><creatorcontrib>Jagust, William J.</creatorcontrib><creatorcontrib>Alzheimer's Disease Neuroimaging Initiative</creatorcontrib><creatorcontrib>for the Alzheimer's Disease Neuroimaging Initiative</creatorcontrib><title>Global brain activity and its coupling with cerebrospinal fluid flow is related to tau pathology</title><title>Alzheimer's &amp; dementia</title><addtitle>Alzheimers Dement</addtitle><description>INTRODUCTION Factors responsible for the deposition of pathological tau in the brain are incompletely understood. This study links macroscale tau deposition in the human brain to cerebrospinal fluid (CSF) flow dynamics using resting‐state functional magnetic resonance imaging (rsfMRI). METHODS Low‐frequency (&lt; 0.1 Hz) resting‐state global brain activity is coupled with CSF flow and potentially reflects CSF dynamics‐related clearance. We examined the correlation between rsfMRI measures of CSF inflow and global activity (gBOLD–CSF coupling) as a predictor, interacting with amyloid beta (Aβ), of tau and cortical thickness (dependent variables) across Alzheimer's Disease Neuroimaging Initiative (ADNI) participants from cognitively unimpaired through mild cognitive impairment (MCI) and Alzheimer's disease (AD). RESULTS Tau deposition in Aβ+ participants, accompanied by cortical thinning and cognitive decline, is associated with decreased gBOLD–CSF coupling. Tau mediates the relationship between coupling and thickness. DISCUSSION Findings suggest that resting‐state global brain activity and CSF movements comodulate Alzheimer's tau deposition, presumably related to CSF clearance. Highlights A non‐invasive functional magnetic resonance imaging (fMRI) assessment of a CSF clearance‐related process is carried out. Global brain activity is coupled with CSF inflow in human fMRI during resting state. Global fMRI–CSF coupling is correlated with tau in Alzheimer's disease (AD). This coupling measure is also associated with cortical thickness, mediated by tau.</description><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Alzheimer Disease - cerebrospinal fluid</subject><subject>Alzheimer Disease - diagnostic imaging</subject><subject>Alzheimer Disease - physiopathology</subject><subject>Alzheimer's disease pathology</subject><subject>Amyloid beta-Peptides - cerebrospinal fluid</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - pathology</subject><subject>brain atrophy</subject><subject>cerebrospinal fluid (CSF) flow</subject><subject>Cerebrospinal Fluid - physiology</subject><subject>Cognitive Dysfunction - cerebrospinal fluid</subject><subject>Cognitive Dysfunction - physiopathology</subject><subject>CSF dynamics‐related clearance</subject><subject>Female</subject><subject>global resting‐state fMRI signal</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>tau deposition</subject><subject>tau Proteins - cerebrospinal fluid</subject><issn>1552-5260</issn><issn>1552-5279</issn><issn>1552-5279</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kc1OGzEURq2qVUPTLvoCyMt2keCfsWdmhVBEA1KkbmDDxr3jcRIjZzzYHqLw9LgkRLBgY1vy8bm-90PoJyVTSgg7A_c0pQWr5Sd0QoVgE8HK-vPxLMkIfYvxnpCCVFR8RSNeC1KVVJ6gf3PnG3C4CWA7DDrZR5t2GLoW2xSx9kPvbLfCW5vWWJtgmuBjb7v8ZOkG2-bVb7GNOBgHybQ4eZxgwD2ktXd-tfuOvizBRfPjsI_R7Z_Lm9nVZPF3fj27WEw0J1JOKl63rDSSS60BGg2yWLKiLYmoG6goryXjopQMjGZtxbXOvbSEssJUZaYMH6Pzvbcfmo1ptelSAKf6YDcQdsqDVe9vOrtWK_-oKJWyFIJnw6-DIfiHwcSkNjZq4xx0xg9RccoqTqtMZ_T3HtV5GjGY5bEOJep_JCpHol4iyezp248dydcMMnC2B7bWmd3HJnWxuNsrnwEjGJeS</recordid><startdate>202412</startdate><enddate>202412</enddate><creator>Han, Feng</creator><creator>Lee, JiaQie</creator><creator>Chen, Xi</creator><creator>Ziontz, Jacob</creator><creator>Ward, Tyler</creator><creator>Landau, Susan M.</creator><creator>Baker, Suzanne L.</creator><creator>Harrison, Theresa M.</creator><creator>Jagust, William J.</creator><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3561-4304</orcidid></search><sort><creationdate>202412</creationdate><title>Global brain activity and its coupling with cerebrospinal fluid flow is related to tau pathology</title><author>Han, Feng ; Lee, JiaQie ; Chen, Xi ; Ziontz, Jacob ; Ward, Tyler ; Landau, Susan M. ; Baker, Suzanne L. ; Harrison, Theresa M. ; Jagust, William J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3066-839d27e636ccaabca64f24d7059ba81396235762aec2d83cc040d0124e87d70e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Alzheimer Disease - cerebrospinal fluid</topic><topic>Alzheimer Disease - diagnostic imaging</topic><topic>Alzheimer Disease - physiopathology</topic><topic>Alzheimer's disease pathology</topic><topic>Amyloid beta-Peptides - cerebrospinal fluid</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - pathology</topic><topic>brain atrophy</topic><topic>cerebrospinal fluid (CSF) flow</topic><topic>Cerebrospinal Fluid - physiology</topic><topic>Cognitive Dysfunction - cerebrospinal fluid</topic><topic>Cognitive Dysfunction - physiopathology</topic><topic>CSF dynamics‐related clearance</topic><topic>Female</topic><topic>global resting‐state fMRI signal</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>tau deposition</topic><topic>tau Proteins - cerebrospinal fluid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Han, Feng</creatorcontrib><creatorcontrib>Lee, JiaQie</creatorcontrib><creatorcontrib>Chen, Xi</creatorcontrib><creatorcontrib>Ziontz, Jacob</creatorcontrib><creatorcontrib>Ward, Tyler</creatorcontrib><creatorcontrib>Landau, Susan M.</creatorcontrib><creatorcontrib>Baker, Suzanne L.</creatorcontrib><creatorcontrib>Harrison, Theresa M.</creatorcontrib><creatorcontrib>Jagust, William J.</creatorcontrib><creatorcontrib>Alzheimer's Disease Neuroimaging Initiative</creatorcontrib><creatorcontrib>for the Alzheimer's Disease Neuroimaging Initiative</creatorcontrib><collection>Wiley Open Access Journals</collection><collection>Wiley Online Library Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Alzheimer's &amp; dementia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Han, Feng</au><au>Lee, JiaQie</au><au>Chen, Xi</au><au>Ziontz, Jacob</au><au>Ward, Tyler</au><au>Landau, Susan M.</au><au>Baker, Suzanne L.</au><au>Harrison, Theresa M.</au><au>Jagust, William J.</au><aucorp>Alzheimer's Disease Neuroimaging Initiative</aucorp><aucorp>for the Alzheimer's Disease Neuroimaging Initiative</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Global brain activity and its coupling with cerebrospinal fluid flow is related to tau pathology</atitle><jtitle>Alzheimer's &amp; dementia</jtitle><addtitle>Alzheimers Dement</addtitle><date>2024-12</date><risdate>2024</risdate><volume>20</volume><issue>12</issue><spage>8541</spage><epage>8555</epage><pages>8541-8555</pages><issn>1552-5260</issn><issn>1552-5279</issn><eissn>1552-5279</eissn><abstract>INTRODUCTION Factors responsible for the deposition of pathological tau in the brain are incompletely understood. This study links macroscale tau deposition in the human brain to cerebrospinal fluid (CSF) flow dynamics using resting‐state functional magnetic resonance imaging (rsfMRI). METHODS Low‐frequency (&lt; 0.1 Hz) resting‐state global brain activity is coupled with CSF flow and potentially reflects CSF dynamics‐related clearance. We examined the correlation between rsfMRI measures of CSF inflow and global activity (gBOLD–CSF coupling) as a predictor, interacting with amyloid beta (Aβ), of tau and cortical thickness (dependent variables) across Alzheimer's Disease Neuroimaging Initiative (ADNI) participants from cognitively unimpaired through mild cognitive impairment (MCI) and Alzheimer's disease (AD). RESULTS Tau deposition in Aβ+ participants, accompanied by cortical thinning and cognitive decline, is associated with decreased gBOLD–CSF coupling. Tau mediates the relationship between coupling and thickness. DISCUSSION Findings suggest that resting‐state global brain activity and CSF movements comodulate Alzheimer's tau deposition, presumably related to CSF clearance. Highlights A non‐invasive functional magnetic resonance imaging (fMRI) assessment of a CSF clearance‐related process is carried out. Global brain activity is coupled with CSF inflow in human fMRI during resting state. Global fMRI–CSF coupling is correlated with tau in Alzheimer's disease (AD). This coupling measure is also associated with cortical thickness, mediated by tau.</abstract><cop>United States</cop><pub>John Wiley and Sons Inc</pub><pmid>39508716</pmid><doi>10.1002/alz.14296</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-3561-4304</orcidid><oa>free_for_read</oa></addata></record>
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source Open Access: PubMed Central; Publicly Available Content Database; Wiley Open Access Journals
subjects Aged
Aged, 80 and over
Alzheimer Disease - cerebrospinal fluid
Alzheimer Disease - diagnostic imaging
Alzheimer Disease - physiopathology
Alzheimer's disease pathology
Amyloid beta-Peptides - cerebrospinal fluid
Brain - diagnostic imaging
Brain - pathology
brain atrophy
cerebrospinal fluid (CSF) flow
Cerebrospinal Fluid - physiology
Cognitive Dysfunction - cerebrospinal fluid
Cognitive Dysfunction - physiopathology
CSF dynamics‐related clearance
Female
global resting‐state fMRI signal
Humans
Magnetic Resonance Imaging
Male
tau deposition
tau Proteins - cerebrospinal fluid
title Global brain activity and its coupling with cerebrospinal fluid flow is related to tau pathology
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