Functional brain architecture is associated with the rate of tau accumulation in Alzheimer’s disease
Nicolai Franzmeier(LMU Klinikum), Julia Neitzel(Ludwig-Maximilians-Universität München), Anna Rubinski(Ludwig-Maximilians-Universität München), Ruben Smith(Lund University), Olof Strandberg(Lund University), Rik Ossenkoppele(Lund University), Oskar Hansson(Lund University), Michael Ewers(Ludwig-Maximilians-Universität München), Alzheimer’s Disease Neuroimaging Initiative (ADNI)(University of California, San Francisco), Michael Weiner(UC San Diego Health System), Paul Aisen(Mayo Clinic in Florida), Ronald C. Petersen(Mayo Clinic in Florida), Clifford R. Jack(Berkeley College), William J. Jagust(California University of Pennsylvania), John Q. Trojanowki(LAC+USC Medical Center), Arthur W. Toga(University of California, Davis), Laurel Beckett(Brigham and Women's Hospital), Robert C. Green(Indiana University Bloomington), Andrew J. Saykin(Washington University in St. Louis), John C. Morris(University of Pennsylvania), Leslie M. Shaw(Janssen (United States)), Enchi Liu(University of Washington), Tom Montine(UC San Diego Health System), Ronald G. Thomas(UC San Diego Health System), Michael Donohue(UC San Diego Health System), Sarah Walter(UC San Diego Health System), Devon Gessert(UC San Diego Health System), Tamie Sather(UC San Diego Health System), Gus Jiminez(University of California, Davis), Danielle Harvey(UC San Diego Health System), Michael Donohue(Mayo Clinic in Florida), Matt A. Bernstein(University of London), Nick C. Fox(LAC+USC Medical Center), Paul M. Thompson, Norbert Schuff(University of California, Davis), Charles DeCarli(Mayo Clinic in Florida), Bret Borowski(Mayo Clinic in Florida), Jeff Gunter(Mayo Clinic in Florida), Matthew L. Senjem(Mayo Clinic in Florida), Prashanthi Vemuri(Mayo Clinic in Florida), David T. Jones(Mayo Clinic in Florida), Kejal Kantarci(Mayo Clinic in Florida), Chad Ward(University of Michigan), Robert A. Koeppe(University of Utah), Norm Foster(Banner Alzheimer’s Institute), Eric M. Reiman(Banner Alzheimer’s Institute), Kewei Chen(University of Pittsburgh), Chet Mathis(Berkeley College), Susan Landau(Washington University in St. Louis), Nigel J. Cairns(Washington University in St. Louis), Erin Householder(Washington University in St. Louis), Lisa Taylor Reinwald(University of Pennsylvania), Virginia Lee(University of Pennsylvania), Magdalena Korecka(University of Pennsylvania), Michal Figurski(LAC+USC Medical Center), Karen Crawford(LAC+USC Medical Center), Scott Neu(Indiana University Bloomington), Tatiana Foroud(University of California, Irvine), Steven Potkin(Indiana University Bloomington), Li Shen(Indiana University Bloomington), Kelley Faber(Indiana University Bloomington), Sung Eun Kim(Indiana University Bloomington), Kwangsik Nho(Alzheimer's Association), Zaven Kachaturian(General Electric (United States)), Richard Frank(Brown University), Peter J. Snyder(National Institutes of Health), Susan Molchan(Oregon Health & Science University), Jeffrey Kaye(Oregon Health & Science University), Joseph F. Quinn(Oregon Health & Science University), Betty Lind(Oregon Health & Science University), Raina Carter(Oregon Health & Science University), Sara Dolen(University of Southern California), Lon S. Schneider(University of Southern California), Sonia Pawluczyk(University of Southern California), Mauricio Beccera(University of Southern California), Liberty Teodoro(University of Southern California), Bryan M. Spann(University of California San Diego), James B. Brewer(University of California San Diego), Helen Vanderswag(Banner Alzheimer’s Institute), Adam Fleisher(University of Michigan), Judith L. Heidebrink(University of Michigan), Joanne Lord(Mayo Clinic in Florida), Ronald C. Petersen(Mayo Clinic in Florida), Sara S. Mason(Mayo Clinic in Florida), Colleen S. Albers(Mayo Clinic in Florida), David S. Knopman(Mayo Clinic in Florida), Kris Johnson(Baylor College of Medicine), Rachelle S. Doody(Baylor College of Medicine), Javier Villanueva Meyer(Baylor College of Medicine), Munir Chowdhury(Baylor College of Medicine), Susan Rountree(Baylor College of Medicine), Mimi Dang(Columbia University Irving Medical Center), Yaakov Stern(Columbia University Irving Medical Center), Lawrence S. Honig(Columbia University Irving Medical Center), Karen L. Bell(Washington University in St. Louis), Beau M. Ances(Washington University in St. Louis), John C. Morris(Washington University in St. Louis), Maria Carroll(Washington University in St. Louis), Sue Leon(Washington University in St. Louis), Erin Householder(Washington University in St. Louis), Mark A. Mintun(Washington University in St. Louis), Stacy Schneider(University of Alabama at Birmingham), Angela OliverNG(University of Alabama at Birmingham), Randall Griffith(University of Alabama at Birmingham), David W. Clark(University of Alabama at Birmingham), David Geldmacher(University of Alabama at Birmingham), John Brockington(University of Alabama at Birmingham), Erik D. Roberson(Icahn School of Medicine at Mount Sinai), Hillel Grossman(Icahn School of Medicine at Mount Sinai), Effie Mitsis(Rush University Medical Center), Leyla deToledo‐Morrell(Rush University Medical Center), Raj C. Shah, Ranjan Duara, Daniel Varón, Maria T. Greig, Peggy Roberts(Johns Hopkins University), Marilyn Albert(Johns Hopkins University), Chiadi U. Onyike(Johns Hopkins University), Daniel D’Agostino(Johns Hopkins University), Stephanie Kielb(New York University), James E. Galvin(New York University), Dana M. Pogorelec(New York University), Brittany Cerbone(New York University), Christina A. Michel(New York University), Henry Rusinek(New York University), Mony J. de Leon(New York University), Lidia Glodzik(New York University), Susan De Santi(Duke Medical Center), P. Murali Doraiswamy(Duke Medical Center), Jeffrey R. Petrella(Duke Medical Center), Terence Z. Wong(University of Pennsylvania), Steven E. Arnold(University of Pennsylvania), Jason Karlawish(University of Pennsylvania), David A. Wolk(University of Kentucky), Charles D. Smith(University of Kentucky), Gregory A. Jicha(University of Kentucky), Peter Hardy(University of Kentucky), Partha Sinha(University of Kentucky), Elizabeth Oates(University of Kentucky), Gary Conrad(University of Pittsburgh), Oscar L. López(University of Pittsburgh), MaryAnn Oakley(University of Pittsburgh), Donna M. Simpson(University of Rochester Medical Center), Anton P. Porsteinsson(University of Rochester Medical Center), Bonnie S. Goldstein(University of Rochester Medical Center), Kim Martin(University of Rochester Medical Center), Kelly M. Makino(University of Rochester Medical Center), M. Saleem Ismail(University of Rochester Medical Center), Connie Brand(University of California, Irvine), Ruth A. Mulnard(University of California, Irvine), Gaby Thai(University of California, Irvine), Catherine Mc Adams Ortiz(The University of Texas Southwestern Medical Center), Kyle Womack(The University of Texas Southwestern Medical Center), Dana Mathews(The University of Texas Southwestern Medical Center), Mary Quiceno(The University of Texas Southwestern Medical Center), Ramon Diaz Arrastia(The University of Texas Southwestern Medical Center), Richard King(The University of Texas Southwestern Medical Center), Myron Weiner(The University of Texas Southwestern Medical Center), Kristen Martin Cook(The University of Texas Southwestern Medical Center), Michael D. Devous(Emory University), Allan I. Levey(Emory University), James J. Lah(Emory University), Janet S. Cellar(University of Kansas Medical Center), Jeffrey M. Burns(University of Kansas Medical Center), Heather S. Anderson(University of Kansas Medical Center), Russell H. Swerdlow(University of California, Los Angeles), Liana G. Apostolova(University of California, Los Angeles), Kathleen Tingus(University of California, Los Angeles), Ellen Woo(University of California, Los Angeles), Daniel Silverman(University of California, Los Angeles), Po H. Lu(University of California, Los Angeles), George Bartzokis(WinnMed), Neill R. Graff Radford(WinnMed), Francine ParfittH(WinnMed), Tracy Kendall(WinnMed), Heather Johnson(Indiana University Bloomington), Martin R. Farlow(Indiana University Bloomington), Ann Marie Hake(Indiana University Bloomington), Brandy R. Matthews(Indiana University Bloomington), Scott Herring(Indiana University Bloomington), Cynthia Hunt(Yale University), Christopher H. van Dyck(Yale University), Richard E. Carson(Yale University), Martha G. MacAvoy, Howard Chertkow, Howard Bergman, Chris Hosein(Sunnybrook Health Science Centre), Sandra E. Black(Sunnybrook Health Science Centre), Bojana Stefanovic(Sunnybrook Health Science Centre), Curtis Caldwell, Ging‐Yuek Robin Hsiung, Howard Feldman, Benita Mudge, Michele Assaly Past(St Joseph's Health Centre), Andrew Kertesz(St Joseph's Health Centre), John Rogers(St Joseph's Health Centre), Dick Trost(Cleveland Clinic), Charles Bernick(Cleveland Clinic), Donna Munic(Northwestern University), Diana Kerwin(Northwestern University), Marek Marsel Mesulam(Northwestern University), Kristine Lipowski(Northwestern University), Chuang Wu(Northwestern University), Nancy Johnson(Palm Beach Neurology), Carl Sadowsky(Palm Beach Neurology), Walter Martínez(Palm Beach Neurology), Teresa Villena(Georgetown University), Raymond Scott Turner(Georgetown University), Kathleen Johnson(Georgetown University), Brigid Reynolds(Brigham and Women's Hospital), Reisa A. Sperling(Brigham and Women's Hospital), Keith A. Johnson(Brigham and Women's Hospital), Gad A. Marshall(Brigham and Women's Hospital), Meghan Frey(Stanford University), Jerome A. Yesavage(Stanford University), Joy L. Taylor(Stanford University), Barton Lane(Stanford University), Allyson Rosen(Stanford University), Jared Tinklenberg(Banner Sun Health Research Institute), Marwan N. Sabbagh(Banner Sun Health Research Institute), Christine M. Belden(Banner Sun Health Research Institute), Sandra A. Jacobson(Banner Sun Health Research Institute), Sherye A. Sirrel, Neil W. Kowall, Ronald Killiany, Andrew E. Budson, Alexander Norbash, Patricia Lynn Johnson(Howard University), Thomas O. Obisesan(Howard University), Saba Wolday(Howard University), Joanne Allard(Case Western Reserve University), Alan J. Lerner(Case Western Reserve University), Paula Ogrocki(Case Western Reserve University), Leon Hudson(University of California, Davis), Evan Fletcher(University of California, Davis), Owen Carmichael(University of California, Davis), John Olichney(University of California, Davis), Charles DeCarli, Smita Kittur(Beaumont Hospital, Dearborn), Michael Borrie(Beaumont Hospital, Dearborn), T Y Lee(Beaumont Hospital, Dearborn), Robert Bartha(University of Wisconsin–Madison), Sterling C. Johnson(University of Wisconsin–Madison), Sanjay Asthana(University of Wisconsin–Madison), Cynthia M. Carlsson(University of California, Irvine), Steven G. Potkin(University of California, Irvine), Adrian Preda(University of California, Irvine), Dana Nguyen(Banner Alzheimer’s Institute), Pierre N. Tariot(University of California San Diego), Adam Fleisher(Banner Alzheimer’s Institute), Stephanie Reeder(Dent Neurologic Institute), Vernice Bates(Dent Neurologic Institute), Horacio Capote(Dent Neurologic Institute), Michelle Rainka(The Ohio State University), Douglas W. Scharre(The Ohio State University), Maria Kataki(The Ohio State University), Anahita Adeli(Albany Medical Center Hospital), Earl A. Zimmerman(Albany Medical Center Hospital), Dzintra Celmins(Albany Medical Center Hospital), Alice D. Brown(Hartford Hospital), Godfrey D. Pearlson(Hartford Hospital), Karen Blank(Hartford Hospital), Karen Anderson(Dartmouth–Hitchcock Medical Center), Robert B. Santulli(Dartmouth–Hitchcock Medical Center), Tamar J. Kitzmiller(Dartmouth–Hitchcock Medical Center), Eben S. Schwartz(Wake Forest University), Kaycee M. SinkS(Wake Forest University), Jeff D. Williamson(Wake Forest University), Pradeep Garg(Wake Forest University), Franklin Watkins(Rhode Island Hospital), Brian R. Ott(Rhode Island Hospital), Henry Querfurth(Rhode Island Hospital), Geoffrey Tremont(Providence College), Stephen Salloway(Providence College), Paul Malloy(Providence College), Stephen Correia(University of California, San Francisco), Howard J. Rosen(University of California, San Francisco), Bruce L. Miller(Medical University of South Carolina), Jacobo Mintzer(Medical University of South Carolina), Kenneth Spicer(Medical University of South Carolina), David Bachman(St Joseph's Health Care), Elizabeth Finger(St Joseph's Health Care), Stephen Pasternak(St Joseph's Health Care), Irina Rachinsky(St Joseph's Health Care), John Rogers(St Joseph's Health Care), Andrew Kertesz(St Joseph's Health Care), Dick Drost(Nathan Kline Institute for Psychiatric Research), Nunzio Pomara(Nathan Kline Institute for Psychiatric Research), Raymundo Hernando(Nathan Kline Institute for Psychiatric Research), Antero Sarrael(University of Iowa), Susan K. Schultz(University of Iowa), Laura L. Boles Ponto(University of Iowa), Hyungsub Shim(University of Iowa), Karen E. Smith(Cornell University), Norman Relkin(Cornell University), Gloria Chaing(Cornell University), Lisa Raudin(University of South Florida), Amanda Smith(University of South Florida), Kristin Fargher(University of South Florida), Balebail Ashok Raj
Cited by 341Open Access
Abstract
In Alzheimer's diseases (AD), tau pathology is strongly associated with cognitive decline. Preclinical evidence suggests that tau spreads across connected neurons in an activity-dependent manner. Supporting this, cross-sectional AD studies show that tau deposition patterns resemble functional brain networks. However, whether higher functional connectivity is associated with higher rates of tau accumulation is unclear. Here, we combine resting-state fMRI with longitudinal tau-PET in two independent samples including 53 (ADNI) and 41 (BioFINDER) amyloid-biomarker defined AD subjects and 28 (ADNI) vs. 16 (BioFINDER) amyloid-negative healthy controls. In both samples, AD subjects show faster tau accumulation than controls. Second, in AD, higher fMRI-assessed connectivity between 400 regions of interest (ROIs) is associated with correlated tau-PET accumulation in corresponding ROIs. Third, we show that a model including baseline connectivity and tau-PET is associated with future tau-PET accumulation. Together, connectivity is associated with tau spread in AD, supporting the view of transneuronal tau propagation.
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