Journal article
Anatomically interpretable deep learning of brain age captures domain-specific cognitive impairment
Proceedings of the National Academy of Sciences - PNAS, Vol.120(2), e2214634120
01/10/2023
DOI: 10.1073/pnas.2214634120
PMCID: PMC9926270
PMID: 36595679
Abstract
The gap between chronological age (CA) and biological brain age, as estimated from magnetic resonance images (MRIs), reflects how individual patterns of neuroanatomic aging deviate from their typical trajectories. MRI-derived brain age (BA) estimates are often obtained using deep learning models that may perform relatively poorly on new data or that lack neuroanatomic interpretability. This study introduces a convolutional neural network (CNN) to estimate BA after training on the MRIs of 4,681 cognitively normal (CN) participants and testing on 1,170 CN participants from an independent sample. BA estimation errors are notably lower than those of previous studies. At both individual and cohort levels, the CNN provides detailed anatomic maps of brain aging patterns that reveal sex dimorphisms and neurocognitive trajectories in adults with mild cognitive impairment (MCI, N = 351) and Alzheimer’s disease (AD, N = 359). In individuals with MCI (54% of whom were diagnosed with dementia within 10.9 y from MRI acquisition), BA is significantly better than CA in capturing dementia symptom severity, functional disability, and executive function. Profiles of sex dimorphism and lateralization in brain aging also map onto patterns of neuroanatomic change that reflect cognitive decline. Significant associations between BA and neurocognitive measures suggest that the proposed framework can map, systematically, the relationship between aging-related neuroanatomy changes in CN individuals and in participants with MCI or AD. Early identification of such neuroanatomy changes can help to screen individuals according to their AD risk.
Details
- Title: Subtitle
- Anatomically interpretable deep learning of brain age captures domain-specific cognitive impairment
- Creators
- Chenzhong Yin - Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089Reisa A. SperlingPhoebe Imms - Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089Keith A. JohnsonMingxi Cheng - Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089Gad A. MarshallAnar Amgalan - Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089Jerome YesavageNahian F. Chowdhury - Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089Joy L. TaylorRoy J. Massett - Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089Steven ChaoNikhil N. Chaudhari - Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089, Corwin D. Denney Research Center, Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089Jaila ColemanJessica D. WhiteXinghe Chen - Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089Paul M. Thompson - University of Southern CaliforniaBarton LanePaul Bogdan - Ming Hsieh Department of Electrical and Computer Engineering, Viterbi School of Engineering, University of Southern California, Los Angeles, CA 90089Allyson RosenAndrei Irimia - University of Southern CaliforniaJared TinklenbergMichael W. WeinerChristine M. BeldenPaul AisenKelly A. ClarkRonald PetersenEdward ZamriniClifford R. JackMarwan SabbaghWilliam JagustRonald KillianyJohn Q. TrojanowkiRobert SternJesse MezArthur W. TogaLaurel BeckettNeil KowallRobert C. GreenAndrew E. BudsonAndrew J. SaykinJohn C. MorrisRichard J. PerrinLeslie M. ShawZaven KhachaturianMaria CarrilloWilliam PotterLisa BarnesMarie BernardHector GonzálezCarole HoJohn K. HsiaoJonathan JacksonEliezer MasliahDonna MastermanOzioma OkonkwoRichard PerrinLaurie RyanNina SilverbergAdam FleisherEli LillyDiana Truran SacreyJuliet FocklerCat ContiDallas VeitchJohn NeuhausChengshi JinRachel NoshenyMiriam AshfordDerek FlennikenAdrienne KormosTom MontineMichael RafiiRema RamanGustavo JimenezMichael DonohueDevon GessertJennifer SalazarCaileigh ZimmermanYuliana CabreraSarah WalterGarrett MillerGodfrey CokerTaylor ClantonLindsey HergesheimerStephanie SmithOlusegun AdegokePayam MahboubiShelley MooreJeremy PizzolaElizabeth ShafferBrittany SloanDanielle HarveyArvin Forghanian-AraniBret BorowskiChad WardChristopher Schwarz - Mayo ClinicDavid JonesJeff GunterKejal KantarciMatthew SenjemPrashanthi VemuriRobert ReidNick C. FoxIan MaloneSophia I. ThomopoulosTalia M. NirNeda JahanshadCharles DeCarliAlexander KnaackEvan FletcherDuygu Tosun-TurgutStephanie Rossi ChenMark ChoeKaren CrawfordPaul A. YushkevichSandhitsu DasRobert A. KoeppeEric M. ReimanKewei ChenChet MathisSusan LandauNigel J. CairnsErin HouseholderErin FranklinHaley BernhardtLisa Taylor-ReinwaldMagdalena KoreckaMichal FigurskiScott NeuKwangsik NhoShannon L. RisacherLiana G. ApostolovaLi ShenTatiana M. ForoudKelly NudelmanKelley FaberKristi WilmesLeon ThalLisa C. SilbertBetty LindRachel CrisseyJeffrey A. KayeRaina CarterSara DolenJoseph QuinnLon S. SchneiderSonia PawluczykMauricio BecerraLiberty TeodoroKaren DagermanBryan M. SpannJames BrewerHelen VanderswagJaimie ZiolkowskiJudith L. HeidebrinkLisa Zbizek-NulphJoanne L. LordSara S. MasonColleen S. AlbersDavid KnopmanKris JohnsonJavier Villanueva-MeyerValory PavlikNathaniel PaciniAshley LambJoseph S. KassRachelle S. DoodyVictoria ShibleyMunir ChowdhurySusan RountreeMimi DangYaakov SternLawrence S. HonigAkiva MintzBeau AncesDavid WinkfieldMaria CarrollGeorgia Stobbs-CucchiAngela OliverMary L. CreechMark A. MintunStacy SchneiderDavid GeldmacherMarissa Natelson LoveRandall GriffithDavid ClarkJohn BrockingtonDaniel MarsonHillel GrossmanMartin A. GoldsteinJonathan GreenbergEffie MitsisRaj C. ShahMelissa LamarPatricia SamuelsRanjan DuaraMaria T. Greig-CustoRosemarie RodriguezMarilyn AlbertChiadi OnyikeLeonie FarringtonScott RudowRottislav BrichkoStephanie KielbAmanda SmithBalebail Ashok RajKristin FargherMartin SadowskiThomas WisniewskiMelanie ShulmanArline FaustinJulia RaoKaren M. CastroAnaztasia UlysseShannon ChenMohammed O. SheikhJamika Singleton-GarvinP. Murali DoraiswamyJeffrey R. PetrellaOlga JamesTerence Z. WongSalvador Borges-NetoJason H. KarlawishDavid A. WolkSanjeev VaishnaviChristopher M. ClarkSteven E. ArnoldCharles D. SmithGregory A. JichaRiham El KhouliFlavius D. RaslauOscar L. LopezMaryAnn OakleyDonna M. SimpsonAnton P. PorsteinssonKim MartinNancy KowalskiMelanie KeltzBonnie S. GoldsteinKelly M. MakinoM. Saleem IsmailConnie BrandGaby ThaiAimee PierceBeatriz YanezElizabeth SosaMegan WitbrachtBrendan KelleyTrung NguyenKyle WomackDana MathewsMary QuicenoAllan I. LeveyJames J. LahIhab HajjarJanet S. CellarJeffrey M. BurnsRussell H. SwerdlowWilliam M. BrooksDaniel H.S. SilvermanSarah KremenKathleen TingusPo H. LuGeorge BartzokisEllen WooEdmond TengNeill R. Graff-RadfordFrancine ParfittKim Poki-WalkerMartin R. FarlowAnn Marie HakeBrandy R. MatthewsJared R. BroschScott HerringChristopher H. van DyckAdam P. MeccaMartha G. MacAvoyRichard E. CarsonPradeep VarmaHoward ChertkowSusan VaitekunisChris HoseinSandra BlackBojana StefanovicChris (Chinthaka) HeynGing-Yuek Robin HsiungEllen KimBenita MudgeVesna SossiHoward FeldmanMichele AssalyElizabeth FingerStephen PasternakIrina RachinskyAndrew KerteszDick DrostJohn RogersIan GrantBrittanie MuseEmily RogalskiJordan RobsonM.-Marsel MesulamDiana KerwinChuang-Kuo WuNancy JohnsonKristine LipowskiSandra WeintraubBorna BonakdarpourNunzio PomaraRaymundo HernandoAntero SarraelHoward J. RosenBruce L. MillerDavid PerryRaymond Scott TurnerKathleen Johnson - Georgetown University Medical CenterBrigid ReynoldsKelly MCCannJessica PoeThomas O. ObisesanOyonumo E. NtekimSaba WoldayJaved I. KhanEvaristus NwuliaSheeba NadarajahAlan LernerPaula OgrockiCurtis TatsuokaParianne FaticaPauline MaillardJohn OlichneyOwen CarmichaelVernice BatesHoracio CapoteMichelle RainkaMichael BorrieT-Y LeeDr Rob BarthaSterling JohnsonSanjay AsthanaCynthia M. CarlssonAllison PerrinAnna BurkeDouglas W. ScharreMaria KatakiRawan TarawnehDavid HartEarl A. ZimmermanDzintra CelminsDelwyn D. MillerLaura L. Boles PontoKaren Ekstam SmithHristina KolevaHyungsub ShimKi Won NamSusan K. SchultzJeff D. WilliamsonSuzanne CraftJo ClevelandMia YangKaycee M. SinkBrian R. OttGeoffrey TremontLori A. DaielloJonathan D. DrakeAaron RitterCharles BernickDonna MunicAbigail O’ConnelllJacobo MintzerArthur WiliamsJoseph MasdeuJiong ShiAngelica GarciaPaul NewhouseSteven PotkinStephen SallowayPaul MalloyStephen CorreiaSmita KitturGodfrey D. PearlsonKaren BlankKaren AndersonLaura A. FlashmanMarc SeltzerMary L. HynesRobert B. SantulliNorman RelkinGloria ChiangAthena LeeMichael LinLisa RavdinRon PetersenThomas NeylanJordan GrafmanSarah DanowskiCatherine Nguyen-BarreraJacqueline HayesShannon FinleyMatthew BernsteinMatt SenjemNorm FosterSungeun KimAjay SoodKimberly S. BlanchardDebra FleischmanKonstantinos ArfanakisDr. Ranjan DuaraDr. Daniel VaronMaria T GreigKimberly S. MartinChristopher ReistCarl SadowskyWalter MartinezTeresa VillenaHoward RosenElaine R. PeskindEric C. PetrieGail LiScott MackinGustavo Jimenez-MaggioraErin DrakeMike DonohueCraig NelsonDavid BickfordMeryl ButtersMichelle ZmudaDenise ReyesKelley M. FaberYiu Ho AuKelly SchererDaniel CatalinottoSamuel StarkElise OngDariella FernandezAlzheimer’s Disease Neuroimaging Initiative
- Resource Type
- Journal article
- Publication Details
- Proceedings of the National Academy of Sciences - PNAS, Vol.120(2), e2214634120
- DOI
- 10.1073/pnas.2214634120
- PMID
- 36595679
- PMCID
- PMC9926270
- NLM abbreviation
- Proc Natl Acad Sci U S A
- ISSN
- 0027-8424
- eISSN
- 1091-6490
- Grant note
- DOI: 10.13039/100000002, name: HHS | National Institutes of Health, award: R01 NS 100973; DOI: 10.13039/100000005, name: U.S. Department of Defense, award: W81-XWH-1810413; name: James J. & Sue Femino Foundation, award: NA; name: Hanson-Thorell Research Scholarship, award: NA; name: URAP at the University of Southern California, award: NA; name: CURVE at the University of Southern California, award: NA; DOI: 10.13039/100000001, name: National Science Foundation, award: CPS/CNS-1453860; DOI: 10.13039/100000001, name: National Science Foundation, award: CCF-1837131; DOI: 10.13039/100000001, name: National Science Foundation, award: MCB-1936775; DOI: 10.13039/100000001, name: National Science Foundation, award: CNS-1932620; DOI: 10.13039/100000001, name: National Science Foundation, award: CMMI-1936624; DOI: 10.13039/501100004399, name: Okawa Foundation for Information and Telecommunications, award: NA; DOI: 10.13039/100000185, name: DOD | Defense Advanced Research Projects Agency, award: N66001-17-1-4044; DOI: 10.13039/100018305, name: USC | Stevens Center for Innovation, University of Southern California, award: NA; DOI: 10.13039/100002418, name: Intel Corporation, award: NA; DOI: 10.13039/100005014, name: Northrop Grumman, award: NA
- Language
- English
- Date published
- 01/10/2023
- Academic Unit
- Neurology; Radiology; Psychiatry
- Record Identifier
- 9984354392602771
Metrics
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