| Title: | Anatomically interpretable deep learning of brain age captures domain-specific cognitive impairment |
| Journal: | Proceedings of the National Academy of Sciences of the United States of America |
| Published: | 3 Jan 2023 |
| Pubmed: | https://pubmed.ncbi.nlm.nih.gov/36595679/ |
| DOI: | https://doi.org/10.1073/pnas.2214634120 |
Publication 10907
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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.</p>
642 Authors
- Chenzhong Yin
- Phoebe Imms
- Mingxi Cheng
- Anar Amgalan
- Nahian F. Chowdhury
- Roy J. Massett
- Nikhil N. Chaudhari
- Xinghe Chen
- Paul M. Thompson
- Paul Bogdan
- Andrei Irimia
- the Alzheimer's Disease Neuroimaging Initiative
- Michael W. Weiner
- Paul Aisen
- Ronald Petersen
- Michael W. Weiner
- Paul Aisen
- Ronald Petersen
- Clifford R. Jack
- William Jagust
- John Q. Trojanowki
- Arthur W. Toga
- Laurel Beckett
- Robert C. Green
- Andrew J. Saykin
- John C. Morris
- Richard J. Perrin
- Leslie M. Shaw
- Zaven Khachaturian
- Maria Carrillo
- William Potter
- Lisa Barnes
- Marie Bernard
- Hector González
- Carole Ho
- John K. Hsiao
- Jonathan Jackson
- Eliezer Masliah
- Donna Masterman
- Ozioma Okonkwo
- Richard Perrin
- Laurie Ryan
- Nina Silverberg
- Adam Fleisher
- Eli Lilly
- Michael W. Weiner
- Diana Truran Sacrey
- Juliet Fockler
- Cat Conti
- Dallas Veitch
- John Neuhaus
- Chengshi Jin
- Rachel Nosheny
- Miriam Ashford
- Derek Flenniken
- Adrienne Kormos
- Robert C. Green
- Tom Montine
- Cat Conti
- Ronald Petersen
- Paul Aisen
- Michael Rafii
- Rema Raman
- Gustavo Jimenez
- Michael Donohue
- Devon Gessert
- Jennifer Salazar
- Caileigh Zimmerman
- Yuliana Cabrera
- Sarah Walter
- Garrett Miller
- Godfrey Coker
- Taylor Clanton
- Lindsey Hergesheimer
- Stephanie Smith
- Olusegun Adegoke
- Payam Mahboubi
- Shelley Moore
- Jeremy Pizzola
- Elizabeth Shaffer
- Brittany Sloan
- Laurel Beckett
- Danielle Harvey
- Michael Donohue
- Clifford R. Jack
- Arvin Forghanian-Arani
- Bret Borowski
- Chad Ward
- Christopher Schwarz
- David Jones
- Jeff Gunter
- Kejal Kantarci
- Matthew Senjem
- Prashanthi Vemuri
- Robert Reid
- Nick C. Fox
- Ian Malone
- Paul Thompson
- Sophia I. Thomopoulos
- Talia M. Nir
- Neda Jahanshad
- Charles DeCarli
- Alexander Knaack
- Evan Fletcher
- Danielle Harvey
- Duygu Tosun-Turgut
- Stephanie Rossi Chen
- Mark Choe
- Karen Crawford
- Paul A. Yushkevich
- Sandhitsu Das
- William Jagust
- Robert A. Koeppe
- Eric M. Reiman
- Kewei Chen
- Chet Mathis
- Susan Landau
- John C. Morris
- Richard Perrin
- Nigel J. Cairns
- Erin Householder
- Erin Franklin
- Haley Bernhardt
- Lisa Taylor-Reinwald
- Leslie M. Shaw
- John Q. Trojanowki
- Magdalena Korecka
- Michal Figurski
- Arthur W. Toga
- Karen Crawford
- Scott Neu
- Andrew J. Saykin
- Kwangsik Nho
- Shannon L. Risacher
- Liana G. Apostolova
- Li Shen
- Tatiana M. Foroud
- Kelly Nudelman
- Kelley Faber
- Kristi Wilmes
- Michael W. Weiner
- Leon Thal
- Zaven Khachaturian
- John K. Hsiao
- Lisa C. Silbert
- Betty Lind
- Rachel Crissey
- Jeffrey A. Kaye
- Raina Carter
- Sara Dolen
- Joseph Quinn
- Lon S. Schneider
- Sonia Pawluczyk
- Mauricio Becerra
- Liberty Teodoro
- Karen Dagerman
- Bryan M. Spann
- James Brewer
- Helen Vanderswag
- Adam Fleisher
- Jaimie Ziolkowski
- Judith L. Heidebrink
- Lisa Zbizek-Nulph
- Joanne L. Lord
- Lisa Zbizek-Nulph
- Ronald Petersen
- Sara S. Mason
- Colleen S. Albers
- David Knopman
- Kris Johnson
- Javier Villanueva-Meyer
- Valory Pavlik
- Nathaniel Pacini
- Ashley Lamb
- Joseph S. Kass
- Rachelle S. Doody
- Victoria Shibley
- Munir Chowdhury
- Susan Rountree
- Mimi Dang
- Yaakov Stern
- Lawrence S. Honig
- Akiva Mintz
- Beau Ances
- John C. Morris
- David Winkfield
- Maria Carroll
- Georgia Stobbs-Cucchi
- Angela Oliver
- Mary L. Creech
- Mark A. Mintun
- Stacy Schneider
- David Geldmacher
- Marissa Natelson Love
- Randall Griffith
- David Clark
- John Brockington
- Daniel Marson
- Hillel Grossman
- Martin A. Goldstein
- Jonathan Greenberg
- Effie Mitsis
- Raj C. Shah
- Melissa Lamar
- Patricia Samuels
- Ranjan Duara
- Maria T. Greig-Custo
- Rosemarie Rodriguez
- Marilyn Albert
- Chiadi Onyike
- Leonie Farrington
- Scott Rudow
- Rottislav Brichko
- Stephanie Kielb
- Amanda Smith
- Balebail Ashok Raj
- Kristin Fargher
- Martin Sadowski
- Thomas Wisniewski
- Melanie Shulman
- Arline Faustin
- Julia Rao
- Karen M. Castro
- Anaztasia Ulysse
- Shannon Chen
- Mohammed O. Sheikh
- Jamika Singleton-Garvin
- P. Murali Doraiswamy
- Jeffrey R. Petrella
- Olga James
- Terence Z. Wong
- Salvador Borges-Neto
- Jason H. Karlawish
- David A. Wolk
- Sanjeev Vaishnavi
- Christopher M. Clark
- Steven E. Arnold
- Charles D. Smith
- Gregory A. Jicha
- Riham El Khouli
- Flavius D. Raslau
- Oscar L. Lopez
- MaryAnn Oakley
- Donna M. Simpson
- Anton P. Porsteinsson
- Kim Martin
- Nancy Kowalski
- Melanie Keltz
- Bonnie S. Goldstein
- Kelly M. Makino
- M. Saleem Ismail
- Connie Brand
- Gaby Thai
- Aimee Pierce
- Beatriz Yanez
- Elizabeth Sosa
- Megan Witbracht
- Brendan Kelley
- Trung Nguyen
- Kyle Womack
- Dana Mathews
- Mary Quiceno
- Allan I. Levey
- James J. Lah
- Ihab Hajjar
- Janet S. Cellar
- Jeffrey M. Burns
- Russell H. Swerdlow
- William M. Brooks
- Daniel H.S. Silverman
- Sarah Kremen
- Liana Apostolova
- Kathleen Tingus
- Po H. Lu
- George Bartzokis
- Ellen Woo
- Edmond Teng
- Neill R. Graff-Radford
- Francine Parfitt
- Kim Poki-Walker
- Martin R. Farlow
- Ann Marie Hake
- Brandy R. Matthews
- Jared R. Brosch
- Scott Herring
- Christopher H. van Dyck
- Adam P. Mecca
- Martha G. MacAvoy
- Richard E. Carson
- Pradeep Varma
- Howard Chertkow
- Susan Vaitekunis
- Chris Hosein
- Sandra Black
- Bojana Stefanovic
- Chris Heyn
- Ging-Yuek Robin Hsiung
- Ellen Kim
- Benita Mudge
- Vesna Sossi
- Howard Feldman
- Michele Assaly
- Elizabeth Finger
- Stephen Pasternak
- Irina Rachinsky
- Andrew Kertesz
- Dick Drost
- John Rogers
- Ian Grant
- Brittanie Muse
- Emily Rogalski
- Jordan Robson
- M.-Marsel Mesulam
- Diana Kerwin
- Chuang-Kuo Wu
- Nancy Johnson
- Kristine Lipowski
- Sandra Weintraub
- Borna Bonakdarpour
- Nunzio Pomara
- Raymundo Hernando
- Antero Sarrael
- Howard J. Rosen
- Bruce L. Miller
- David Perry
- Raymond Scott Turner
- Kathleen Johnson
- Brigid Reynolds
- Kelly MCCann
- Jessica Poe
- Reisa A. Sperling
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- Jared Tinklenberg
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- Bryan M. Spann
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- Edward Zamrini
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- Ronald Killiany
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- Jesse Mez
- Neil Kowall
- Andrew E. Budson
- Thomas O. Obisesan
- Oyonumo E. Ntekim
- Saba Wolday
- Javed I. Khan
- Evaristus Nwulia
- Sheeba Nadarajah
- Alan Lerner
- Paula Ogrocki
- Curtis Tatsuoka
- Parianne Fatica
- Evan Fletcher
- Pauline Maillard
- John Olichney
- Charles DeCarli
- Owen Carmichael
- Vernice Bates
- Horacio Capote
- Michelle Rainka
- Michael Borrie
- T-Y Lee
- Rob Bartha
- Sterling Johnson
- Sanjay Asthana
- Cynthia M. Carlsson
- Allison Perrin
- Anna Burke
- Douglas W. Scharre
- Maria Kataki
- Rawan Tarawneh
- Brendan Kelley
- David Hart
- Earl A. Zimmerman
- Dzintra Celmins
- Delwyn D. Miller
- Laura L. Boles Ponto
- Karen Ekstam Smith
- Hristina Koleva
- Hyungsub Shim
- Ki Won Nam
- Susan K. Schultz
- Jeff D. Williamson
- Suzanne Craft
- Jo Cleveland
- Mia Yang
- Kaycee M. Sink
- Brian R. Ott
- Jonathan Drake
- Geoffrey Tremont
- Lori A. Daiello
- Jonathan D. Drake
- Marwan Sabbagh
- Aaron Ritter
- Charles Bernick
- Donna Munic
- Akiva Mintz
- Abigail O'Connelll
- Jacobo Mintzer
- Arthur Wiliams
- Joseph Masdeu
- Jiong Shi
- Angelica Garcia
- Marwan Sabbagh
- Paul Newhouse
- Steven Potkin
- Stephen Salloway
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- Stephen Correia
- Smita Kittur
- Godfrey D. Pearlson
- Karen Blank
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- Mary L. Hynes
- Robert B. Santulli
- Norman Relkin
- Gloria Chiang
- Athena Lee
- Michael Lin
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- Michael W. Weiner
- Paul Aisen
- Ron Petersen
- Michael W. Weiner
- Paul Aisen
- Ronald Petersen
- Robert C. Green
- Danielle Harvey
- Clifford R. Jack
- William Jagust
- John C. Morris
- Andrew J. Saykin
- Leslie M. Shaw
- Arthur W. Toga
- John Q. Trojanowki
- Thomas Neylan
- Jordan Grafman
- Robert C. Green
- Tom Montine
- Paul Aisen
- Gustavo Jimenez
- Michael Donohue
- Devon Gessert
- Jennifer Salazar
- Caileigh Zimmerman
- Sarah Walter
- Olusegun Adegoke
- Payam Mahboubi
- Sarah Danowski
- Godfrey Coker
- Taylor Clanton
- Jeremy Pizzola
- Elizabeth Shaffer
- Catherine Nguyen-Barrera
- Thomas Neylan
- Jacqueline Hayes
- Shannon Finley
- Danielle Harvey
- Michael Donohue
- Clifford R. Jack
- Matthew Bernstein
- Bret Borowski
- Jeff Gunter
- Matt Senjem
- Kejal Kantarci
- Chad Ward
- Duygu Tosun-Turgut
- Stephanie Rossi Chen
- Susan Landau
- Robert A. Koeppe
- Norm Foster
- Eric M. Reiman
- Kewei Chen
- John C. Morris
- Richard J. Perrin
- Erin Franklin
- Leslie M. Shaw
- John Q. Trojanowki
- Magdalena Korecka
- Michal Figurski
- Arthur W. Toga
- Karen Crawford
- Scott Neu
- Andrew J. Saykin
- Tatiana M. Foroud
- Steven Potkin
- Li Shen
- Kelley Faber
- Sungeun Kim
- Kwangsik Nho
- Kristi Wilmes
- Lon S. Schneider
- Sonia Pawluczyk
- Mauricio Becerra
- Liberty Teodoro
- Karen Dagerman
- Bryan M. Spann
- James Brewer
- Helen Vanderswag
- Adam Fleisher
- Yaakov Stern
- Lawrence S. Honig
- Akiva Mintz
- Raj C. Shah
- Ajay Sood
- Kimberly S. Blanchard
- Debra Fleischman
- Konstantinos Arfanakis
- Ranjan Duara
- Daniel Varon
- Maria T Greig
- P. Murali Doraiswamy
- Jeffrey R. Petrella
- Olga James
- Salvador Borges-Neto
- Terence Z. Wong
- Anton P. Porsteinsson
- Kimberly S. Martin
- Gaby Thai
- Aimee Pierce
- Christopher Reist
- Beatriz Yanez
- Elizabeth Sosa
- Megan Witbracht
- Carl Sadowsky
- Walter Martinez
- Teresa Villena
- Howard Rosen
- David Perry
- Raymond Scott Turner
- Kathleen Johnson
- Brigid Reynolds
- Kelly MCCann
- Jessica Poe
- Reisa A. Sperling
- Keith A. Johnson
- Gad Marshall
- Christine M. Belden
- Bryan M. Spann
- Kelly A. Clark
- Edward Zamrini
- Marwan Sabbagh
- Thomas O. Obisesan
- Oyonumo E. Ntekim
- Evaristus Nwulia
- Sheeba Nadarajah
- Sanjay Asthana
- Cynthia M. Carlsson
- Elaine R. Peskind
- Eric C. Petrie
- Gail Li
- Jerome Yesavage
- Joy L. Taylor
- Steven Chao
- Jaila Coleman
- Jessica D. White
- Barton Lane
- Allyson Rosen
- Jared Tinklenberg
- Michael Lin
- Gloria Chiang
- Lisa Ravdin
- Norman Relkin
- Abigail O'Connelll
- Jacobo Mintzer
- Arthur Wiliams
- Scott Mackin
- Paul Aisen
- Rema Raman
- Gustavo Jimenez-Maggiora
- Michael Donohue
- Devon Gessert
- Jennifer Salazar
- Caileigh Zimmerman
- Sarah Walter
- Olusegun Adegoke
- Payam Mahboubi
- Scott Mackin
- Michael W. Weiner
- Paul Aisen
- Rema Raman
- Clifford R. Jack
- Susan Landau
- Andrew J. Saykin
- Arthur W. Toga
- Charles DeCarli
- Robert A. Koeppe
- Robert C. Green
- Erin Drake
- Michael W. Weiner
- Paul Aisen
- Rema Raman
- Mike Donohue
- Scott Mackin
- Craig Nelson
- David Bickford
- Meryl Butters
- Michelle Zmuda
- Clifford R. Jack
- Matthew Bernstein
- Bret Borowski
- Jeff Gunter
- Matt Senjem
- Kejal Kantarci
- Chad Ward
- Denise Reyes
- Robert A. Koeppe
- Susan Landau
- Arthur W. Toga
- Karen Crawford
- Scott Neu
- Andrew J. Saykin
- Tatiana M. Foroud
- Kelley M. Faber
- Kwangsik Nho
- Kelly N. Nudelman
- Scott Mackin
- Howard Rosen
- Craig Nelson
- David Bickford
- Yiu Ho Au
- Kelly Scherer
- Daniel Catalinotto
- Samuel Stark
- Elise Ong
- Dariella Fernandez
- Meryl Butters
- Michelle Zmuda
- Oscar L. Lopez
- MaryAnn Oakley
- Donna M. Simpson
Enabling scientific discoveries that improve human health