Individual Variation in Functional Topography of Association Networks in Youth

Zaixu Cui; Hongming Li; Cedric H. Xia; Bart Larsen; Azeez Adebimpe; Graham L. Baum; Matt Cieslak; Raquel E. Gur; Ruben C. Gur; Tyler M. Moore; Desmond J. Oathes; Aaron F. Alexander-Bloch; Armin Raznahan; David R. Roalf; Russell T. Shinohara; Daniel H. Wolf; Christos Davatzikos; Danielle S. Bassett; Damien A. Fair; Yong Fan; Theodore D. Satterthwaite

doi:10.1016/j.neuron.2020.01.029

Individual Variation in Functional Topography of Association Networks in Youth

Zaixu Cui, Hongming Li, Cedric H. Xia, Bart Larsen, Azeez Adebimpe, Graham L. Baum, Matt Cieslak, Raquel E. Gur, Ruben C. Gur, Tyler M. Moore, Desmond J. Oathes, Aaron F. Alexander-Bloch, Armin Raznahan, David R. Roalf, Russell T. Shinohara, Daniel H. Wolf, Christos Davatzikos, Danielle S. Bassett, Damien A. Fair, Yong FanTheodore D. Satterthwaite

Research output: Contribution to journal › Article › peer-review

158 Scopus citations

Abstract

The spatial distribution of large-scale functional networks on the cerebral cortex differs between individuals and is particularly variable in association networks that are responsible for higher-order cognition. However, it remains unknown how this functional topography evolves in development and supports cognition. Capitalizing on advances in machine learning and a large sample imaged with 27 min of high-quality functional MRI (fMRI) data (n = 693, ages 8–23 years), we delineate how functional topography evolves during youth. We found that the functional topography of association networks is refined with age, allowing accurate prediction of unseen individuals’ brain maturity. The cortical representation of association networks predicts individual differences in executive function. Finally, variability of functional topography is associated with fundamental properties of brain organization, including evolutionary expansion, cortical myelination, and cerebral blood flow. Our results emphasize the importance of considering the plasticity and diversity of functional neuroanatomy during development and suggest advances in personalized therapeutics.

Original language	English (US)
Pages (from-to)	340-353.e8
Journal	Neuron
Volume	106
Issue number	2
DOIs	https://doi.org/10.1016/j.neuron.2020.01.029
State	Published - Apr 22 2020

Bibliographical note

Funding Information:
This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute. We thank Ru Kong and Jingwei Li for help with the MS-HBM. T.D.S. and Z.C. designed the study. Z.C. and T.D.S. performed the analyses with support from H.L. B.L. A.A. G.L.B. and M.C. H.L. and Y.F. provided parcellation tools. H.L. replicated all analyses. Z.C. C.H.X. and T.D.S. created the figures. A.A. M.C. T.M.M. D.R.R. and T.D.S. completed data preprocessing. R.E.G. R.C.G. C.D. and T.D.S. provided resources. D.S.B. A.F.A.-B. A.R. D.J.O. R.T.S. D.H.W. C.D. D.A.F. and Y.F. commented on analyses. Z.C. and T.D.S. wrote the manuscript with review and editing from all other authors. R.T.S. has received income from Genentech/Roche. All other authors declare no competing interests.

Funding Information:
This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute . We thank Ru Kong and Jingwei Li for help with the MS-HBM.

Publisher Copyright:
© 2020 Elsevier Inc.

Keywords

MRI
adolescence
cognition
cognitive control
development
executive function
functional MRI
network
parcellation
topography

Publisher link

10.1016/j.neuron.2020.01.029

Find It

Find It at U of M Libraries

Cite this

Cui, Z., Li, H., Xia, C. H., Larsen, B., Adebimpe, A., Baum, G. L., Cieslak, M., Gur, R. E., Gur, R. C., Moore, T. M., Oathes, D. J., Alexander-Bloch, A. F., Raznahan, A., Roalf, D. R., Shinohara, R. T., Wolf, D. H., Davatzikos, C., Bassett, D. S., Fair, D. A., ... Satterthwaite, T. D. (2020). Individual Variation in Functional Topography of Association Networks in Youth. Neuron, 106(2), 340-353.e8. https://doi.org/10.1016/j.neuron.2020.01.029

Cui, Z, Li, H, Xia, CH, Larsen, B, Adebimpe, A, Baum, GL, Cieslak, M, Gur, RE, Gur, RC, Moore, TM, Oathes, DJ, Alexander-Bloch, AF, Raznahan, A, Roalf, DR, Shinohara, RT, Wolf, DH, Davatzikos, C, Bassett, DS, Fair, DA, Fan, Y & Satterthwaite, TD 2020, 'Individual Variation in Functional Topography of Association Networks in Youth', Neuron, vol. 106, no. 2, pp. 340-353.e8. https://doi.org/10.1016/j.neuron.2020.01.029

@article{77c8f9f9ff284b3aa97e55e77b8830c3,

title = "Individual Variation in Functional Topography of Association Networks in Youth",

abstract = "The spatial distribution of large-scale functional networks on the cerebral cortex differs between individuals and is particularly variable in association networks that are responsible for higher-order cognition. However, it remains unknown how this functional topography evolves in development and supports cognition. Capitalizing on advances in machine learning and a large sample imaged with 27 min of high-quality functional MRI (fMRI) data (n = 693, ages 8–23 years), we delineate how functional topography evolves during youth. We found that the functional topography of association networks is refined with age, allowing accurate prediction of unseen individuals{\textquoteright} brain maturity. The cortical representation of association networks predicts individual differences in executive function. Finally, variability of functional topography is associated with fundamental properties of brain organization, including evolutionary expansion, cortical myelination, and cerebral blood flow. Our results emphasize the importance of considering the plasticity and diversity of functional neuroanatomy during development and suggest advances in personalized therapeutics.",

keywords = "MRI, adolescence, cognition, cognitive control, development, executive function, functional MRI, network, parcellation, topography",

author = "Zaixu Cui and Hongming Li and Xia, {Cedric H.} and Bart Larsen and Azeez Adebimpe and Baum, {Graham L.} and Matt Cieslak and Gur, {Raquel E.} and Gur, {Ruben C.} and Moore, {Tyler M.} and Oathes, {Desmond J.} and Alexander-Bloch, {Aaron F.} and Armin Raznahan and Roalf, {David R.} and Shinohara, {Russell T.} and Wolf, {Daniel H.} and Christos Davatzikos and Bassett, {Danielle S.} and Fair, {Damien A.} and Yong Fan and Satterthwaite, {Theodore D.}",

note = "Funding Information: This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute. We thank Ru Kong and Jingwei Li for help with the MS-HBM. T.D.S. and Z.C. designed the study. Z.C. and T.D.S. performed the analyses with support from H.L. B.L. A.A. G.L.B. and M.C. H.L. and Y.F. provided parcellation tools. H.L. replicated all analyses. Z.C. C.H.X. and T.D.S. created the figures. A.A. M.C. T.M.M. D.R.R. and T.D.S. completed data preprocessing. R.E.G. R.C.G. C.D. and T.D.S. provided resources. D.S.B. A.F.A.-B. A.R. D.J.O. R.T.S. D.H.W. C.D. D.A.F. and Y.F. commented on analyses. Z.C. and T.D.S. wrote the manuscript with review and editing from all other authors. R.T.S. has received income from Genentech/Roche. All other authors declare no competing interests. Funding Information: This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute . We thank Ru Kong and Jingwei Li for help with the MS-HBM. Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",

year = "2020",

month = apr,

day = "22",

doi = "10.1016/j.neuron.2020.01.029",

language = "English (US)",

volume = "106",

pages = "340--353.e8",

journal = "Neuron",

issn = "0896-6273",

publisher = "Cell Press",

number = "2",

}

TY - JOUR

T1 - Individual Variation in Functional Topography of Association Networks in Youth

AU - Cui, Zaixu

AU - Li, Hongming

AU - Xia, Cedric H.

AU - Larsen, Bart

AU - Adebimpe, Azeez

AU - Baum, Graham L.

AU - Cieslak, Matt

AU - Gur, Raquel E.

AU - Gur, Ruben C.

AU - Moore, Tyler M.

AU - Oathes, Desmond J.

AU - Alexander-Bloch, Aaron F.

AU - Raznahan, Armin

AU - Roalf, David R.

AU - Shinohara, Russell T.

AU - Wolf, Daniel H.

AU - Davatzikos, Christos

AU - Bassett, Danielle S.

AU - Fair, Damien A.

AU - Fan, Yong

AU - Satterthwaite, Theodore D.

N1 - Funding Information: This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute. We thank Ru Kong and Jingwei Li for help with the MS-HBM. T.D.S. and Z.C. designed the study. Z.C. and T.D.S. performed the analyses with support from H.L. B.L. A.A. G.L.B. and M.C. H.L. and Y.F. provided parcellation tools. H.L. replicated all analyses. Z.C. C.H.X. and T.D.S. created the figures. A.A. M.C. T.M.M. D.R.R. and T.D.S. completed data preprocessing. R.E.G. R.C.G. C.D. and T.D.S. provided resources. D.S.B. A.F.A.-B. A.R. D.J.O. R.T.S. D.H.W. C.D. D.A.F. and Y.F. commented on analyses. Z.C. and T.D.S. wrote the manuscript with review and editing from all other authors. R.T.S. has received income from Genentech/Roche. All other authors declare no competing interests. Funding Information: This study was supported by R01MH113550, R01EB022573, R01MH107703, RF1MH116920, R01MH112847, P50MH096891, R01MH11186, K01MH102609, R01MH107235, R01NS085211, RC2MH08998, RC2MH089924, and the Penn/CHOP Lifespan Brain Institute . We thank Ru Kong and Jingwei Li for help with the MS-HBM. Publisher Copyright: © 2020 Elsevier Inc.

PY - 2020/4/22

Y1 - 2020/4/22

N2 - The spatial distribution of large-scale functional networks on the cerebral cortex differs between individuals and is particularly variable in association networks that are responsible for higher-order cognition. However, it remains unknown how this functional topography evolves in development and supports cognition. Capitalizing on advances in machine learning and a large sample imaged with 27 min of high-quality functional MRI (fMRI) data (n = 693, ages 8–23 years), we delineate how functional topography evolves during youth. We found that the functional topography of association networks is refined with age, allowing accurate prediction of unseen individuals’ brain maturity. The cortical representation of association networks predicts individual differences in executive function. Finally, variability of functional topography is associated with fundamental properties of brain organization, including evolutionary expansion, cortical myelination, and cerebral blood flow. Our results emphasize the importance of considering the plasticity and diversity of functional neuroanatomy during development and suggest advances in personalized therapeutics.

AB - The spatial distribution of large-scale functional networks on the cerebral cortex differs between individuals and is particularly variable in association networks that are responsible for higher-order cognition. However, it remains unknown how this functional topography evolves in development and supports cognition. Capitalizing on advances in machine learning and a large sample imaged with 27 min of high-quality functional MRI (fMRI) data (n = 693, ages 8–23 years), we delineate how functional topography evolves during youth. We found that the functional topography of association networks is refined with age, allowing accurate prediction of unseen individuals’ brain maturity. The cortical representation of association networks predicts individual differences in executive function. Finally, variability of functional topography is associated with fundamental properties of brain organization, including evolutionary expansion, cortical myelination, and cerebral blood flow. Our results emphasize the importance of considering the plasticity and diversity of functional neuroanatomy during development and suggest advances in personalized therapeutics.

KW - MRI

KW - adolescence

KW - cognition

KW - cognitive control

KW - development

KW - executive function

KW - functional MRI

KW - network

KW - parcellation

KW - topography

UR - http://www.scopus.com/inward/record.url?scp=85081542531&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85081542531&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2020.01.029

DO - 10.1016/j.neuron.2020.01.029

M3 - Article

C2 - 32078800

AN - SCOPUS:85081542531

SN - 0896-6273

VL - 106

SP - 340-353.e8

JO - Neuron

JF - Neuron

IS - 2

ER -

Individual Variation in Functional Topography of Association Networks in Youth

Abstract

Bibliographical note

Keywords

Publisher link

Find It

Other files and links

Fingerprint

Cite this