Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group

Rachel M. Brouwer; Matthew S. Panizzon; David C. Glahn; Derrek P. Hibar; Xue Hua; Neda Jahanshad; Lucija Abramovic; Greig I. de Zubicaray; Carol E. Franz; Narelle K. Hansell; Ian B. Hickie; Marinka M.G. Koenis; Nicholas G. Martin; Karen A. Mather; Katie L. McMahon; Hugo G. Schnack; Lachlan T. Strike; Suzanne C. Swagerman; Anbupalam Thalamuthu; Wei Wen; John H. Gilmore; Nitin Gogtay; René S. Kahn; Perminder S. Sachdev; Margaret J. Wright; Dorret I. Boomsma; William S. Kremen; Paul M. Thompson; Hilleke E. Hulshoff Pol

doi:10.1002/hbm.23672

Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group

Rachel M. Brouwer, Matthew S. Panizzon, David C. Glahn, Derrek P. Hibar, Xue Hua, Neda Jahanshad, Lucija Abramovic, Greig I. de Zubicaray, Carol E. Franz, Narelle K. Hansell, Ian B. Hickie, Marinka M.G. Koenis, Nicholas G. Martin, Karen A. Mather, Katie L. McMahon, Hugo G. Schnack, Lachlan T. Strike, Suzanne C. Swagerman, Anbupalam Thalamuthu, Wei WenJohn H. Gilmore, Nitin Gogtay, René S. Kahn, Perminder S. Sachdev, Margaret J. Wright, Dorret I. Boomsma, William S. Kremen, Paul M. Thompson, Hilleke E. Hulshoff Pol

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

34 Scopus citations

Abstract

Structural brain changes that occur during development and ageing are related to mental health and general cognitive functioning. Individuals differ in the extent to which their brain volumes change over time, but whether these differences can be attributed to differences in their genotypes has not been widely studied. Here we estimate heritability (h²) of changes in global and subcortical brain volumes in five longitudinal twin cohorts from across the world and in different stages of the lifespan (N = 861). Heritability estimates of brain changes were significant and ranged from 16% (caudate) to 42% (cerebellar gray matter) for all global and most subcortical volumes (with the exception of thalamus and pallidum). Heritability estimates of change rates were generally higher in adults than in children suggesting an increasing influence of genetic factors explaining individual differences in brain structural changes with age. In children, environmental influences in part explained individual differences in developmental changes in brain structure. Multivariate genetic modeling showed that genetic influences of change rates and baseline volume significantly overlapped for many structures. The genetic influences explaining individual differences in the change rate for cerebellum, cerebellar gray matter and lateral ventricles were independent of the genetic influences explaining differences in their baseline volumes. These results imply the existence of genetic variants that are specific for brain plasticity, rather than brain volume itself. Identifying these genes may increase our understanding of brain development and ageing and possibly have implications for diseases that are characterized by deviant developmental trajectories of brain structure. Hum Brain Mapp 38:4444–4458, 2017.

Original language	English (US)
Pages (from-to)	4444-4458
Number of pages	15
Journal	Human Brain Mapping
Volume	38
Issue number	9
DOIs	https://doi.org/10.1002/hbm.23672
State	Published - Sep 2017
Externally published	Yes

Keywords

ENIGMA plasticity working group
heritability
individual brain plasticity
longitudinal magnetic resonance imaging
twins

ASJC Scopus subject areas

Anatomy
Radiological and Ultrasound Technology
Radiology Nuclear Medicine and imaging
Neurology
Clinical Neurology

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10.1002/hbm.23672

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Brouwer, R. M., Panizzon, M. S., Glahn, D. C., Hibar, D. P., Hua, X., Jahanshad, N., Abramovic, L., de Zubicaray, G. I., Franz, C. E., Hansell, N. K., Hickie, I. B., Koenis, M. M. G., Martin, N. G., Mather, K. A., McMahon, K. L., Schnack, H. G., Strike, L. T., Swagerman, S. C., Thalamuthu, A., ... Hulshoff Pol, H. E. (2017). Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group. Human Brain Mapping, 38(9), 4444-4458. https://doi.org/10.1002/hbm.23672

Brouwer, RM, Panizzon, MS, Glahn, DC, Hibar, DP, Hua, X, Jahanshad, N, Abramovic, L, de Zubicaray, GI, Franz, CE, Hansell, NK, Hickie, IB, Koenis, MMG, Martin, NG, Mather, KA, McMahon, KL, Schnack, HG, Strike, LT, Swagerman, SC, Thalamuthu, A, Wen, W, Gilmore, JH, Gogtay, N, Kahn, RS, Sachdev, PS, Wright, MJ, Boomsma, DI, Kremen, WS, Thompson, PM & Hulshoff Pol, HE 2017, 'Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group', Human Brain Mapping, vol. 38, no. 9, pp. 4444-4458. https://doi.org/10.1002/hbm.23672

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title = "Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group",

abstract = "Structural brain changes that occur during development and ageing are related to mental health and general cognitive functioning. Individuals differ in the extent to which their brain volumes change over time, but whether these differences can be attributed to differences in their genotypes has not been widely studied. Here we estimate heritability (h2) of changes in global and subcortical brain volumes in five longitudinal twin cohorts from across the world and in different stages of the lifespan (N = 861). Heritability estimates of brain changes were significant and ranged from 16% (caudate) to 42% (cerebellar gray matter) for all global and most subcortical volumes (with the exception of thalamus and pallidum). Heritability estimates of change rates were generally higher in adults than in children suggesting an increasing influence of genetic factors explaining individual differences in brain structural changes with age. In children, environmental influences in part explained individual differences in developmental changes in brain structure. Multivariate genetic modeling showed that genetic influences of change rates and baseline volume significantly overlapped for many structures. The genetic influences explaining individual differences in the change rate for cerebellum, cerebellar gray matter and lateral ventricles were independent of the genetic influences explaining differences in their baseline volumes. These results imply the existence of genetic variants that are specific for brain plasticity, rather than brain volume itself. Identifying these genes may increase our understanding of brain development and ageing and possibly have implications for diseases that are characterized by deviant developmental trajectories of brain structure. Hum Brain Mapp 38:4444–4458, 2017.",

keywords = "ENIGMA plasticity working group, heritability, individual brain plasticity, longitudinal magnetic resonance imaging, twins",

author = "Brouwer, {Rachel M.} and Panizzon, {Matthew S.} and Glahn, {David C.} and Hibar, {Derrek P.} and Xue Hua and Neda Jahanshad and Lucija Abramovic and {de Zubicaray}, {Greig I.} and Franz, {Carol E.} and Hansell, {Narelle K.} and Hickie, {Ian B.} and Koenis, {Marinka M.G.} and Martin, {Nicholas G.} and Mather, {Karen A.} and McMahon, {Katie L.} and Schnack, {Hugo G.} and Strike, {Lachlan T.} and Swagerman, {Suzanne C.} and Anbupalam Thalamuthu and Wei Wen and Gilmore, {John H.} and Nitin Gogtay and Kahn, {Ren{\'e} S.} and Sachdev, {Perminder S.} and Wright, {Margaret J.} and Boomsma, {Dorret I.} and Kremen, {William S.} and Thompson, {Paul M.} and {Hulshoff Pol}, {Hilleke E.}",

note = "Funding Information: BrainSCALE and Utwins1 We thank all the participating families. QTIM: We are grateful to the twins for their generosity of time and willingness to participate in our studies. We thank research assistants Marlene Grace, Ann Eldridge, and Kerrie McAloney, radiographers Aiman Al Najjar and Anita Burns for acquisition of the scans, and David Smyth, Anthony Conciatore, Daniel Park, and David Butler for IT support. OATS: We gratefully acknowledge and thank the OATS participants and the OATS research team. OATS was facilitated through access to the Australian Twin Registry, which is administered by Melbourne University. Publisher Copyright: {\textcopyright} 2017 Wiley Periodicals, Inc.",

year = "2017",

month = sep,

doi = "10.1002/hbm.23672",

language = "English (US)",

volume = "38",

pages = "4444--4458",

journal = "Human Brain Mapping",

issn = "1065-9471",

publisher = "Wiley-Liss Inc.",

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T1 - Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes

T2 - Results of the ENIGMA plasticity working group

AU - Brouwer, Rachel M.

AU - Panizzon, Matthew S.

AU - Glahn, David C.

AU - Hibar, Derrek P.

AU - Hua, Xue

AU - Jahanshad, Neda

AU - Abramovic, Lucija

AU - de Zubicaray, Greig I.

AU - Franz, Carol E.

AU - Hansell, Narelle K.

AU - Hickie, Ian B.

AU - Koenis, Marinka M.G.

AU - Martin, Nicholas G.

AU - Mather, Karen A.

AU - McMahon, Katie L.

AU - Schnack, Hugo G.

AU - Strike, Lachlan T.

AU - Swagerman, Suzanne C.

AU - Thalamuthu, Anbupalam

AU - Wen, Wei

AU - Gilmore, John H.

AU - Gogtay, Nitin

AU - Kahn, René S.

AU - Sachdev, Perminder S.

AU - Wright, Margaret J.

AU - Boomsma, Dorret I.

AU - Kremen, William S.

AU - Thompson, Paul M.

AU - Hulshoff Pol, Hilleke E.

N1 - Funding Information: BrainSCALE and Utwins1 We thank all the participating families. QTIM: We are grateful to the twins for their generosity of time and willingness to participate in our studies. We thank research assistants Marlene Grace, Ann Eldridge, and Kerrie McAloney, radiographers Aiman Al Najjar and Anita Burns for acquisition of the scans, and David Smyth, Anthony Conciatore, Daniel Park, and David Butler for IT support. OATS: We gratefully acknowledge and thank the OATS participants and the OATS research team. OATS was facilitated through access to the Australian Twin Registry, which is administered by Melbourne University. Publisher Copyright: © 2017 Wiley Periodicals, Inc.

PY - 2017/9

Y1 - 2017/9

N2 - Structural brain changes that occur during development and ageing are related to mental health and general cognitive functioning. Individuals differ in the extent to which their brain volumes change over time, but whether these differences can be attributed to differences in their genotypes has not been widely studied. Here we estimate heritability (h2) of changes in global and subcortical brain volumes in five longitudinal twin cohorts from across the world and in different stages of the lifespan (N = 861). Heritability estimates of brain changes were significant and ranged from 16% (caudate) to 42% (cerebellar gray matter) for all global and most subcortical volumes (with the exception of thalamus and pallidum). Heritability estimates of change rates were generally higher in adults than in children suggesting an increasing influence of genetic factors explaining individual differences in brain structural changes with age. In children, environmental influences in part explained individual differences in developmental changes in brain structure. Multivariate genetic modeling showed that genetic influences of change rates and baseline volume significantly overlapped for many structures. The genetic influences explaining individual differences in the change rate for cerebellum, cerebellar gray matter and lateral ventricles were independent of the genetic influences explaining differences in their baseline volumes. These results imply the existence of genetic variants that are specific for brain plasticity, rather than brain volume itself. Identifying these genes may increase our understanding of brain development and ageing and possibly have implications for diseases that are characterized by deviant developmental trajectories of brain structure. Hum Brain Mapp 38:4444–4458, 2017.

AB - Structural brain changes that occur during development and ageing are related to mental health and general cognitive functioning. Individuals differ in the extent to which their brain volumes change over time, but whether these differences can be attributed to differences in their genotypes has not been widely studied. Here we estimate heritability (h2) of changes in global and subcortical brain volumes in five longitudinal twin cohorts from across the world and in different stages of the lifespan (N = 861). Heritability estimates of brain changes were significant and ranged from 16% (caudate) to 42% (cerebellar gray matter) for all global and most subcortical volumes (with the exception of thalamus and pallidum). Heritability estimates of change rates were generally higher in adults than in children suggesting an increasing influence of genetic factors explaining individual differences in brain structural changes with age. In children, environmental influences in part explained individual differences in developmental changes in brain structure. Multivariate genetic modeling showed that genetic influences of change rates and baseline volume significantly overlapped for many structures. The genetic influences explaining individual differences in the change rate for cerebellum, cerebellar gray matter and lateral ventricles were independent of the genetic influences explaining differences in their baseline volumes. These results imply the existence of genetic variants that are specific for brain plasticity, rather than brain volume itself. Identifying these genes may increase our understanding of brain development and ageing and possibly have implications for diseases that are characterized by deviant developmental trajectories of brain structure. Hum Brain Mapp 38:4444–4458, 2017.

KW - ENIGMA plasticity working group

KW - heritability

KW - individual brain plasticity

KW - longitudinal magnetic resonance imaging

KW - twins

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Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: Results of the ENIGMA plasticity working group

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