Human Connectome Project: heritability of brain volumes in young healthy adults.
Cortical
Dizygotic twins
Global
Monozygotic
Subcortical brain volumes
Journal
Experimental brain research
ISSN: 1432-1106
Titre abrégé: Exp Brain Res
Pays: Germany
ID NLM: 0043312
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
06
09
2020
accepted:
04
02
2021
pubmed:
22
2
2021
medline:
29
7
2021
entrez:
21
2
2021
Statut:
ppublish
Résumé
Here we report on the heritability and Intraclass Correlation Coefficients (ICCs) of brain volumes in 1,103 young healthy adults with mean age 29.2 years. Among them are: 153 monozygotic (MZ) twin pairs and 86 dizygotic (DZ) twin pairs, 133 non-twin siblings of MZ twins, 76 non-twin siblings of DZ twins, 335 siblings, and 81 unrelated individuals. ICCs were calculated between pairs of the following genetic groups: (1) MZ twins; (2) DZ twins; (3) MZ twins-their singleton siblings; (4) DZ twins-their singleton siblings; (5) siblings (SB); and (6) unrelated individuals (NR). We studied 4 brain groups: global, lobar, subcortical, and cortical brain regions. For each of 4 brain groups we found the same order of ICCs ranging from the highest values for MZ twins, statistically significantly smaller for the DZ twins and 3 sibling groups, and practically zero for NR. The DZ twins and 3 sibling groups were not different. No hemispheric difference was found in any genetic group. Among brain groups, the highest heritability was for the global regions, followed by lobar and subcortical groups. Only the cortical brain group heritability was statistically lower than other brain groups. We found less genetic control on the left hemisphere than on the right but no significant difference between hemispheres, and no hemispheric lateralization of heritability for any of the brain groups. These findings document substantial and systematic heritability of global and regional brain volumes.
Identifiants
pubmed: 33611617
doi: 10.1007/s00221-021-06057-0
pii: 10.1007/s00221-021-06057-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1273-1286Références
Adams HHH, Hibar DP, Chouraki V et al (2016) Novel genetic loci underlying human intracranial volume identified through genome-wide association. Nat Neurosci 19:1569–1582. https://doi.org/10.1038/nn.4398
doi: 10.1038/nn.4398
pubmed: 27694991
pmcid: 5227112
Baaré WFC, Pol HEH et al (2001) Quantitative genetic modeling of variation in human brain morphology. Cereb Cortex 11:816–824. https://doi.org/10.1093/cercor/11.9.816
doi: 10.1093/cercor/11.9.816
pubmed: 11532887
Baranzini SE, Mudge J, van Velkinburgh JC et al (2010) Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis. Nature 464:1351–1356. https://doi.org/10.1038/nature08990
doi: 10.1038/nature08990
pubmed: 20428171
pmcid: 2862593
Bartley AJ, Jones DW, Weinberger DR (1997) Genetic variability of human brain size and cortical gyral patterns. Brain J Neurol 120:257–269
doi: 10.1093/brain/120.2.257
Batouli SAH, Sachdev PS, Wen W et al (2014) Heritability of brain volumes in older adults: the Older Australian Twins Study. Neurobiol Aging 35:937.e5-937.e18. https://doi.org/10.1016/j.neurobiolaging.2013.10.079
doi: 10.1016/j.neurobiolaging.2013.10.079
Bearden CE, Thompson PM (2017) Emerging global initiatives in neurogenetics: The Enhancing Neuroimaging Genetics through Meta-analysis (ENIGMA) Consortium. Neuron 94:232–236. https://doi.org/10.1016/j.neuron.2017.03.033
doi: 10.1016/j.neuron.2017.03.033
pubmed: 28426957
pmcid: 5918136
Brouwer RM, Panizzon MS, Glahn DC et al (2017) Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: results of the ENIGMA plasticity working group. Hum Brain Mapp 38:4444–4458. https://doi.org/10.1002/hbm.23672
doi: 10.1002/hbm.23672
pubmed: 28580697
pmcid: 5572837
Chou Y-Y, Leporé N, Chiang M-C et al (2009) Mapping genetic influences on ventricular structure in twins. NeuroImage 44:1312–1323. https://doi.org/10.1016/j.neuroimage.2008.10.036
doi: 10.1016/j.neuroimage.2008.10.036
pubmed: 19041405
Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021
doi: 10.1016/j.neuroimage.2006.01.021
Eyler LT, Prom-Wormley E, Fennema-Notestine C, Panizzon MS, Neale MC, Jernigan TL et al (2011) Genetic patterns of correlation among subcortical volumes in humans: results from a magnetic resonance imaging twin study. Hum Brain Mapp 32(4):641–653
doi: 10.1002/hbm.21054
Eyler LT, Chen C-H, Panizzon MS, Fennema-Notestine C, Neale MC, Jak A et al (2012) A comparison of heritability maps of cortical surface area and thickness and the influence of adjustment for whole brain measures: a magnetic resonance imaging twin study. Twin Research and Human Genetics 15(3):304–314
doi: 10.1017/thg.2012.3
Eyler LT, Vuoksimaa E, Panizzon MS, Fennema-Notestine C, Neale MC, Chen C-H et al (2014) Conceptual and data-based investigation of genetic influences and brain asymmetry: a twin study of multiple structural phenotypes. J Cognit Neurosci 26(5):1100–1117
doi: 10.1162/jocn_a_00531
Falconer DS (1965) The inheritance of liability to certain diseases, estimated from the incidence among relatives. Ann Hum Genet 29:51–76. https://doi.org/10.1111/j.1469-1809.1965.tb00500.x
doi: 10.1111/j.1469-1809.1965.tb00500.x
Falconer DS, Mackay TF, Frankham R (1996) Introduction to quantitative genetics (4th edn). Trends Genet 12:280
doi: 10.1016/0168-9525(96)81458-2
Fisher RA (1958) Statistical methods for research workers. Hafner, New York
Geschwind DH, Miller BL, DeCarli C, Carmelli D (2002) Heritability of lobar brain volumes in twins supports genetic models of cerebral laterality and handedness. PNAS 99:3176–3181. https://doi.org/10.1073/pnas.052494999
doi: 10.1073/pnas.052494999
pubmed: 11867730
Giraudeau B (1996) Negative values of the intraclass correlation coefficient are not theoretically possible. J Clin Epidemiol 49:1205–1206
doi: 10.1016/0895-4356(96)00053-4
Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL et al (2013) The minimal preprocessing pipelines for the Human Connectome Project. NeuroImage 80:105–124
doi: 10.1016/j.neuroimage.2013.04.127
Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. PNAS 101(21):8174–8179
doi: 10.1073/pnas.0402680101
Gómez-Robles A, Hopkins WD, Schapiro SJ, Sherwood CC (2016) The heritability of chimpanzee and human brain asymmetry. Proc R Soc B Biol Sci 283(1845):20161319
doi: 10.1098/rspb.2016.1319
Greenspan KS, Arakelian CR, van Erp TGM (2016) Heritability of hippocampal formation sub-region volumes. J Neurol Neurosci. https://doi.org/10.21767/2171-6625.1000159
doi: 10.21767/2171-6625.1000159
pubmed: 28503392
pmcid: 5424602
Hedman AM, van Haren NEM, Schnack HG et al (2012) Human brain changes across the life span: a review of 56 longitudinal magnetic resonance imaging studies. Hum Brain Mapp 33:1987–2002. https://doi.org/10.1002/hbm.21334
doi: 10.1002/hbm.21334
pubmed: 21915942
Hibar DP, Adams HHH, Jahanshad N et al (2017) Novel genetic loci associated with hippocampal volume. Nat Commun. https://doi.org/10.1038/ncomms13624
doi: 10.1038/ncomms13624
pubmed: 28098162
pmcid: 5253632
Hulshoff Pol HE, Posthuma D, Baaré WFC et al (2002) Twin-singleton differences in brain structure using structural equation modelling. Brain 125:384–390
doi: 10.1093/brain/awf035
Hulshoff Pol HE, Schnack HG, Posthuma D et al (2006) Genetic contributions to human brain morphology and intelligence. J Neurosci 26:10235–10242. https://doi.org/10.1523/JNEUROSCI.1312-06.2006
doi: 10.1523/JNEUROSCI.1312-06.2006
pubmed: 17021179
pmcid: 6674628
Kochunov P, Donohue B, Mitchell BD, Ganjgahi H, Adhikari B, Ryan M et al (2019) Genomic kinship construction to enhance genetic analyses in the human connectome project data. Hum Brain Mapp 40(5):1677–1688
doi: 10.1002/hbm.24479
Kong X-Z, Mathias SR, Guadalupe T, Glahn DC, Franke B, Group ELW et al (2018) Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. PNAS 115(22):E5154–E5163
doi: 10.1073/pnas.1718418115
Lenroot RK, Schmitt JE, Ordaz SJ, Wallace GL, Neale MC, Lerch JP et al (2009) Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence. Hum Brain Mapp 30(1):163–174
doi: 10.1002/hbm.20494
Lukies MW, Watanabe Y, Tanaka H et al (2017) Heritability of brain volume on MRI in middle to advanced age: a twin study of Japanese adults. PLoS ONE 12:e0175800. https://doi.org/10.1371/journal.pone.0175800
doi: 10.1371/journal.pone.0175800
pubmed: 28426696
pmcid: 5398540
Ordaz SJ, Lenroot RK, Wallace GL et al (2010) Are there differences in brain morphometry between twins and unrelated singletons? A pediatric MRI study. Genes Brain Behav 9:288–295. https://doi.org/10.1111/j.1601-183X.2009.00558.x
doi: 10.1111/j.1601-183X.2009.00558.x
pubmed: 20100212
Patel S, Park MTM, Devenyi GA et al (2017) Heritability of hippocampal subfield volumes using a twin and non-twin siblings design. Hum Brain Mapp 38:4337–4352. https://doi.org/10.1002/hbm.23654
doi: 10.1002/hbm.23654
pubmed: 28561418
pmcid: 6866954
Patel S, Patel R, Park MTM, Masellis M, Knight J, Chakravarty MM (2018) Heritability estimates of cortical anatomy: the influence and reliability of different estimation strategies. NeuroImage 178:78–91
doi: 10.1016/j.neuroimage.2018.05.014
Pfefferbaum A, Sullivan EV, Swan GE, Carmelli D (2000) Brain structure in men remains highly heritable in the seventh and eighth decades of life. Neurobiol Aging 21:63–74. https://doi.org/10.1016/S0197-4580(00)00086-5
doi: 10.1016/S0197-4580(00)00086-5
pubmed: 10794850
Posthuma D, de Geus EJ, Neale MC et al (2000) Multivariate genetic analysis of brain structure in an extended twin design. Behav Genet 30:311–319
doi: 10.1023/A:1026501501434
Powell HWR, Parker GJM, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CAM et al (2006) Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. NeuroImage 32(1):388–399
doi: 10.1016/j.neuroimage.2006.03.011
Rentería ME, Hansell NK, Strike LT et al (2014) Genetic architecture of subcortical brain regions: common and region-specific genetic contributions. Genes Brain Behav 13:821–830. https://doi.org/10.1111/gbb.12177
doi: 10.1111/gbb.12177
pubmed: 25199620
pmcid: 4241157
Scamvougeras A, Kigar DL, Jones D et al (2003) Size of the human corpus callosum is genetically determined: an MRI study in mono and dizygotic twins. Neurosci Lett 338:91–94. https://doi.org/10.1016/S0304-3940(02)01333-2
doi: 10.1016/S0304-3940(02)01333-2
pubmed: 12566160
Schmitt JE, Wallace GL, Lenroot RK et al (2010) A twin study of intracerebral volumetric relationships. Behav Genet 40:114–124. https://doi.org/10.1007/s10519-010-9332-6
doi: 10.1007/s10519-010-9332-6
pubmed: 20112130
pmcid: 3403699
Schmitt JE, Neale MC, Fassassi B, Perez J, Lenroot RK, Wells EM et al (2014) The dynamic role of genetics on cortical patterning during childhood and adolescence. PNAS 111(18):6774–6779
doi: 10.1073/pnas.1311630111
Schmitt JE, Giedd JN, Raznahan A, Neale MC (2018) The genetic contributions to maturational coupling in the human cerebrum: a longitudinal pediatric twin imaging study. Cereb Cortex 28(9):3184–3191
doi: 10.1093/cercor/bhx190
Schmitt JE, Raznahan A, Clasen LS, Wallace GL, Pritikin JN, Lee NR et al (2019) The dynamic associations between cortical thickness and general intelligence are genetically mediated. Cereb Cortex 29(11):4743–4752
doi: 10.1093/cercor/bhz007
Strike LT, Couvy-Duchesne B, Hansell NK, Cuellar-Partida G, Medland SE, Wright MJ (2015) Genetics and brain morphology. Neuropsychol Rev 25(1):63–96
doi: 10.1007/s11065-015-9281-1
Strike LT, Hansell NK, Couvy-Duchesne B, Thompson PM, de Zubicaray GI, McMahon KL et al (2019) Genetic complexity of cortical structure: differences in genetic and environmental factors influencing cortical surface area and thickness. Cereb Cortex 29(3):952–962
doi: 10.1093/cercor/bhy002
Thompson PM, Cannon TD, Narr KL, van Erp T, Poutanen V-P, Huttunen M et al (2001) Genetic influences on brain structure. Nat Neurosci 4(12):1253–1258
doi: 10.1038/nn758
Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4(1):37–48
doi: 10.1038/nrn1009
Toro R, Poline J-B, Huguet G, Loth E, Frouin V, Banaschewski T et al (2015) Genomic architecture of human neuroanatomical diversity. Mol Psychiatry 20(8):1011–1016
doi: 10.1038/mp.2014.99
Tzourio N, Nkanga-Ngila B, Mazoyer B (1998) Left planum temporale surface correlates with functional dominance during story listening. NeuroReport 9(5):829–833
doi: 10.1097/00001756-199803300-00012
Uğurbil K, Xu J, Auerbach EJ, Moeller S, Vu AT, Duarte-Carvajalino JM et al (2013) Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project. Neuroimage 80:80–104
doi: 10.1016/j.neuroimage.2013.05.012
van der Meer D, Rokicki J, Kaufmann T, Córdova-Palomera A, Moberget T, Alnæs D et al (2020) Brain scans from 21,297 individuals reveal the genetic architecture of hippocampal subfield volumes. Mol Psychiatry 25(11):3053–3065
doi: 10.1038/s41380-018-0262-7
Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K (2013) The WU-Minn human connectome project: an overview. Neuroimage 80:62–79
doi: 10.1016/j.neuroimage.2013.05.041
Visscher PM, Medland SE, Ferreira MAR et al (2006) Assumption-free estimation of heritability from genome-wide identity-by-descent sharing between full siblings. PLoS Genet 2:e41. https://doi.org/10.1371/journal.pgen.0020041
doi: 10.1371/journal.pgen.0020041
pubmed: 16565746
pmcid: 1413498
Visscher PM, Macgregor S, Benyamin B et al (2007) Genome partitioning of genetic variation for height from 11,214 sibling pairs. Am J Hum Genet 81:1104–1110. https://doi.org/10.1086/522934
doi: 10.1086/522934
pubmed: 17924350
pmcid: 2265649
Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era–concepts and misconceptions. Nat Rev Genet 9:255–266. https://doi.org/10.1038/nrg2322
doi: 10.1038/nrg2322
pubmed: 18319743
Wallace GL, Eric Schmitt J, Lenroot R et al (2006) A pediatric twin study of brain morphometry. J Child Psychol Psychiatry 47:987–993. https://doi.org/10.1111/j.1469-7610.2006.01676.x
doi: 10.1111/j.1469-7610.2006.01676.x
pubmed: 17073977
Wen W, Thalamuthu A, Mather KA et al (2016) Distinct genetic influences on cortical and subcortical brain structures. Sci Rep. https://doi.org/10.1038/srep32760
doi: 10.1038/srep32760
pubmed: 28009018
pmcid: 5180224
Wright IC, Sham P, Murray RM et al (2002) Genetic contributions to regional variability in human brain structure: methods and preliminary results. NeuroImage 17:256–271. https://doi.org/10.1006/nimg.2002.1163
doi: 10.1006/nimg.2002.1163
pubmed: 12482082
Zhao B, Luo T, Li T, Li Y, Zhang J, Shan Y et al (2019) Genome-wide association analysis of 19,629 individuals identifies variants influencing regional brain volumes and refines their genetic co-architecture with cognitive and mental health traits. Nat Genet 51(11):1637–1644
doi: 10.1038/s41588-019-0516-6