Heritable changes in regional cortical thickness with age

Brain Imaging and Behavior

Volumn 8, Issue 2, 2014, Pages 208-216

  Chouinard Decorte, Francois ^a   McKay, D Reese ^b,c   Reid, Andrew ^a   Khundrakpam, Budhachandra ^a   Zhao, Lu ^a   Karama, Sherif ^a,d   Rioux, Pierre ^a   Sprooten, Emma ^b,c   Knowles, Emma ^b,c   Kent Jr , Jack W ^e   Curran, Joanne E ^e   Göring, Harald H H ^e   Dyer, Thomas D ^e   Olvera, Rene L ^{a,b,c,d,e,f,g,h,i}   Kochunov, Peter ^f   Duggirala, Ravi ^e   Fox, Peter T ^g   Almasy, Laura ^e   Blangero, John ^e   Bellec, Pierre ^h   Evans, Alan C ^a   Glahn, David C ^b,c   more..

^a MCGILL UNIVERSITY   (Canada)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTE OF LIVING   (United States)

^d DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^e SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^f UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^h CENTRE DE RECHERCHE   (Canada)

ⁱ Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Clustering; Cortical Thickness; Genotype by Age Interaction; Heritability

Indexed keywords

ADULT; ADULTHOOD; AGE; AGED; ANGULAR GYRUS; ARTICLE; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); FEMALE; GENE INTERACTION; GENETIC CORRELATION; GENETIC VARIABILITY; GENOTYPE; HEREDITY; HERITABILITY; HUMAN; HUMAN EXPERIMENT; MALE; MIDDLE TEMPORAL GYRUS; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PLEIOTROPY; PRIORITY JOURNAL; SUPERIOR FRONTAL GYRUS; SUPERIOR TEMPORAL GYRUS; SUPRAMARGINAL GYRUS; ADOLESCENT; AGING; BRAIN CORTEX; FAMILY; GENETICS; HISPANIC; IMAGE PROCESSING; MIDDLE AGED; ORGAN SIZE; PATHOLOGY; PHENOTYPE; PROCEDURES; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGING; CEREBRAL CORTEX; FAMILY; FEMALE; GENETIC PLEIOTROPY; HISPANIC AMERICANS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; ORGAN SIZE; PHENOTYPE; YOUNG ADULT;

EID: 84899836578     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-014-9296-x     Document Type: Article

References (48)

1. Almasy, L, & Blangero, J (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. American Journal of Human Genetics, 62(5), 1198-1211. doi: 10. 1086/301844, PMID: 9545414.
2. Bassett, D. S., Bullmore, E., Verchinski, B. A., Mattay, V. S., Weinberger, D. R., Meyer-Lindenberg, A. (2008). Hierarchical organization of human cortical networks in health and schizophrenia. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28(37), 9239-9248. doi: 10. 1523/JNEUROSCI. 1929-08. 2008. http://www. ncbi. nlm. nih. gov/pmc/articles/PMC2878961/, PMID: 18784304 PMCID: PMC2878961.
3. Batagelj, V. (1988). Generalized Ward and related clustering problems. In H. H. Bock (Ed.), Classification and related methods of data analysis: Proceedings of the first conference of the International Federation of Classification Societies (IFCS). North-Holland: Technical University of Aachen, F. R. G. 29 June-1 July 1987. doi: 10. 1016/j. neuroimage. 2010. 02. 082, PMID: 20226257.
4. Bellec, P., Rosa-Neto, P., Lyttelton, O. C., Benali, H., Evans, A. C. (2010). Multi-level bootstrap analysis of stable clusters in resting-state fMRI. NeuroImage, 51(3), 1126-1139. PMID: 8300087.
5. Blangero, J. (1993). Statistical genetic approaches to human adaptability. Human Biology, 65(6), 941-966. doi: 10. 1038/nature01495, PMID: 12712196.
6. Carroll, S. B. (2003). Genetics and the making of homo sapiens. Nature, 422(6934), 849-857. doi: 10. 1126/science. 1215330, PMID: 22461613.
7. Chen, C. H., Fiecas, M., Gutirrez, E. D., Panizzon, M. S., Eyler, L. T., Vuoksimaa, E., Thompson, W. K., Fennema-Notestine, C., Hagler, J., Donald, J., Jernigan, T. L., Neale, M. C., Franz, C. E., Lyons, M. J., Fischl, B., Tsuang, M. T., Dale, A. M., Kremen, W. S. (2013). Genetic topography of brain morphology. Proceedings of the National Academy of Sciences of the United States of America, 110(42), 17, 089-17, 094. doi: 10. 1093/cercor/bhn003. http://cercor. oxfordjournals. org/content/18/10/2374, PMID: 18267952.
8. Chen, C. H., Gutierrez, E. D., Thompson, W., Panizzon, M. S., Jernigan, T. L., Eyler, L. T., Fennema-Notestine, C., Jak, A. J., Neale, M. C., Franz, C. E., Lyons, M. J., Grant, M. D., Fischl, B., Seidman, L. J., Tsuang, M. T., Kremen, W. S., Dale, A. M. (2012). Hierarchical genetic organization of human cortical surface area. Science (New York, NY), 335(6076), 1634-1636. doi: 10. 1073/pnas. 1308091110, PMID: 24082094.
9. Chen, Z. J., He, Y., Rosa-Neto, P., Germann, J., Evans, A. C. (2008). Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cerebral Cortex, 18(10), 2374-2381. PMID: 8126267.
10. Collins, D. L., Neelin, P., Peters, T. M., Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized talairach space. Journal of Computer Assisted Tomography, 18(2), 192-205. doi: 10. 1017/thg. 2012. 3, PMID: 22856366.
11. Eyler, L. T., Chen, C. H., Panizzon, M. S., Fennema-Notestine, C., Neale, M. C., Jak, A., Jernigan, T. L., Fischl, B., Franz, C. E., Lyons, M. J., Grant, M., Prom-Wormley, E., Seidman, L. J., Tsuang, M. T., Fiecas, M. J. A., Dale, A. M., Kremen, W. S. (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: The Official Journal of the International Society for Twin Studies, 15(3), 304-314. doi: 10. 1017/thg. 2012. 3, PMID: 22856366.
12. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics, 4th edtion. Benjamin Cummings.
13. Fisher, S. E., & Marcus, G. F. (2006). The eloquent ape: genes, brains and the evolution of language. Nature Reviews Genetics, 7(1), 9-20. doi: 10. 1038/nrg1747, PMID: 16369568.
14. Fred, A., & Jain, A. (2005). Combining multiple clusterings using evidence accumulation. IEEE Transactions on Pattern Analysis and Machine Intelligence, 27(6), 835-850. doi: 10. 1109/TPAMI. 2005. 113.
15. Frisoni, G. B., Redolfi, A., Manset, D., Rousseau, M., Toga, A., Evans, A. C. (2011). Virtual imaging laboratories for marker discovery in neurodegenerative diseases. Nature Reviews Neurology, 7(8), 429-438. doi: 10. 1038/nrneurol. 2011. 99, PMID: 21727938.
16. Glahn, D. C., Kent, J., Jack, W., Sprooten, E., Diego, V. P., Winkler, A. M., Curran, J. E., McKay, D. R., Knowles, E. E., Carless, M. A., Gring, H. H. H., Dyer, T. D., Olvera, R. L., Fox, P. T., Almasy, L., Charlesworth, J., Kochunov, P., Duggirala, R., Blangero, J. (2013). Genetic basis of neurocognitive decline and reduced white-matter integrity in normal human brain aging. Proceedings of the National Academy of Sciences of the United States of America. doi: 10. 1073/pnas. 1313735110, PMID: 24191011.
17. He, Y., Chen, Z. J., Evans, A. C. (2007). Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cerebral cortex (New York, NY: 1991), 17(10), 2407-2419. doi: 10. 1093/cercor/bhl149, PMID: 17204824.
18. Hulshoff Pol, H. E., Schnack, H. G., Posthuma, D., Mandl, R. C. W., Baar, W. F., van Oel, C., van Haren, N. E., Collins, D. L., Evans, A. C., Amunts, K., Brgel, U., Zilles, K., de Geus, E., Boomsma, D. I., Kahn, R. S. (2006). Genetic contributions to human brain morphology and intelligence. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(40), 10, 235-10, 242. doi: 10. 1523/JNEUROSCI. 1312-06. 2006, PMID: 17021179.
19. Im, K., Lee, J. M., Lyttelton, O., Kim, S. H., Evans, A. C., Kim, S. I. (2008). Brain size and cortical structure in the adult human brain. Cerebral Cortex (New York, NY: 1991), 18(9), 2181-2191. doi: 10. 1093/cercor/bhm244, PMID: 18234686.
20. Joshi, A. A., Lepor, N., Joshi, S. H., Lee, A. D., Barysheva, M., Stein, J. L., McMahon, K. L., Johnson, K., de Zubicaray, G. I., Martin, N. G., Wright, M. J., Toga, A. W., Thompson, P. M. (2011). The contribution of genes to cortical thickness and volume. Neuroreport, 22(3), 101-105. doi: 10. 1097/WNR. 0b013e3283424c84, PMID: 21233781.
21. Kelly, C., Toro, R., Di Martino, A., Cox, C. L., Bellec, P., Castellanos, F. X., Milham, M. P. (2012). A convergent functional architecture of the insula emerges across imaging modalities. NeuroImage, 61(4), 1129-1142. doi: 10. 1016/j. neuroimage. 2012. 03. 021, PMID: 22440648.
22. Kim, J. S., Singh, V., Lee, J. K., Lerch, J., Ad-Dab'bagh, Y., MacDonald, D., Lee, J. M., Kim, S. I., Evans, A. C. (2005). Automated 3-d extraction and evaluation of the inner and outer cortical surfaces using a laplacian map and partial volume effect classification. NeuroImage, 27(1), 210-221. doi: 10. 1016/j. neuroimage. 2005. 03. 036 PMID: 15896981.
23. Kochunov, P., Lancaster, J. L., Glahn, D. C., Purdy, D., Laird, A. R., Gao, F., Fox, P. (2006). Retrospective motion correction protocol for high-resolution anatomical MRI. Human Brain Mapping, 27(12), 957-962. doi: 10. 1002/hbm. 20235, PMID: 16628607.
24. Kremen, W. S., Prom-Wormley, E., Panizzon, M. S., Eyler, L. T., Fischl, B., Neale, M. C., Franz, C. E., Lyons, M. J., Pacheco, J., Perry, M. E., Stevens, A., Schmitt, J. E., Grant, M. D., Seidman, L. J., Thermenos, H. W., Tsuang, M. T., Eisen, S. A., Dale, A. M., Fennema-Notestine, C. (2010). Genetic and environmental influences on the size of specific brain regions in midlife: the VETSA MRI study. NeuroImage, 49(2), 1213-1223. doi: 10. 1016/j. neuroimage. 2009. 09. 043, PMID: 19786105.
25. Lenroot, R. K., Schmitt, J. E., Ordaz, S. J., Wallace, G. L., Neale, M. C., Lerch, J. P., Kendler, K. S., Evans, A. C., Giedd, J. N. (2009). Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence. Human Brain Mapping, 30(1), 163-174. doi: 10. 1002/hbm. 20494, PMID: 18041741.
26. Lu, T., Pan, Y., Kao, S. Y., Li, C., Kohane, I., Chan, J., Yankner, B. A. (2004). Gene regulation and DNA damage in the ageing human brain. Nature, 429(6994), 883-891. doi: 10. 1038/nature02661, PMID: 15190254.
27. Lyttelton, O., Boucher, M., Robbins, S., Evans, A. (2007). An unbiased iterative group registration template for cortical surface analysis. NeuroImage, 34(4), 1535-1544. doi: 10. 1016/j. neuroimage. 2006. 10. 041 PMID: 17188895.
28. MacDonald, D., Kabani, N., Avis, D., Evans, A. C. (2000). Automated 3-d extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage, 12(3), 340-356. doi: 10. 1006/nimg. 1999. 0534, PMID: 10944416.
29. Olvera, R. L., Bearden, C. E., Velligan, D. I., Almasy, L., Carless, M. A., Curran, J. E., Williamson, D. E., Duggirala, R., Blangero, J., Glahn, D. C. (2011). Common genetic influences on depression, alcohol, and substance use disorders in mexican-american families. American journal of medical genetics Part B. Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 156B(5), 561-568. doi: 10. 1002/ajmg. b. 31196, PMID: 21557468.
30. Panizzon, M. S., Fennema-Notestine, C., Eyler, L. T., Jernigan, T. L., Prom-Wormley, E., Neale, M., Jacobson, K., Lyons, M. J., Grant, M. D., Franz, C. E., Xian, H., Tsuang, M., Fischl, B., Seidman, L., Dale, A., Kremen, W. S. (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex (New York, NY: 1991), 19(11), 2728-2735. doi: 10. 1093/cercor/bhp026, PMID: 19299253.
31. Parker, G. J. M., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A. M., Ciccarelli, O., Lambon Ralph, M. A. (2005). Lateralization of ventral and dorsal auditory-language pathways in the human brain. NeuroImage, 24(3), 656-666. doi: 10. 1016/j. neuroimage. 2004. 08. 047 PMID: 15652301.
32. Pennington, B. F., Filipek, P. A., Lefly, D., Chhabildas, N., Kennedy, D. N., Simon, J. H., Filley, C. M., Galaburda, A., DeFries, J. C. (2000). A twin MRI study of size variations in human brain. Journal of Cognitive Neuroscience, 12(1), 223-232. PMID: 10769318.
33. Pfefferbaum, A., Sullivan, E. V., Swan, G. E., Carmelli, D. (2000). Brain structure in men remains highly heritable in the seventh and eighth decades of life. Neurobiology of Aging, 21(1), 63-74. PMID: 10794850.
34. Rimol, L. M., Panizzon, M. S., Fennema-Notestine, C., Eyler, L. T., Fischl, B., Franz, C. E., Hagler, D. J., Lyons, M. J., Neale, M. C., Pacheco, J., Perry, M. E., Schmitt, J. E., Grant, M. D., Seidman, L. J., Thermenos, H. W., Tsuang, M. T., Eisen, S. A., Kremen, W. S., Dale, A. M. (2010). Cortical thickness is influenced by regionally specific genetic factors. Biological Psychiatry, 67(5), 493-499. doi: 10. 1016/j. biopsych. 2009. 09. 032, PMID: 19963208.
35. Rousseeuw, P. J. (1987). Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics, 20, 53-65. doi: 10. 1016/0377-0427(87)90125-7. http://www. sciencedirect. com/science/article/pii/0377042787901257.
36. Schmitt, J. E., Wallace, G. L., Lenroot, R. K., Ordaz, S. E., Greenstein, D., Clasen, L., Kendler, K. S., Neale, M. C., Giedd, J. N. (2010). A twin study of intracerebral volumetric relationships. Behavior Genetics, 40(2), 114-124. doi: 10. 1007/s10519-010-9332-6, PMID: 20112130.
37. Sled, J. G., Zijdenbos, A. P., Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging, 17(1), 87-97. doi: 10. 1109/42. 668698, PMID: 9617910.
38. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143-155. doi: 10. 1002/hbm. 10062, PMID: 12391568.
39. Somel, M., Khaitovich, P., Bahn, S., Pbo, S., Lachmann, M. (2006). Gene expression becomes heterogeneous with age. Current Biology, 16(10), R359-R360. doi: 10. 1016/j. cub. 2006. 04. 024. http://www. sciencedirect. com/science/article/pii/S0960982206014850.
40. Somel, M., Guo, S., Fu, N., Yan, Z., Hu, H. Y., Xu, Y., Yuan, Y., Ning, Z., Hu, Y., Menzel, C., Hu, H., Lachmann, M., Zeng, R., Chen, W., Khaitovich, P. (2010). MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Research, 20(9), 1207-1218. doi: 10. 1101/gr. 106849. 110, PMID: 20647238.
41. Sterner, K. N., Weckle, A., Chugani, H. T., Tarca, A. L., Sherwood, C. C., Hof, P. R., Kuzawa, C. W., Boddy, A. M., Abbas, A., Raaum, R. L., Grgoire, L., Lipovich, L., Grossman, L. I., Uddin, M., Goodman, M., Wildman, D. E. (2012). Dynamic gene expression in the human cerebral cortexdistinguishes children from adults. PloS one, 7(5), e37, 714. doi: 10. 1371/journal. pone. 0037714, PMID: 22666384.
42. Thompson, P. M., Cannon, T. D., Narr, K. L., van Erp, T., Poutanen, V. P., Huttunen, M., Lnnqvist, J., Standertskjld-Nordenstam, C. G., Kaprio, J., Khaledy, M., Dail, R., Zoumalan, C. I., Toga, A. W. (2001). Genetic influences on brain structure. Nature Neuroscience, 4(12), 1253-1258. doi: 10. 1038/nn758, PMID: 11694885.
43. Tohka, J., Zijdenbos, A., Evans, A. (2004). Fast and robust parameter estimation for statistical partial volume models in brain MRI. NeuroImage, 23(1), 84-97. doi: 10. 1016/j. neuroimage. 2004. 05. 007, PMID: 15325355.
44. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273-289. doi: 10. 1006/nimg. 2001. 0978, PMID: 11771995.
45. Winkler, A. M., Kochunov, P., Blangero, J., Almasy, L., Zilles, K., Fox, P. T., Duggirala, R., Glahn, D. C. (2010). Cortical thickness or grey matter volume? the importance of selecting the phenotype for imaging genetics studies. NeuroImage, 53(3), 1135-1146. doi: 10. 1016/j. neuroimage. 2009. 12. 028, PMID: 20006715.
46. Wright, I. C., Sham, P., Murray, R. M., Weinberger, D. R., Bullmore, E. T. (2002). Genetic contributions to regional variability in human brain structure: methods and preliminary results. NeuroImage, 17(1), 256-271. PMID: 12482082.
47. Yoon, U., Fahim, C., Perusse, D., Evans, A. C. (2010). Lateralized genetic and environmental influences on human brain morphology of 8-year-old twins. NeuroImage, 53(3), 1117-1125. doi: 10. 1016/j. neuroimage. 2010. 01. 007, PMID: 20074649.
48. Yoon, U., Perusse, D., Evans, A. C. (2012). Mapping genetic and environmental influences on cortical surface area of pediatric twins. Neuroscience, 220, 169-178. doi: 10. 1016/j. neuroscience. 2012. 06. 030 PMID: 22728098.