Genetic analysis of cortical thickness and fractional anisotropy of water diffusion in the brain.

[en] OBJECTIVES: The thickness of the brain's cortical gray matter (GM) and the fractional anisotropy (FA) of the cerebral white matter (WM) each follow an inverted U-shape trajectory with age. The two measures are positively correlated and may be modulated by common biological mechanisms. We employed four types of genetic analyses to localize individual genes acting pleiotropically upon these phenotypes. METHODS: Whole-brain and regional GM thickness and FA values were measured from high-resolution anatomical and diffusion tensor MR images collected from 712, Mexican American participants (438 females, age = 47.9 +/- 13.2 years) recruited from 73 (9.7 +/- 9.3 individuals/family) large families. The significance of the correlation between two traits was estimated using a bivariate genetic correlation analysis. Localization of chromosomal regions that jointly influenced both traits was performed using whole-genome quantitative trait loci (QTL) analysis. Gene localization was performed using SNP genotyping on Illumina 1M chip and correlation with leukocyte-based gene-expression analyses. The gene-expressions were measured using the Illumina BeadChip. These data were available for 371 subjects. RESULTS: Significant genetic correlation was observed among GM thickness and FA values. Significant logarithm of odds (LOD >/= 3.0) QTLs were localized within chromosome 15q22-23. More detailed localization reported no significant association (p < 5.10(-5)) for 1565 SNPs located within the QTLs. Post hoc analysis indicated that 40% of the potentially significant (p </= 10(-3)) SNPs were localized to the related orphan receptor alpha (RORA) and NARG2 genes. A potentially significant association was observed for the rs2456930 polymorphism reported as a significant GWAS finding in Alzheimer's disease neuroimaging initiative subjects. The expression levels for RORA and ADAM10 genes were significantly (p < 0.05) correlated with both FA and GM thickness. NARG2 expressions were significantly correlated with GM thickness (p < 0.05) but failed to show a significant correlation (p = 0.09) with FA. DISCUSSION: This study identified a novel, significant QTL at 15q22-23. SNP correlation with gene-expression analyses indicated that RORA, NARG2, and ADAM10 jointly influence GM thickness and WM-FA values.

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology
Neurosciences & behavior

Author, co-author :

Kochunov, Peter

Glahn, David C.

Nichols, Thomas E.

Winkler, Anderson ; Université de Liège - ULiège > Form. doc. sc. bioméd. & pharma.

Hong, Elliot L.

Holcomb, Henry H.

Stein, Jason L.

Thompson, Paul M.

Curran, Joanne E.

Carless, Melanie A.

More authors (6 more)

Language :

English

Title :

Genetic analysis of cortical thickness and fractional anisotropy of water diffusion in the brain.

Publication date :

2011

Journal title :

Frontiers in Neuroscience

ISSN :

1662-4548

eISSN :

1662-453X

Publisher :

Frontiers Media S.A., Switzerland

Volume :

Pages :

120

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 03 May 2017

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Abe, O., Aoki, S., Hayashi, N., Yamada, H., Kunimatsu, A., Mori, H., Yoshikawa, T., Okubo, T., and Ohtomo, K. (2002). Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol. Aging 23, 433-441.
Abecasis, G. R., Cherny, S. S., Cookson, W. O., and Cardon, L. R. (2002). Merlin - rapid analysis of dense genetic maps using sparse gene flow trees. Nat. Genet. 30, 97-101.
Aganj, I., Sapiro, G., Parikshak, N., Madsen, S. K., and Thompson, P. M. (2009). Measurement of cortical thickness from MRI by minimum line integrals on soft-classified tissue. Hum. Brain Mapp. 30,3188-3199.
Almasy, L., and Blangero, J. (1998). Multipoint quantitative-trait linkage analysis in general pedigrees. Am. J. Hum. Genet. 62, 1198-1211.
Almasy, L., Dyer, T. D., and Blangero, J. (1997). Bivariate quantitative trait linkage analysis: pleiotropy versus co-incident linkages. Genet. Epidemiol. 14, 953-958.
Amos, C., de Andrade, M., and Zhu, D. (2001). Comparison of multivariate tests for genetic linkage. Hum. Hered. 51, 133-144.
Amos, C. I., and Laing, A. E. (1993). A comparison of univariate and multivariate tests for genetic linkage. Genet. Epidemiol. 10, 671-676.
Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 15, 435-455.
Biffi, A., Anderson, C. D., Desikan, R. S., Sabuncu, M., Cortellini, L., Schmansky, N., Salat, D., and Rosand, J. (2010). Genetic variation and neuroimaging measures in Alzheimer disease. Arch. Neurol. 67, 677-685.
Blangero, J., Williams, J. T., and Almasy, L. (2003). Novel family-based approaches to genetic risk in thrombosis. J. Thromb. Haemost. 1, 1391-1397.
Boehnke, M. (1991). Allele frequency estimation from data on relatives. Am. J. Hum. Genet. 48, 22-25.
Boerwinkle, E., and Sing, C. F. (1986). Bias of the contribution of single-locus effects to the variance of a quantitative trait. Am. J. Hum. Genet. 39, 137-144.
Boukhtouche, F., Vodjdani, G., Jarvis, C. I., Bakouche, J., Staels, B., Mallet, J., Mariani, J., Lemaigre-Dubreuil, Y., and Brugg, B. (2006). Human retinoic acid receptor-related orphan receptor alpha1 over-expression protects neurones against oxidative stress-induced apoptosis. J. Neurochem. 96, 1778-1789.
Brouwer, R. M., Mandl, R. C., Peper, J. S., van Baal, G. C., Kahn, R. S., Boomsma, D. I., and Hulshoff Pol, H. E. (2010). Heritability of DTI and MTR in nine-year-old children. Neuroimage 53,1085-1092.
Burdick, J. T., Chen, W. M., Abecasis, G. R., and Cheung, V. G. (2006). In silico method for inferring genotypes in pedigrees. Nat. Genet. 38, 1002-1004.
Cachia, A., Mangin, J. F., Riviere, D., Papadopoulos-Orfanos, D., Kherif, E, Bloch, I., and Regis, J. (2003). A generic framework for the parcella-tion of the cortical surface into gyri using geodesic Voronoi diagrams. Med. Image Anal. 7,403-416.
Chiang, M. C., McMahon, K. L., de Zubicaray, G. I., Martin, N. G., Hickie, I., Toga, A. W., Wright, M. J., and Thompson, P. M. (2011). Genetics of white matter development: a DTI study of 705 twins and their siblings aged 12 to 29. Neuroimage 54, 2308-2317.
Dussault, I., Fawcett, D., Matthyssen, A., Bader, J. A., and Giguere, V. (1998). Orphan nuclear receptor ROR alpha-deficient mice display the cerebellar defects of staggerer. Mech. Dev. 70, 147-153.
Edenberg, H. J., Bierut, L. J., Boyce, P., Cao, M., Cawley, S., Chiles, R., Doheny, K. F., Hansen, M., Hinrichs, T., Jones, K., Kelleher, M., Kennedy, G. C., Liu, G., Marcus, G., McBride, C., Murray, S. S., Oliphant, A., Pettengill, J., Porjesz, B., Pugh, E. W., Rice, J. P., Rubano, T., Shannon, S., Steeke, R., Tischfield, J. A., Tsai, Y. Y., Zhang, C., and Begleiter, H. (2005). Description of the data from the collaborative study on the genetics of alcoholism (COGA) and single-nucleotide polymorphism genotyping for genetic analysis workshop 14. BMC Genet. 6(Suppl. 1) doi:10.1186/1471-2156-6-S1-S2
Edwards, T. L., Scott, W. K., Almonte, C., Burt, A., Powell, E. H., Beecham, G. W., Wang, L., Zuchner, S., Konidari, I., Wang, G., Singer, C., Nahab, F., Scott, B., Stajich, J. M., Pericak-Vance, M., Haines, J., Vance, J. M., and Martin, E. R. (2010). Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann. Hum. Genet. 74, 97-109.
Epis, R., Marcello, E., Gardoni, F., Vastagh, C., Malinverno, M., Bal-ducci, C., Colombo, A., Borroni, B., Vara, H., Dell'Agli, M., Cattabeni, F., Giustetto, M., Borsello, T., Forloni, G., Padovani, A., and Di Luca, M. (2010). Blocking ADAM10 synaptic trafficking generates a model of sporadic Alzheimer's disease. Brain 133, 3323-3335.
Escamilla, M., Hare, E., Dassori, A. M., Peralta, J. M., Ontiveros, A., Nicolini, H., Raventos, H., Medina, R., Men-doza, R., Jerez, A., Munoz, R., and Almasy, L. (2009). A schizophrenia gene locus on chromosome 17q21 in a new set of families of Mexican and central American ancestry: evidence from the NIMH Genetics of schizophrenia in latino populations study. Am. J. Psychiatry 166, 442-449.
Farnham, J. M., Camp, N. J., Neuhausen, S. L., Tsuruda, J., Parker, D., Mac-Donald, J., and Cannon-Albright, L. A. (2004). Confirmation of chromosome 7q11 locus for predisposition to intracranial aneurysm. Hum. Genet. 114,250-255.
Fischl, B., and Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U.S.A. 97, 11050-11055.
Gaitanis, J. N., and Walsh, C. A. (2004). Genetics of disorders of cortical development. Neuroimaging Clin. N. Am. 14, 219-229, viii.
Gao, W., Lin, W., Chen, Y., Gerig, G., Smith, J. K., Jewells, V., and Gilmore, J. H. (2009). Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am. J. Neuroradiol. 30, 290-296.
Garriock, H. A., Kraft, J. B., Shyn, S. I., Peters, E. J., Yokoyama, J. S., Jenkins, G. D., Reinalda, M. S., Slager, S. L., McGrath, P. J., and Hamilton, S. P. (2009). A genomewide association study of citalopram response in major depressive disorder. Biol Psychiatry 67, 133-138.
Glahn, D. C., Thompson, P. M., and Blangero, J. (2007). Neuroimaging endophenotypes: strategies for finding genes influencing brain structure and function. Hum. Brain Mapp. 28, 488-501.
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. E III, Herman, D. H., Clasen, L. S., Toga, A. W., Rapoport, J. L., and Thompson, P. M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 101, 8174-8179.
Goring, H. H., Curran, J. E., Johnson, M. P., Dyer, T. D., Charlesworth, J., Cole, S. A., Jowett, J. B., Abraham, L. J., Rainwater, D. L., Comuzzie, A. G., Mahaney, M. C., Almasy, L., MacCluer, J. W., Kissebah, A. H., Collier, G. R., Moses, E. K., and Blangero, J. (2007). Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nat. Genet. 39, 1208-1216.
Hamilton, B. A., Frankel, W. N., Ker-rebrock, A. W., Hawkins, T. L., FitzHugh, W., Kusumi, K., Russell, L. B., Mueller, K. L., van Berkel, V., Birren, B. W., Kruglyak, L., and Lander, E. S. (1996). Disruption of the nuclear hormone receptor RORal-pha in staggerer mice. Nature 379, 736-739.
Hu, V. W., Frank, B. C., Heine, S., Lee, N. H., and Quackenbush, J. (2006). Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics 7, 118. doi:10.1186/1471-2164-7-118
Hu, V. W., Sarachana, T., Kim, K. S., Nguyen, A., Kulkarni, S., Steinberg, M. E., Luu, T., Lai, Y., and Lee, N. H. (2009). Gene expression profiling differentiates autism case-controls and phenotypic variants of autism spectrum disorders: evidence for cir-cadian rhythm dysfunction in severe autism. Autism Res. 2, 78-97.
Huttenlocher, P. R., and Dabholkar, A. S. (1997). Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387, 167-178.
Jarvis, C. I., Goncalves, M. B., Clarke, E., Dogruel, M., Kalindjian, S. B., Thomas, S. A., Maden, M., and Corcoran, J. P. (2010). Retinoic acid receptor-alpha signalling antagonizes both intracellular and extracellular amyloid-beta production and prevents neuronal cell death caused by amyloid-beta. Eur. J. Neurosci. 32, 1246-1255.
Jarvis, C. I., Staels, B., Brugg, B., Lemaigre-Dubreuil, Y., Tedgui, A., and Mariani, J. (2002). Age-related phenotypes in the staggerer mouse expand the RORalpha nuclear receptor's role beyond the cerebellum. Mol. Cell. Endocrinol. 186, 1-5.
Jones, D. K., Horsfield, M. A., and Simmons, A. (1999). Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn. Reson. Med. 42, 515-525.
Jones, K. A., Porjesz, B., Almasy, L., Bierut, L., Goate, A., Wang, J. C., Dick, D. M., Hinrichs, A., Kwon, J., Rice, J. P., Rohrbaugh, J., Stock, H., Wu, W., Bauer, L. O., Chor-lian, D. B., Crowe, R. R., Edenberg, H. J., Foroud, T., Hessel-brock, V., Kuperman, S., Nurnberger, J. Jr., O'Connor, S. J., Schuckit, M. A., Stimus, A. T., Tischfield, J. A., Reich, T., and Begleiter, H. (2004). Linkage and linkage disequilibrium of evoked EEG oscillations with CHRM2 receptor gene polymorphisms: implications for human brain dynamics and cognition. Int. J. Psychophysiol. 53, 75-90.
Joshi, A. A., Lepore, 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., and Thompson, P. M. (2011). The contribution of genes to cortical thickness and volume. Neuroreport 22, 101-105.
Kamarajan, C., Porjesz, B., Jones, K., Chorlian, D., Padmanabhapillai, A., Rangaswamy, M., Stimus, A., and Begleiter, H. (2006). Event-related oscillations in offspring of alcoholics: neurocognitive disinhibition as a risk for alcoholism. Biol. Psychiatry 59, 625-634.
Kammerer, C. M., Schneider, J. L., Cole, S. A., Hixson, J. E., Samollow, P. B., O'Connell, J. R., Perez, R., Dyer, T. D., Almasy, L., Blangero, J., Bauer, R. L., and Mitchell, B. D. (2003). Quantitative trait loci on chromosomes 2p, 4p, and 13q influence bone mineral density of the forearm and hip in Mexican Americans. J. Bone Miner. Res. 18,2245-2252.
Kim, M., Suh, J., Romano, D., Truong, M. H., Mullin, K., Hooli, B., Norton, D., Tesco, G., Elliott, K., Wagner, S. L., Moir, R. D., Becker, K. D., and Tanzi, R. E. (2009). Potential late-onset Alzheimer's disease-associated mutations in the ADAM10 gene attenuate {alpha}-secretase activity. Hum. Mol. Genet. 18, 3987-3996.
Klein, R. J., Zeiss, C., Chew, E. Y., Tsai, J. Y., Sackler, R. S., Haynes, C., Hen-ning, A. K., SanGiovanni, J. P., Mane, S. M., Mayne, S. T., Bracken, M. B., Ferris, E L., Ott, J., Barnstable, C., and Hoh, J. (2005). Complement factor H polymorphism in age-related macular degeneration. Science 308, 385-389.
Kochunov, P., and Davis, M. (2009). Development of structural MR brain imaging protocols to study genetics and maturation. Methods 50, 136-146.
Kochunov, P., Glahn, D., Lancaster, J., Wincker, P., Smith, S., Thompson, P., Almasy, L., Duggirala, R., Fox, P., and Blangero, J. (2010a). Genetics of microstructure of cerebral white matter using diffusion tensor imaging. Neuroimage 15, 1109-1116.
Kochunov, P., Williamson, D., Lancaster, J., Fox, P., Cornell, J., Blangero, J., and Glahn, D. (2010b). Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiol. Aging. doi: 10.1016/j.neurobiolaging.2010.0 1.014. [Epub ahead of print].
Kochunov, P., Glahn, D. C., Lancaster, J., Thompson, P. M., Kochunov, V., Rogers, B., Fox, P., Blangero, J., and Williamson, D. E. (2011). Fractional anisotropy of cerebral white matter and thickness of cortical gray matter across the lifespan. Neuroimage 58, 41-49.
Kochunov, P., Lancaster, J. L., Glahn, D. C., Purdy, D., Laird, A. R., Gao, F., and Fox, P. (2006). Retrospective motion correction protocol for high-resolution anatomical MRI. Hum. Brain Mapp. 27, 957-962.
Kochunov, P., Lancaster, J. L., Thompson, P., Woods, R., Mazziotta, J., Hardies, J., and Fox, P. (2001). Regional spatial normalization: toward an optimal target. J. Comput. Assist. Tomogr. 25, 805-816.
Kochunov, P., Mangin, J. F., Coyle, T., Lancaster, J., Thompson, P., Riviére, D., Cointepas, Y., Régis, J., Schlosser, A., Royall, D. R., Zilles, K., Mazziotta, J., Toga, A., and Fox, P. T. (2005). Age-related morphology trends of cortical sulci. Hum. Brain Mapp. 26, 210-220.
Kochunov, P., Thompson, P. M., Coyle, T. R., Lancaster, J. L., Kochunov, V., Royall, D., Mangin, J. F., Riviere, D., and Fox, P. T. (2008). Relationship among neuroimaging indices of cerebral health during normal aging. Hum. Brain Mapp. 29, 36-45.
Kochunov, P., Thompson, P. M., Lancaster, J. L., Bartzokis, G., Smith, S., Coyle, T., Royall, D. R., Laird, A., and Fox, P. T. (2007). Relationship between white matter fractional anisotropy and other indices of cerebral health in normal aging: tract-based spatial statistics study of aging. Neuroimage 35,478-487.
Koivisto, P. A., Koivisto, H., Haapala, K., and Simola, K. O. (1999). A de novo deletion of chromosome 15(q15.2q21.2) in a dysmorphic, mentally retarded child with congenital scalp defect. Clin. Dysmor-phol. 8,139-141.
Lalani, S. R., Sahoo, T., Sanders, M. E., Peters, S. U., and Bejjani, B. A. (2006). Coarctation of the aorta and mild to moderate developmental delay in a child with a de novo deletion of chromosome 15(q21.1q22.2). BMCMed. Genet. 7, 8. doi:10.1186/1471-2350-7-8
Lavebratt, C., Sjoholm, L. K., Parto-nen, T., Schalling, M., and Forsell, Y. (2009). PER2 variantion is associated with depression vulnerability. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 570-581.
Le-Niculescu, H., Patel, S. D., Bhat, M., Kuczenski, R., Faraone, S. V., Tsuang, M. T., McMahon, E J., Schork, N. J., Nurnberger, J. I. Jr., Niculescu, A. B. III. (2009). Convergent functional genomics of genome-wide association data for bipolar disorder: comprehensive identification of candidate genes, pathways and mechanisms. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 155-181.
Lerch, J. P., and Evans, A. C. (2005). Cortical thickness analysis examined through power analysis and a population simulation. Neuroimage 24, 163-173.
Machado, I. N., Heinrich, J. K., and Barini, R. (2010). Genomic imbalances detected through array CGH in fetuses with holoprosencephaly. Arq. Neuropsiquiatr. 69, 3-8.
Madler, B., Drabycz, S. A., Kolind, S. H., Whittall, K. P., and MacKay, A. L. (2008). Is diffusion anisotropy an accurate monitor of myelina-tion? Correlation of multicompo-nent T2 relaxation and diffusion tensor anisotropy in human brain. Magn. Reson. Imaging 26, 874-888.
Mangin, J. F., Riviere, D., Cachia, A., Duchesnay, E., Cointepas, Y., Papadopoulos-Orfanos, D., Collins, D. L., Evans, A. C., and Regis, J. (2004). Object-based morphometry of the cerebral cortex. IEEE Trans. Med. Imaging 23, 968-982.
Marcello, E., Epis, R., Saraceno, C., Gardoni, F., Borroni, B., Cat-tabeni, F., Padovani, A., and Di Luca, M. (2010). SAP97-mediated local trafficking is altered in Alzheimer disease patients' hippocampus. Neurobiol.Aging. doi: 10.1016/j.neurobiolaging.2010.09.015.
McGrath, C. L., Glatt, S. J., Sklar, P., Le-Niculescu, H., Kuczenski, R., Doyle, A. E., Biederman, J., Mick, E., Faraone, S. V., Niculescu, A. B., and Tsuang, M. T. (2009). Evidence for genetic association of RORB with bipolar disorder. BMC Psychiatry 9, 70. doi:10.1186/1471-244X-9-70
Meyer-Lindenberg, A. (2010). Imaging genetics of schizophrenia. Dialogues Clin. Neurosci. 12,449-456.
Mitchell, B. D., Kammerer, C. M., Blangero, J., Mahaney, M. C., Rainwater, D. L., Dyke, B., Hixson, J. E., Henkel, R. D., Sharp, R. M., Comuzzie, A. G., VandeBerg, J. L., Stern, M. P., and MacCluer, J. W. (1996). Genetic and environmental contributions to cardiovascular risk factors in Mexican Americans. The San Antonio Family Heart Study. Circulation 94,2159-2170.
Moskvina, V., and Schmidt, K. M. (2008). On multiple-testing correction in genome-wide association studies. Genet. Epidemiol. 32, 567-573.
Neale, B. M., Lasky-Su, J., Anney, R., Franke, B., Zhou, K., Maller, J. B., Vasquez, A. A., Asherson, P., Chen, W., Banaschewski, T., Buitelaar, J., Ebstein, R., Gill, M., Miranda, A., Oades, R. D., Roeyers, H., Rothen-berger, A., Sergeant, J., Steinhausen, H. C., Sonuga-Barke, E., Mulas, E, Taylor, E., Laird, N., Lange, C., Daly, M., and Faraone, S. V. (2008). Genome-wide association scan of attention deficit hyperactivity disorder. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 1337-1344.
Nguyen, A., Rauch, T. A., Pfeifer, G. P., and Hu, V.W. (2010). Global methy-lation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA, whose protein product is reduced in autistic brain. FASEB J. 24,3036-3051.
Olvera, R. L., Bearden, C. E., Velligan, D. I., Almasy, L., Carless, M. A., Cur-ran, J. E., Williamson, D. E., Duggirala, R., Blangero, J., and Glahn, D. C. (2010). Common genetic influ ences on depression, alcohol, and substance use disorders in Mexican-American families. Am. J. Med. Genet. B Neuropsychiatr. Genet. 156, 561-568.
Salthouse, T. A. (2009). When does age-related cognitive decline begin? Neurobiol Aging 30, 507-514.
Sarachana, T., Xu, M., Wu, R. C., and Hu, V. W (2010). Sex hormones in autism: androgens and estrogens differentially and reciprocally Regulate RORA, a novel candidate gene for autism. PLoS ONE 6, e17116. doi:10.1371/journal.pone.0017116
Schaumberg, D. A., Chasman, D., Morrison, M. A., Adams, S. M., Guo, Q., Hunter, D. J., Hank-inson, S. E., and DeAngelis, M. M. (2010). Prospective study of common variants in the retinoic acid receptor-related orphan receptor alpha gene and risk of neo-vascular age-related macular degeneration. Arch. Ophthalmol. 128, 1462-1471.
Schmitz, S., Cherny, S. S., and Fulker, D W (1998). Increase in power through multivariate analyses. Behav. Genet. 28, 357-363.
Schones, D. E., and Zhao, K. (2008). Genome-wide approaches to studying chromatin modifications. Nat. Rev. Genet.9, 179-191.
Smith, M., Filipek, P. A., Wu, C., Bocian, M., Hakim, S., Modahl, C., and Spence, M. A. (2000). Analysis of a 1-megabase deletion in 15q22-q23 in an autistic patient: identification of candidate genes for autism and of homologous DNA segments in 15q22-q23 and 15q11-q13. Am. J. Med. Genet. 96, 765-770.
Smith, S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143-155.
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., Watkins, K. E., Ciccarelli, O., Cader, M. Z., Matthews, P. M., and Behrens, T. E. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505.
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flit-ney, D. E., Niazy, R. K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J. M., and Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl. 1), S208-S219.
Sobel, E., and Lange, K. (1996). Descent graphs in pedigree analysis: applications to haplotyping, location scores, and marker-sharing statistics. Am. J. Hum. Genet. 58, 1323-1337.
Song, S. K., Yoshino, J., Le, T. Q., Lin, S. J., Sun, S. W., Cross, A. H., and Armstrong, R. C. (2005). Demyeli-nation increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140.
Sowell, E. R., Peterson, B. S., Thompson, P. M., Welcome, S. E., Henkenius, A. L., and Toga, A. W (2003). Mapping cortical change across the human life span. Nat. Neurosci. 6, 309-315.
Stein, J. L., Hua, X., Lee, S., Ho, A. J., Leow, A. D., Toga, A. W., Saykin, A. J., Shen, L., Foroud, T., Pankratz, N., Huentelman, M. J., Craig, D. W., Gerber, J. D., Allen, A. N., Corne-veaux, J. J., Dechairo, B. M., Potkin, S. G., Weiner, M. W., and Thompson, P. (2010a). Voxelwise genome-wide association study (vGWAS). Neuroimage 53, 1160-1174.
Stein, J. L., Hua, X., Morra, J. H., Lee, S., Hibar, D. P., Ho, A. J., Leow, A. D., Toga, A. W., Sul, J. H., Kang, H. M., Eskin, E., Saykin, A. J., Shen, L., Foroud, T., Pankratz, N., Huentelman, M. J., Craig, D. W., Gerber, J. D., Allen, A. N., Corneveaux, J. J., Stephan, D. A., Webster, J., DeChairo, B. M., Potkin, S. G., Jack, C. R. Jr., Weiner, M. W., and Thompson, P. M. (2010b). Genome-wide analysis reveals novel genes influencing temporal lobe structure with relevance to neurodegeneration in Alzheimer's disease. Neuroimage 51, 542-554.
Sugiura, N., Dadashev, V., and Cor-riveau, R. A. (2004). NARG2 encodes a novel nuclear protein with (S/T)PXX motifs that is expressed during development. Eur. J. Biochem. 271, 4629-4637.
Sugiura, N., Patel, R. G., and Cor-riveau, R. A. (2001). N-methyl-D-aspartate receptors regulate a group of transiently expressed genes in the developing brain. J. Biol. Chem. 276, 14257-14263.
Terracciano, A., Tanaka, T., Sutin, A. R., Sanna, S., Deiana, B., Lai, S., Uda, M., Schlessinger, D., Abecasis, G. R., Ferrucci, L., Costa, P. T. Jr. (2010). Genome-wide association scan of trait depression. Biol Psychiatry 68, 811-817.
Thompson, P. M., Cannon, T. D., Narr, K. L., van Erp, T., Pouta-nen, V. P., Huttunen, M., Lonnqvist, J., Standertskjold-Nordenstam, C. G., Kaprio, J., Khaledy, M., Dail, R., Zoumalan, C. I., and Toga, A. W. (2001). Genetic influences on brain structure. Nat. Neurosci. 4, 1253-1258.
Wakana, S., Jiang, H., Nagae-Poetscher, L. M., van Zijl, P. C., and Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology 230, 77-87.
Walsh, C. A. (2000). Genetics of neu-ronal migration in the cerebral cortex. Ment. Retard Dev. Disabil. Res. Rev. 6, 34-40.
Wang, C. Y., Zheng, W., Wang, T., Xie, J. W., Wang, S. L., Zhao, B. L., Teng, W. P., and Wang, Z. Y. (2010). Huperzine A activates Wnt/beta-catenin signaling and enhances the nonamyloidogenic pathway in an Alzheimer transgenic mouse model. Neuropsychopharmacology 36, 1073-1089.
Winkler, A. M., Kochunov, P., Blangero, J., Almasy, L., Zilles, K., Fox, P. T., Duggirala, R., and Glahn, D. C. (2010). Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. Neuroimage 53, 1135-1146.
Zhang, S., Salemi, J., Hou, H., Zhu, Y., Mori, T., Giunta, B., Obregon, D., and Tan, J. (2010). Rapamycin promotes beta-amyloid production via ADAM-10 inhibition. Biochem. Biophys. Res. Commun. 398, 337-341.