Quantitative tract-based white matter heritability in twin neonates

NeuroImage

Volumn 111, Issue , 2015, Pages 123-135

  Lee, Seung Jae ^a,b   Steiner, Rachel J ^a   Luo, Shikai ^c   Neale, Michael C ^d   Styner, Martin ^a,e   Zhu, Hongtu ^f,g   Gilmore, John H ^a,g  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Kyungpook National University School of Medicine   (South Korea)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^e University of North Carolina   (United States)

^f University of North Carolina at Chapel Hill   (United States)

^g UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Axial diffusivity; Diffusion tensor imaging (DTI); Fractional anisotropy; Genetics; Quantitative tractography; Radial diffusivity

Indexed keywords

ARCUATE FASCICULUS; ARTICLE; AXIAL DIFFUSION; BRAIN FORNIX; BRAIN MATURATION; CINGULATE GYRUS; CONTROLLED STUDY; CORPUS CALLOSUM; CORTICOFUGAL TRACT; CORTICOTHALAMIC TRACT; DIFFUSION TENSOR IMAGING; DIZYGOTIC TWINS; ENVIRONMENTAL FACTOR; FEMALE; FRACTIONAL ANISOTROPY; GENETIC ANALYSIS; GENETIC VARIABILITY; HERITABILITY; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; MALE; MEDIAL LEMNISCAL PATHWAY; MONOZYGOTIC TWINS; NERVE TRACT; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; NEWBORN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIAL DIFFUSION; RADIOLOGICAL PARAMETERS; SIGNAL NOISE RATIO; SUPERIOR LONGITUDINAL FASCICULUS; TWINS; WHITE MATTER; WHITE MATTER MATURATION; WHITE MATTER MICROSTRUCTURE; WHITE MATTER TRACT; ANATOMY AND HISTOLOGY; BRAIN; GENOTYPE ENVIRONMENT INTERACTION; INHERITANCE; PROCEDURES;

BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; GENE-ENVIRONMENT INTERACTION; HUMANS; INFANT, NEWBORN; INHERITANCE PATTERNS; MALE; WHITE MATTER;

EID: 84923329766     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.02.021     Document Type: Article

References (54)

1. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., Nemeroff C.B., Reyes T.M., Simerly R.B., Susser E.S., Nestler E.J. Early life programming and neurodevelopmental disorders. Biol. Psychiatry 2010, 68:314-319.
2. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
3. Berman J.I., Glass H.C., Miller S.P., Mukherjee P., Ferriero D.M., Barkovich A.J., Vigneron D.B., Henry R.G. Quantitative fiber tracking analysis of the optic radiation correlated with visual performance in premature newborns. Am. J. Neuroradiol. 2009, 30:120-124.
4. Blokland G.A., de Zubicaray G.I., McMahon K.L., Wright M.J. Genetic and environmental influences on neuroimaging phenotypes: a meta-analytical perspective on twin imaging studies. Twin Res. Hum. Genet. 2012, 15:351-371.
5. Brouwer R.M., Mandl R.C., Peper J.S., van Baal G.C., Kahn R.S., Boomsma D.I., Hulshoff Pol H.E. Heritability of DTI and MTR in nine-year-old children. NeuroImage 2010, 53:1085-1092.
6. Brouwer R.M., Mandl R.C., Schnack H.G., van Soelen I.L., van Baal G.C., Peper J.S., Kahn R.S., Boomsma D.I., Hulshoff Pol H.E. White matter development in early puberty: a longitudinal volumetric and diffusion tensor imaging twin study. PLoS ONE 2012, 7:e32316.
7. Chiang M.C., Avedissian C., Barysheva M., Toga A.W., McMahon K.L., de Zubicaray G.I., Wright M.J., Thompson P.M. Extending genetic linkage analysis to diffusion tensor images to map single gene effects on brain fiber architecture. Med. Image Comput. Comput. Assist. Interv. 12 2009, 506-513.
8. Chiang M.C., Barysheva M., Toga A.W., Medland S.E., Hansell N.K., James M.R., McMahon K.L., de Zubicaray G.I., Martin N.G., Wright M.J., Thompson P.M. BDNF gene effects on brain circuitry replicated in 455 twins. NeuroImage 2011, 55:448-454.
9. Chiang M.C., McMahon K.L., de Zubicaray G.I., Martin N.G., Hickie I., Toga A.W., Wright M.J., Thompson P.M. Genetics of white matter development: a DTI study of 705 twins and their siblings aged 12 to 29. NeuroImage 2011, 54:2308-2317.
10. Dennis E.L., Thompson P.M. Typical and atypical brain development: a review of neuroimaging studies. Dialogues Clin. Neurosci. 2013, 15:359-384.
11. Dubois J., Hertz-Pannier L., Dehaene-Lambertz G., Cointepas Y., Le Bihan D. Assessment of the early organization and maturation of infants' cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. NeuroImage 2006, 30:1121-1132.
12. Dubois J., Dehaene-Lambertz G., Perrin M., Mangin J.F., Cointepas Y., Duchesnay E., Le Bihan D., Hertz-Pannier L. Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum. Brain Mapp. 2008, 29:14-27.
13. Dubois J., Dehaene-Lambertz G., Kulikova S., Poupon C., Hüppi P.S., Hertz-Pannier L. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 2014, 12:48-71.
14. 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., Dale A.M., Kremen W.S. 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 Res. Hum. Genet. 2012, 15:304-314.
15. Eyler L.T., Vuoksimaa E., Panizzon M.S., Fennema-Notestine C., Neale M.C., Chen C.-H., Jak A., Franz C.E., Lyons M.J., Thompson W.K., Spoon K.M., Fischl B., Dale A.M., Kremen W.S. Conceptual and data-based investigation of genetic influences and brain asymmetry: a twin study of multiple structural phenotypes. J. Cogn. Neurosci. 2014, 26:1100-1117.
16. Fedorov A., Beichel R., Kalpathy-Cramer J., Finet J., Fillion-Robin J.-C., Pujol S., Bauer C., Jennings D., Fennessy F., Sonka M., Buatti J., Aylward S.R., Miller J.V., Pieper S., Kikinis R. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn. Reson. Imaging 2012, 30:1323-1341.
17. Gao W., Lin W., Chen Y., Gerig G., Smith J.K., Jewells V., Gilmore J.H. Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. Am. J. Neuroradiol. 2009, 30:290-296.
18. Gao W., Zhu H., Giovanello K.S., Smith J.K., Shen D., Gilmore J.H., Lin W. Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6790-6795.
19. Gao W., Gilmore J.H., Giovanello K.S., Smith J.K., Shen D., Zhu H., Lin W. Temporal and spatial evolution of brain network topology during the first two years of life. PLoS ONE 2011, 6:e25278.
20. Gao W., Gilmore J.H., Shen D., Smith J.K., Zhu H., Lin W. The synchronization within and interaction between the default and dorsal attention networks in early infancy. Cereb. Cortex 2013, 23:594-603.
21. Geng X., Gouttard S., Sharma A., Gu H., Styner M., Lin W., Gerig G., Gilmore J.H. Quantitative tract-based white matter development from birth to age 2years. NeuroImage 2012, 61:542-557.
22. Geng X., Prom-Wormley E.C., Perez J., Kubarych T., Styner M., Lin W., Neale M.C., Gilmore J.H. White matter heritability using diffusion tensor imaging in neonatal brains. Twin Res. Hum. Genet. 2012, 15:336-350.
23. Gilmore J.H., Lin W., Corouge I., Vetsa Y.S., Smith J.K., Kang C., Gu H., Hamer R.M., Lieberman J.A., Gerig G. Early postnatal development of corpus callosum and corticospinal white matter assessed with quantitative tractography. Am. J. Neuroradiol. 2007, 28:1789-1795.
24. Gilmore J.H., Schmitt J.E., Knickmeyer R.C., Smith J.K., Lin W., Styner M., Gerig G., Neale M.C. Genetic and environmental contributions to neonatal brain structure: a twin study. Hum. Brain Mapp. 2010, 31:1174-1182.
25. Glahn D.C., Curran J.E., Winkler A.M., Carless M.A., Kent J.W., Charlesworth J.C., Johnson M.P., Goring H.H., Cole S.A., Dyer T.D., Moses E.K., Olvera R.L., Kochunov P., Duggirala R., Fox P.T., Almasy L., Blangero J. High dimensional endophenotype ranking in the search for major depression risk genes. Biol. Psychiatry 2012, 71:6-14.
26. Goodlett C.B., Fletcher P.T., Gilmore J.H., Gerig G. Group analysis of DTI fiber tract statistics with application to neurodevelopment. NeuroImage 2009, 45:S133-S142.
27. Huang H., Zhang J., Wakana S., Zhang W., Ren T., Richards L.J., Yarowsky P., Donohue P., Graham E., van Zijl P.C., Mori S. White and gray matter development in human fetal, newborn and pediatric brains. NeuroImage 2006, 33:27-38.
28. Insel T.R. Rethinking schizophrenia. Nature 2010, 468:187-193.
29. Jones D.K., Christiansen K.F., Chapman R.J., Aggleton J.P. Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: implications for neuropsychological investigations. Neuropsychologia 2013, 51:67-78.
30. Kinney H.C., Brody B.A., Kloman A.S., Gilles F.H. Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J. Neuropathol. Exp. Neurol. 1988, 47:217-234.
31. Knickmeyer R.C., Kang C., Woolson S., Smith J.K., Hamer R.M., Lin W., Gerig G., Styner M., Gilmore J.H. Twin-singleton differences in neonatal brain structure. Twin Res. Hum. Genet. 2011, 14:268-276.
32. Kochunov P., Glahn D.C., Lancaster J.L., Winkler A.M., Smith S., Thompson P.M., Almasy L., Duggirala R., Fox P.T., Blangero J. Genetics of microstructure of cerebral white matter using diffusion tensor imaging. NeuroImage 2010, 53:1109-1116.
33. Kochunov P., Jahanshad N., Sprooten E., Nichols T.E., Mandl R.C., Almasy L., Booth T., Brouwer R.M., Curran J.E., de Zubicaray G.I., Dimitrova R., Duggirala R., Fox P.T., Elliot Hong L., Landman B.A., Lemaitre H., Lopez L.M., Martin N.G., McMahon K.L., Mitchell B.D., Olvera R.L., Peterson C.P., Starr J.M., Sussmann J.E., Toga A.W., Wardlaw J.M., Wright M.J., Wright S.N., Bastin M.E., McIntosh A.M., Boomsma D.I., Kahn R.S., den Braber A., de Geus E.J., Deary I.J., Hulshoff Pol H.E., Williamson D.E., Blangero J., van 't Ent D., Thompson P.M., Glahn D.C. Multi-site study of additive genetic effects on fractional anisotropy of cerebral white matter: comparing meta and megaanalytical approaches for data pooling. NeuroImage 2014, 95:136-150.
34. Kuswanto C.N., Teh I., Lee T.S., Sim K. Diffusion tensor imaging findings of white matter changes in first episode schizophrenia: a systematic review. Clin. Psychopharmacol. Neurosci. 2012, 10:13-24.
35. Lin W., Zhu Q., Gao W., Chen Y., Toh C.H., Styner M., Gerig G., Smith J.K., Biswal B., Gilmore J.H. Functional connectivity MR imaging reveals cortical functional connectivity in the developing brain. Am. J. Neuroradiol. 2008, 29:1883-1889.
36. Looney C.B., Smith J.K., Merck L.H., Wolfe H.M., Chescheir N.C., Hamer R.M., Gilmore J.H. Intracranial hemorrhage in asymptomatic neonates: prevalence on MR images and relationship to obstetric and neonatal risk factors. Radiology 2007, 242:535-541.
37. Lyall A.E., Shi F., Geng X., Woolson S., Li G., Wang L., Hamer R.M., Shen D., Gilmore J.H. Dynamic development of regional cortical thickness and surface area in early childhood. Cereb. Cortex 2014, 10.1093/cercor/bhu027.
38. Medland S.E., Jahanshad N., Neale B.M., Thompson P.M. Whole-genome analyses of whole-brain data: working within an expanded search space. Nat. Neurosci. 2014, 17:791-800.
39. Mueller S., Keeser D., Reiser M.F., Teipel S., Meindl T. Functional and structural MR imaging in neuropsychiatric disorders, Part 1: imaging techniques and their application in mild cognitive impairment and Alzheimer disease. Am. J. Neuroradiol. 2012, 33:1845-1850.
40. Neale M.C., Cardon L.R. Methodology for Genetic Studies of Twins and Families, NATO ASI Series 1992, Kluwer Academic Press, Dordrecht, The Netherlands.
41. NIMH Workgroup Transformative Neurodevelopmental Research in Mental Illness http://www.nimh.nih.gov/about/advisory-boards-and-groups/namhc/neurodevelopment_workgroup_report.pdf.
42. Nortje G., Stein D.J., Radua J., Mataix-Cols D., Horn N. Systematic review and voxel-based meta-analysis of diffusion tensor imaging studies in bipolar disorder. J. Affect. Disord. 2013, 150:192-200.
43. Oguz I., Farzinfar M., Matsui J., Budin F., Liu Z., Gerig G., Johnson H.J., Styner M. DTIPrep: quality control of diffusion-weighted images. Front. Neuroinform. 2014, 30:4.
44. Pfefferbaum A., Sullivan E.V., Carmelli D. Genetic regulation of regional microstructure of the corpus callosum in late life. Neuroreport 2001, 12:1677-1681.
45. Schmahmann J.D., Pandya D.N. Fiber Pathways of the Brain 2006, Oxford University Press, New York.
46. Smith S.M. Fast and robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
47. Song J.W., Mitchell P.D., Kolasinski J., Ellen Grant P., Galaburda A.M., Takahashi E. Asymmetry of white matter pathways in developing human brains. Cereb. Cortex 2014, 10.1093/cercor/bhu084.
48. Verde A.R., Budin F., Berger J.B., Gupta A., Farzinfar M., Kaiser A., Ahn M., Johnson H., Matsui J., Hazlett H.C., Sharma A., Goodlett C., Shi Y., Gouttard S., Vachet C., Piven J., Zhu H., Gerig G., Styner M. UNC-Utah NA-MIC framework for DTI fiber tract analysis. Front. Neuroinform. 2014, 7:51.
49. Voineskos A.N. Genetic underpinnings of white matter 'connectivity': heritability, risk, and heterogeneity in schizophrenia. Schizophr. Res. 2014, 10.1016/j.schres.2014.03.034.
50. Voineskos A.N., Felsky D., Kovacevic N., Tiwari A.K., Zai C., Chakravarty M.M., Lobaugh N.J., Shenton M.E., Rajji T.K., Miranda D., Pollock B.G., Mulsant B.H., McIntosh A.R., Kennedy J.L. Oligodendrocyte genes, white matter tract integrity, and cognition in schizophrenia. Cereb. Cortex 2013, 23:2044-2057.
51. Welker K.M., Patton A. Assessment of normal myelination with magnetic resonance imaging. Semin. Neurol. 2012, 32:15-28.
52. Yuan Y., Gilmore J.H., Geng X.J., Styner M., Chen K.H., Wang J.L., Zhu H.T. FMEM: functional mixed effects modeling for the analysis of longitudinal white matter Tract data. NeuroImage 2014, 84:753-764.
53. Zhu H.T., Kong L., Li R., Styner M., Gerig G., Lin W., Gilmore J.H. FADTTS: functional analysis of diffusion tensor tract statistics. NeuroImage 2011, 56:1412-1425.
54. Zuliani R., Moorhead T.W., Bastin M.E., Johnstone E.C., Lawrie S.M., Brambilla P., O'Donovan M.C., Owen M.J., Hall J., McIntosh A.M. Genetic variants in the ErbB4 gene are associated with white matter integrity. Psychiatry Res. 2011, 191:133-137.