Atlas-based analysis of neurodevelopment from infancy to adulthood using diffusion tensor imaging and applications for automated abnormality detection

NeuroImage

Volumn 52, Issue 2, 2010, Pages 415-428

  Faria, Andreia V ^a,b   Zhang, Jiangyang ^a   Oishi, Kenichi ^a   Li, Xin ^a   Jiang, Hangyi ^a,c   Akhter, Kazi ^a   Hermoye, Laurent ^d   Lee, Seung Koo ^e   Hoon, Alexander ^c   Stashinko, Elaine ^c   Miller, Michael I ^a   van Zijl, Peter C M ^a,c   Mori, Susumu ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c KENNEDY KRIEGER INSTITUTE   (United States)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^e Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ADULTHOOD; AGE; ARTICLE; BRAIN SIZE; CEREBRAL PALSY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DIFFUSION COEFFICIENT; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; INFANCY; MALE; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; WHITE MATTER; ANATOMY AND HISTOLOGY; ANISOTROPY; AUTOMATION; BOOK; BRAIN; COMPARATIVE STUDY; COMPUTER ASSISTED DIAGNOSIS; DIFFUSION; GROWTH, DEVELOPMENT AND AGING; MYELINATED NERVE; ORGAN SIZE; PATHOLOGY; PRESCHOOL CHILD; PROCEDURES; STATISTICAL MODEL; TIME; YOUNG ADULT;

ADOLESCENT; ADULT; ANISOTROPY; ATLASES AS TOPIC; AUTOMATION; BRAIN; CHILD; CHILD, PRESCHOOL; DIAGNOSIS, COMPUTER-ASSISTED; DIFFUSION; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MALE; NERVE FIBERS, MYELINATED; ORGAN SIZE; TIME FACTORS; YOUNG ADULT;

EID: 77953694885     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.04.238     Document Type: Article

References (91)

1. Alexander A.L., Lee J.E., Lazar M., Field A.S. Diffusion tensor imaging of the brain. NeuroTherapeutics 2007, 4(3):316-329.
2. Andersson J.L., Skare S. A model-based method for retrospective correction of geometric distortions in diffusion-weighted EPI. NeuroImage 2002, 16(1):177-199.
3. Armand J., Olivier E., Edgley S.A., Lemon R.N. Postnatal development of corticospinal projections from motor cortex to the cervical enlargement in the macaque monkey. J. Neurosci. 1997, 17(1):251-266.
4. Ballesteros M.C., Hansen P.E., Soila K. MR imaging of the developing human brain. Part 2. Postnatal development. Radiographics 1993, 13(3):611-622.
5. Baratti C., Barnett A.S., Pierpaoli C. Comparative MR imaging study of brain maturation in kittens with T1, T2, and the trace of the diffusion tensor. Radiology 1999, 210(1):133-142.
6. Barkovich A.J. Concepts of myelin and myelination in neuroradiology. Am. J. Neuroradiol. 2000, 21(6):1099-1109.
7. Barkovich A.J., Kjos B.O., Jackson D.E., Norman D. Normal maturation of the neonatal and infant brain: MR imaging at 1.5T. Radiology 1988, 166:173-180.
8. Barnea-Goraly N., Menon V., Eckert M., Tamm L., Bammer R., Karchemskiy A., Dant C.C., Reiss A.L. White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb. Cortex 2005, 15(12):1848-1854.
9. Barres B.A., Barde Y. Neuronal and glial cell biology. Curr. Opin. Neurobiol. 2000, 10(5):642-648.
10. Bartha A.I., Yap K.R., Miller S.P., Jeremy R.J., Nishimoto M., Vigneron D.B., Barkovich A.J., Ferriero D.M. The normal neonatal brain: MR imaging, diffusion tensor imaging, and 3D MR spectroscopy in healthy term neonates. Am. J. Neuroradiol. 2007, 28(6):1015-1021.
11. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. 1994, 103(3):247-254.
12. Ben Bashat D., Ben Sira L., Graif M., Pianka P., Hendler T., Cohen Y., Assaf Y. Normal white matter development from infancy to adulthood: comparing diffusion tensor and high b value diffusion weighted MR images. J. Magn. Reson. Imaging 2005, 21(5):503-511.
13. Benedict R.H., Bobholz J.H. Multiple sclerosis. Semin. Neurol. 2007, 27(1):78-85.
14. Bigler E.D., Kerr B., Victoroff J., Tate D.F., Breitner J.C. White matter lesions, quantitative magnetic resonance imaging, and dementia. Alzheimer Dis. Assoc. Disord. 2002, 16(3):161-170.
15. Bigler E.D., Neeley E.S., Miller M.J., Tate D.F., Rice S.A., Cleavinger H., Wolfson L., Tschanz J., Welsh-Bohmer K. Cerebral volume loss, cognitive deficit and neuropsychological performance: comparative measures of brain atrophy: I. Dementia. J. Int. Neuropsychol. Soc. 2004, 10(3):442-452.
16. Brody B.A., Kinney H.C., Kloman A.S., Gilles F.H. Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J. Neuropathol. Exper. Neurol. 1987, 46(3):283-301.
17. Cascio C.J., Gerig G., Piven J. Diffusion tensor imaging: application to the study of the developing brain. J. Am. Acad. Child Adolesc. Psychiatry 2007, 46(2):213-223.
18. Ceritoglu C., Oishi K., Li X., Chou M.C., Younes L., Albert M., Lyketsos C., van Zijl P.C., Miller M.I., Mori S. Multi-contrast large deformation diffeomorphic metric mapping for diffusion tensor imaging. NeuroImage 2009, 47(2):618-627.
19. Chan T.F., Vese L.A. Active contours without edges. IEEE Transactions on Image Processing: A Publication of the IEEE Signal Processing Society 2001, 10(2):266-277.
20. Chen B., Guo H., Song A.W. Correction for direction-dependent distortions in diffusion tensor imaging using matched magnetic field maps. NeuroImage 2006, 30(1):121-129.
21. Chung M.K., Worsley K.J., Paus T., Cherif C., Collins D.L., Giedd J.N., Rapoport J.L., Evans A.C. A unified statistical approach to deformation-based morphometry. NeuroImage 2001, 14(3):595-606.
22. Dekaban A.S. Changes in brain weight during the in brain weight during the span of human life: relation of brain weights to body heights and body weights. Ann. Neurol. 1978, 4:345-356.
23. Ding X.Q., Sun Y., Braass H., Illies T., Zeumer H., Lanfermann H., Fiehler J. Evidence of rapid ongoing brain development beyond 2years of age detected by fiber tracking. Am. J. Neuroradiol. 2008, 29(7):1261-1265.
24. Du Y., Dreyfus C.F. Oligodendrocytes as providers of growth factors. J. Neurosci. Res. 2002, 68(6):647-654.
25. 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(4):1121-1132.
26. Dubois J., Dehaene-Lambertz G., Soares C., Cointepas Y., Le Bihan D., Hertz-Pannier L. Microstructural correlates of infant functional development: example of the visual pathways. J. Neurosci. 2008, 28(8):1943-1948.
27. Engelbrecht V., Scherer A., Rassek M., Witsack H.J., Modder U. Diffusion-weighted MR imaging in the brain in children: findings in the normal brain and in the brain with white matter diseases. Radiology 2002, 222(2):410-418.
28. Eyre J.A., Miller S., Ramesh V. Constancy of central conduction delays during development in man: investigation of motor and somatosensory pathways. J. Physiol. 1991, 434:441-452.
29. Fields R.D., Stevens-Graham B. New insights into neuron-glia communication. Science 2002, 298(5593):556-562.
30. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 1999, 2(10):861-863.
31. 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(9):1789-1795.
32. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(21):8174-8179.
33. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 2001, 14:21-36.
34. Hasan K.M., Halphen C., Sankar A., Eluvathingal T.J., Kramer L., Stuebing K.K., Ewing-Cobbs L., Fletcher J.M. Diffusion tensor imaging-based tissue segmentation: validation and application to the developing child and adolescent brain. NeuroImage 2007, 34(4):1497-1505.
35. Hasan K.M., Sankar A., Halphen C., Kramer L.A., Brandt M.E., Juranek J., Cirino P.T., Fletcher J.M., Papanicolaou A.C., Ewing-Cobbs L. Development and organization of the human brain tissue compartments across the lifespan using diffusion tensor imaging. NeuroReport 2007, 18(16):1735-1739.
36. Hasan K.M., Kamali A., Kramer L.A., Papnicolaou A.C., Fletcher J.M., Ewing-Cobbs L. Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan. Brain Res. 2008, 1227:52-67.
37. Hermoye L., Saint-Martin C., Cosnard G., Lee S.K., Kim J., Nassogne M.C., Menten R., Clapuyt P., Donohue P.K., Hua K., et al. Pediatric diffusion tensor imaging: normal database and observation of the white matter maturation in early childhood. NeuroImage 2006, 29(2):493-504.
38. Hua X., Leow A.D., Levitt J.G., Caplan R., Thompson P.M., Toga A.W. Detecting brain growth patterns in normal children using tensor-based morphometry. Hum. Brain Mapp. 2009, 30(1):209-219.
39. Huang H., Zhang J., Wakana S., Zhang W., Ren T., Richards L.J., Yarowsky P., Donohue P., Graham E., van Zijl P.C., et al. White and gray matter development in human fetal, newborn and pediatric brains. NeuroImage 2006, 33(1):27-38.
40. Huang H., Ceritoglu C., Li X., Qiu A., Miller M.I., van Zijl P.C., Mori S. Correction of B0 susceptibility induced distortion in diffusion-weighted images using large-deformation diffeomorphic metric mapping. Magn. Reson. Imaging 2008, 26(9):1294-1302.
41. Huppi P.S., Dubois J. Diffusion tensor imaging of brain development. Semin. Fetal Neonatal Med. 2006, 11(6):489-497.
42. Jiang H., van Zijl P.C., Kim J., Pearlson G.D., Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Prog. Biomed. 2006, 81(2):106-116.
43. Kandel E.R., Schwarz J.H., Jessel T.M. Principles of Neural Science 2000, McGraw-Hill Medical, New York. 4th ed.
44. 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(3):217-234.
45. Klingberg T., Vaidya C.J., Gabrieli J.D., Moseley M.E., Hedehus M. Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. NeuroReport 1999, 10(13):2817-2821.
46. Konishi Y., Hayakawa K., Kuriyama M., Fujii Y., Sudo M., Konishi K., Ishii Y. Developmental features of the brain in preterm and fullterm infants on MR imaging. Early Hum. Dev. 1993, 34(1-2):155-162.
47. Landis J.R., Koch G.G. The measurement of observer agreement for categorical data. Biometrics 1977, 33(1):159-174.
48. Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat. Rev. Neurosci. 2003, 4(6):469-480.
49. Lebel C., Walker L., Leemans A., Phillips L., Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. NeuroImage 2008, 40(3):1044-1055.
50. Lee J.E., Chung M.K., Lazar M., DuBray M.B., Kim J., Bigler E.D., Lainhart J.E., Alexander A.L. A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis. NeuroImage 2009, 44(3):870-883.
51. Lenroot R.K., Giedd J.N. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci. Biobehav. Rev. 2006, 30(6):718-729.
52. Maas L.C., Mukherjee P., Carballido-Gamio J., Veeraraghavan S., Miller S.P., Partridge S.C., Henry R.G., Barkovich A.J., Vigneron D.B. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. NeuroImage 2004, 22(3):1134-1140.
53. McKinstry R.C., Mathur A., Miller J.H., Ozcan A., Snyder A.Z., Schefft G.L., Almli C.R., Shiran S.I., Conturo T.E., Neil J.J. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb. Cortex 2002, 12(12):1237-1243.
54. Miller M.I., Beg M.F., Ceritoglu C., Stark C. Increasing the power of functional maps of the medial temporal lobe by using large deformation diffeomorphic metric mapping. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(27):9685-9690.
55. Mori S., Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006, 51(5):527-539.
56. Mori S., Itoh R., Zhang J., Kaufmann W.E., van Zijl P.C., Solaiyappan M., Yarowsky P. Diffusion tensor imaging of the developing mouse brain. Magn. Reson. Med. 2001, 46(1):18-23.
57. Mori S., Oishi K., Jiang H., Jiang L., Li X., Akhter K., Hua K., Faria A.V., Mahmood A., Woods R., et al. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage 2008, 40(2):570-582.
58. Morrison J.H., Hof P.R. Life and death of neurons in the aging brain. Science 1997, 278(5337):412-419.
59. Moseley M. Diffusion tensor imaging and aging - a review. NMR Biomed. 2002, 15(7-8):553-560.
60. Mukherjee P., Miller J.H., Shimony J.S., Conturo T.E., Lee B.C., Almli C.R., McKinstry R.C. Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology 2001, 221(2):349-358.
61. Mukherjee P., Miller J.H., Shimony J.S., Philip J.V., Nehra D., Snyder A.Z., Conturo T.E., Neil J.J., McKinstry R.C. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. Am. J. Neuroradiol. 2002, 23(9):1445-1456.
62. Muller K., Homberg V., Lenard H.G. Magnetic stimulation of motor cortex and nerve roots in children. maturation of cortico-motoneuronal projections. Electroencephalogr. Clin. Neurophysiol. 1991, 81(1):63-70.
63. Neil J.J., Shiran S.I., McKinstry R.C., Schefft G.L., Snyder A.Z., Almli C.R., Akbudak E., Aronovitz J.A., Miller J.P., Lee B.C., et al. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 1998, 209(1):57-66.
64. Nezu A., Kimura S., Uehara S., Kobayashi T., Tanaka M., Saito K. Magnetic stimulation of motor cortex in children: maturity of corticospinal pathway and problem of clinical application. Brain Dev. 1997, 19(3):176-180.
65. Nilsson M., Latt J., Nordh E., Wirestam R., Stahlberg F., Brockstedt S. On the effects of a varied diffusion time in vivo: is the diffusion in white matter restricted?. Magn. Reson. Imaging 2008, 27(2):176-187.
66. Oishi K., Zilles K., Amunts K., Faria A., Jiang H., Li X., Akhter K., Hua K., Woods R., Toga A.W., et al. Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. NeuroImage 2008, 43(3):447-457.
67. Oishi K., Faria A., Jiang H., Li X., Akhter K., Zhang J., Hsu J.T., Miller M.I., van Zijl P.C., Albert M., et al. Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: application to normal elderly and alzheimer's disease participants. NeuroImage 2009, 46(2):486-499.
68. Paus T., Zijdenbos A., Worsley K., Collins D.L., Blumenthal J., Giedd J.N., Rapoport J.L., Evans A.C. Structural maturation of neural pathways in children and adolescents: in vivo study. Science 1999, 283(5409):1908-1911.
69. Paus T., Collins D.L., Evans A.C., Leonard G., Pike B., Zijdenbos A. Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res. Bull. 2001, 54(3):255-266.
70. Petanjek Z., Judas M., Kostovic I., Uylings H.B. Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: A layer-specific pattern. Cereb. Cortex 2008, 18(4):915-929.
71. Pierpaoli C., Basser P.J. Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996, 36(6):893-906.
72. Pierpaoli C., Barnett A., Pajevic S., Chen R., Penix L.R., Virta A., Basser P. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage 2001, 13:1174-1185.
73. Qiu D., Tan L.H., Zhou K., Khong P.L. Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. NeuroImage 2008, 41(2):223-232.
74. Reiss A.L., Abrams M.T., Singer H.S., Ross J.L., Denckla M.B. Brain development, gender and IQ in children. A volumetric imaging study. Brain 1996, 119:1763-1774.
75. Riddle W.R., Li R., Fitzpatrick J.M., DonLevy S.C., Dawant B.M., Price R.R. Characterizing changes in MR images with color-coded Jacobians. Magn. Reson. Imaging 2004, 22(6):769-777.
76. Salat D.H., Tuch D.S., Hevelone N.D., Fischl B., Corkin S., Rosas H.D., Dale A.M. Age-related changes in prefrontal white matter measured by diffusion tensor imaging. Ann. N. Y. Acad. Sci. 2005, 1064:37-49.
77. Schmithorst V.J., Wilke M., Dardzinski B.J., Holland S.K. Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study. Radiology 2002, 222(1):212-218.
78. Shaw P., Kabani N.J., Lerch J.P., Eckstrand K., Lenroot R., Gogtay N., Greenstein D., Clasen L., Evans A., Rapoport J.L., et al. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 2008, 28(14):3586-3594.
79. 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., et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006, 31(4):1487-1505.
80. Snook L., Paulson L.A., Roy D., Phillips L., Beaulieu C. Diffusion tensor imaging of neurodevelopment in children and young adults. NeuroImage 2005, 26(4):1164-1173.
81. Sowell E.R., Thompson P.M., Tessner K.D., Toga A.W. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J. Neurosci. 2001, 21(22):8819-8829.
82. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., Toga A.W. Mapping cortical change across the human life span. Nat. Neurosci. 2003, 6(3):309-315.
83. Stegemann T., Heimann M., Dusterhus P., Schulte-Markwort M. Diffusion tensor imaging (DTI) and its importance for exploration of normal or pathological brain development. Fortschr. Neurol. Psychiatr. 2006, 74(3):136-148.
84. Thompson P.M., Giedd J.N., Woods R.P., MacDonald D., Evans A.C., Toga A.W. Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature 2000, 404(6774):190-193.
85. Thornton J.S., Ordidge R.J., Penrice J., Cady E.B., Amess P.N., Punwani S., Clemence M., Wyatt J.S. Anisotropic water diffusion in white and gray matter of the neonatal piglet brain before and after transient hypoxia-ischaemia. Magn. Reson. Imaging 1997, 15(4):433-440.
86. van der Knaap M.S., Valk J. MR imaging of the various stages of normal myelination during the first year of life. Neuroradiology 1990, 31(6):459-470.
87. Wilke M., Krageloh-Mann I., Holland S.K. Global and local development of gray and white matter volume in normal children and adolescents. Exp. Brain Res. 2007, 178(3):296-307.
88. Woods R.P., Grafton S.T., Holmes C.J., Cherry S.R., Mazziotta J.C. Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 1998, 22(1):139-152.
89. Xu D., Mori S., Shen D., van Zijl P.C., Davatzikos C. Spatial normalization of diffusion tensor fields. Magn. Reson. Med. 2003, 50(1):175-182.
90. Zhang H., Yushkevich P.A., Alexander D.C., Gee J.C. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med. Image Anal. 2006, 10(5):764-785.
91. Zhuang J., Hrabe J., Kangarlu A., Xu D., Bansal R., Branch C.A., Peterson B.S. Correction of eddy-current distortions in diffusion tensor images using the known directions and strengths of diffusion gradients. J. Magn. Reson. Imaging 2006, 24(5):1188-1193.