Differences of inter-tract correlations between neonates and children around puberty: A study based on microstructural measurements with DTI

Frontiers in Human Neuroscience

Volumn , Issue OCT, 2013, Pages

  Mishra, Virendra ^a   Cheng, Hua ^b,c   Gong, Gaolang ^d   He, Yong ^d   Dong, Qi ^d   Huang, Hao ^a,e  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d BEIJING NORMAL UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Brain development; DTI; Homologous; Inter tract correlation; Microstructure; Neonate

Indexed keywords

ADOLESCENT; ARTICLE; AXIAL DIFFUSIVITY; BRAIN DEVELOPMENT; BRAIN FUNCTION; CHILD; CHILDBIRTH; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; HUMAN EXPERIMENT; MALE; MEAN DIFFUSIVITY; MYELINATION; NEWBORN; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PHYSICAL PARAMETERS; PUBERTY; RADIAL DIFFUSIVITY; SCHOOL CHILD; WHITE MATTER;

EID: 84887957838     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00721     Document Type: Article

References (63)

1. Barnea-Goraly, N., Menon, V., Eckert, M., Tamm, L., Bammer, R., Karchemskiy, A., et al. (2005). White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb. Cortex 15, 1848-1854. doi: 10. 1093/cercor/bhi062.
2. Basser, P. J., Mattiello, J., and LeBihan, D. (1994). Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B 103, 247-254. doi: 10. 1006/jmrb. 1994. 1037.
3. Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., and Aldroubi, A. (2000). In vitro fiber tractography using DT-MRI data. Magn. Reson. Med. 44, 625-632. doi: 10. 1002/1522-2594(200010)44: 4<625:: AID-MRM17>3. 0. CO; 2-0.
4. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system-a technical review. NMR Biomed. 15, 435-455. doi: 10. 1002/nbm. 782.
5. Behrens, T. E., Berg, H. J., Jbabdi, S., Rushworth, M. F., and Woolrich, M. W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: what can we gain. Neuroimage 34, 144-155. doi: 10. 1016/j. neuroimage. 2006. 09. 018.
6. Bonekamp, D., Nagae, L. M., Degaonkar, M., Matson, M., Abdalla, W. M., Barker, P. B., et al. (2007). Diffusion tensor imaging in children and adolescents: reproducibility, hemispheric and age-related differences. Neuroimage 34, 733-742. doi: 10. 1016/j. neuroimage. 2006. 09. 020.
7. Catani, M., Howard, R. J., Pajevic, S., and Jones, D. K. (2002). Virtual in vivointeractive dissection of white matter fasciculi in the human brain. Neuroimage 17, 77-94. doi: 10. 1006/nimg. 2002. 1136.
8. Colby, J. B., Soderberg, L., Lebel, C., Dinov, I. D., Thompson, P. M., and Sowell, E. R. (2012). Along-tract statistics allow for enhanced tractography analysis. Neuroimage59, 3227-3242. doi: 10. 1016/j. neuroimage. 2011. 11. 004.
9. Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., et al. (1999). Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U. S. A. 96, 10422-10427. doi: 10. 1073/pnas. 96. 18. 10422.
10. Doria, V., Beckmann, C. F., Arichi, T., Mercahnt, N., Groppo, M., Turkheimer, F. E., et al. (2010). Emergence of resting state networks in the preterm human brain. Proc. Natl. Acad. Sci. U. S. A. 46, 20015-20020. doi: 10. 1073/pnas. 1007921107.
11. Douaud, G., Jbabdi, S., Behrens, T. E., Menke, R. A., Gass, A., Monsch, A. U., et al. (2011). DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. Neuroimage 55, 880-890. doi: 10. 1016/j. neuroimage. 2010. 12. 008.
12. Dubois, J., Deheane-Lambertz, G., Perrin, M., Mangin, J. F., Cointepas, Y., Duchesnay, E., et al. (2008). Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum. Brain Mapp. 1, 14-27. doi: 10. 1002/hbm. 20363.
13. Eluvathingal, T. J., Hasan, K. M., Kramer, L., Fletcher, J. M., and Ewing-Cobbs, L. (2007). Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cereb. Cortex 12, 2760-2768. doi: 10. 1093/cercor/bhm003.
14. Ennis, D. B., and Kindlmann, G. (2006). Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magn. Reson. Med. 55, 136-146. doi: 10. 1002/mrm. 20741.
15. Fisher, R. A. (1915). Frequency distribution of the values of the correlation coefficient in samples of an infinitely large population. Biometrika 10, 507-521.
16. Fransson, P., Skold, B., Horsch, S., Nordell, A., Blennow, M., Lagercrantz, H., et al. (2007). Resting-state networks in the infant brain. Proc. Natl. Acad. Sci. U. S. A. 104, 15531-15536. doi: 10. 1073/pnas. 0704380104.
17. Fritzsche, K. H., Laun, F. B., Meinzer, H. P., and Stieltjes, B. (2010). Opportunities and pitfalls in the quantification of fiber integrity: what can we gain from Q-ball imaging. Neuroimage 51, 242-251. doi: 10. 1016/j. neuroimage. 2010. 02. 007.
18. Gao, W., Lin, W., Chen, Y., Geirg, G., Smith, J. K., Jewells, V., et al. (2009). Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. Am. J. Neuroradiol. 30, 290-296. doi: 10. 3174/ajnr. A1363.
19. Giorgio, A., Santelli, L., Tomassini, V., Bosnell, R., Smith, S., Se Stefano, N., et al. (2010). Age-related changes in grey and white matter structure throughout adulthood. Neuroimage 51, 943-951. doi: 10. 1016/j. neuroimage. 2010. 03. 004.
20. Goodlett, C. B., Fletcher, P. T., Gilmore, J. H., and Gerig, G. (2009). Group analysis of DTI fiber tract statistics with application to neurodevelopment. Neuroimage 45, S133-S142. doi: 10. 1016/j. neuroimage. 2008. 10. 060.
21. Hosey, T., Harding, S. G., Carpenter, T. A., Ansorge, R. E., and Williams, G. B. (2008). Application of a probabilistic double-fibre structure model to diffusion weighted MR images of the human brain. Magn. Reson. Imaging 26, 236-245. doi: 10. 1016/j. mri. 2007. 07. 002.
22. Huang, H., Fan, X., Weiner, M., Martin-Cook, K., Xiao, G., Davis, J., et al. (2012a). Distinctive disruption patterns of white matter tracts in Alzheimer's disease with full diffusion tensor characterization. Neurobiol. Aging 33, 2029-2045. doi: 10. 1016/j. neurobiolaging. 2011. 06. 027.
23. Huang, H., Gundapuneedi, T., and Rao, U. (2012b). White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology. Neuropsychopharmacology 37, 2693-2701. doi: 10. 1038/npp. 2012. 133.
24. Huang, H., Fan, X., Williamson, D. E., and Rao, U. (2011). White matter changes in healthy adolescents at familial risk for unipolar depression: a diffusion tensor imaging study. Neuropsychopharmacology 36, 684-691. doi: 10. 1038/npp. 2010. 199.
25. Huang, H., Zhang, J., Wakana, S., Zhang, W., Ren, T., Richards, L. J., et al. (2006). White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 33, 27-38. doi: 10. 1016/j. neuroimage. 2006. 06. 009.
26. Jbabdi, S., Behrens, T. E. J., and Smith, S. M. (2010). Crossing fibers in tract-based spatial statistics. Neuroimage 49, 249-256. doi: 10. 1016/j. neuroimage. 2009. 08. 039.
27. Jiang, H., van Zijl, P. C., Kim, J., Pearlson, G. D., and Mori, S. (2006). DTIStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Programs Biomed. 81, 106-116. doi: 10. 1016/j. cmpb. 2005. 08. 004.
28. Jones, D. K., Simmons, A., Williams, S. C., and Horsfield, M. A. (1999a). Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn. Reson. Med. 42, 37-41. doi: 10. 1002/(SICI)1522-2594(199907)42: 1<37:: AID-MRM7>3. 0. CO; 2-O.
29. Jones, D. K., Horsfield, M. A., and Simmons, A. (1999b). Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn. Reson. Med. 42, 515-525. doi: 10. 1002/(SICI)1522-2594(199909)42: 3<515:: AID-MRM14>3. 3. CO; 2-H.
30. Lazar, M., Weinstein, D. M., Tsuruda, J. S., Hasan, K. M., Arfanakis, K., Meyerand, M. E., et al. (2003). White matter tractography using diffusion tensor deflection. Hum. Brain Mapp. 18, 306-321. doi: 10. 1002/hbm. 10102.
31. Lebel, C., Walker, L., Leemans, A., Phillips, L., and Beaulieu, C. (2008). Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40, 1044-1055. doi: 10. 1016/j. neuroimage. 2007. 12. 053.
32. Li, Y. O., Yang, F. G., Nguyen, C. T., Cooper, S. R., LaHue, S. C., Venugopal, S., et al. (2012). Independent component analysis of DTI reveals microstructural correlations of white matter in the human brain. Hum. Brain Mapp. 33, 1431-1451. doi: 10. 1002/hbm. 21292.
33. Martino, J., Brogna, C., Robles, S. G., Vergani, F., and Duffau, H. (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46, 691-699. doi: 10. 1016/j. cortex. 2009. 07. 015.
34. Mori, S., Crain, B. J., Chacko, V. P., and van Zijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265-269. doi: 10. 1002/1531-8249(199902)45: 2<265:: AID-ANA21>3. 0. CO; 2-3.
35. Mukherjee, P., Miller, J. H., Shimony, J. S., Philip, J. V., Nehra, D., Snyder, A. Z., et al. (2002). Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. Am. J. Neuroradiol. 23, 1445-1456.
36. O'Donnell, L. J., Westin, C. F., and Golby, A. J. (2009). Tract-based morphometry for white matter group analysis. Neuroimage 45, 832-844. doi: 10. 1016/j. neuroimage. 2008. 12. 023.
37. Oishi, K., Mori, S., Donohue, P. K., Ernst, T., Anderson, L., Buchthal, S., et al. (2011). Multi-contrast human neonatal brain atlas: application to normal neonate development analysis. Neuroimage 56, 8-20. doi: 10. 1016/j. neuroimage. 2011. 01. 051.
38. Ozarslan, E., Vemuri, B. C., and Mareci, T. H. (2005). Generalized scalar measures for diffusion MRI using trace, variance and entropy. Magn. Reson. Med. 53, 866-876. doi: 10. 1002/mrm. 20411.
39. Parker, G. J., Wheeler-Kingshott, C. A. M., and Barker, G. J. (2002). Estimating distributed anatomical connectivity using fast marching methods and diffusion tensor imaging. IEEE Trans. Med. Imaging 21, 505-512. doi: 10. 1109/TMI. 2002. 1009386.
40. Pierpaoli, C., and Basser, P. J. (1996). Toward a quantitative assessment to diffusion anisotropy. Magn. Reson. Med. 36, 893-906. doi: 10. 1002/mrm. 1910360612.
41. Rencher, A. C. (2002). Methods of Multivariate Analysis, 2nd Edn. Hoboken, NJ: Wiley Interscience. doi: 10. 1002/0471271357.
42. Saxena, K., Tamm, L., Walley, A., Simmons, A., Rollins, N., Chia, J., et al. (2012). A preliminary investigation of corpus callosum and anterior commissure aberrations in aggressive youth with bipolar disorders. J. Child Adolesc. Psychopharmacol. 22, 112-119. doi: 10. 1089/cap. 2011. 0063.
43. Schmithorst, V. J., and Yuan, W. (2010). White matter development during adolescence as shown by diffusion MRI. Brain Cogn. 72, 16-25. doi: 10. 1016/j. bandc. 2009. 06. 005.
44. Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Syst. Biol 51, 492-508. doi: 10. 1080/10635150290069913.
45. Shimodaira, H. (2004). Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann. Stat. 32, 2616-2641. doi: 10. 1214/009053604000000823.
46. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505. doi: 10. 1016/j. neuroimage. 2006. 02. 024.
47. Snook, L., Paulson, L., Roy, D., Phillips, L., and Beaulieu, C. (2005). Diffusion tensor imaging of neurodevelopment in children and young adults. Neuroimage 26, 1164-1173. doi: 10. 1016/j. neuroimage. 2005. 03. 016.
48. Song, S. K., Sun, S. W., Ramsbottom, M. J., Chang, C., Russell, J., and Cross, A. H. (2002). Dysmelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429-1436. doi: 10. 1006/nimg. 2002. 1267.
49. Stieltjes, B., Kaufmann, W. E., van Zijl, P. C. M., Fredericksen, K., Pearlson, G. D., and Mori, S. (2001). Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14, 723-735. doi: 10. 1006/nimg. 2001. 0861.
50. Suzuki, R., and Shimodaira, H. (2006). Pvclust: an R package for assessing the uncertainity in hierarchical clustering. Bioinformatics 22, 1540-1542. doi: 10. 1093/bioinformatics/btl117.
51. Tamnes, C. K., Ostby, Y., Fiell, A. M., Westlye, L. T., Due-Tonnessen, P., and Walhovd, K. B. (2010). Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 20, 534-548. doi: 10. 1093/cercor/bhp118.
52. Tournier, J. D., Calamante, F., Gadian, D. G., and Connelly, A. (2004). Direct estimation of the fiber orientation density function from diffusion-weighed MRI data using spherical deconvolution. Neuroimage 23, 1176-1185. doi: 10. 1016/j. neuroimage. 2004. 07. 037.
53. Tuch, D. S. (2004). Q-ball imaging. Magn. Reson. Med. 52, 1358-1372. doi: 10. 1002/mrm. 20279.
54. Wahl, M., Li, Y. O., Ng, J., Lahue, S. C., Cooper, S. R., Sherr, E. H., et al. (2010). Microstructural correlations of white matter tracts in the human brain. Neuroimage51, 531-541. doi: 10. 1016/j. neuroimage. 2010. 02. 072.
55. Wakana, S., Caprihan, A., Panzenboeck, M. M., Fallon, J. H., Perry, M., Gollub, R. L., et al. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36, 630-644. doi: 10. 1016/j. neuroimage. 2007. 02. 049.
56. 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. doi: 10. 1148/radiol. 2301021640.
57. Westlye, L. T., Walhovd, K. B., Dale, A. M., Bjornerud, A., Due-Tonnessen, P., Engvig, A., et al. (2010). Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and Volumetry. Cereb. Cortex 20, 2055-2068. doi: 10. 1093/cercor/bhp280.
58. Wheeler-Kingshott, C. A., and Cercignani, M. (2009). About "axial" and "radial" diffusivities. Magn. Reson. Med. 61, 1255-1260. doi: 10. 1002/mrm. 21965.
59. Wilde, E. A., McCauley, S. R., Chu, Z., Hunter, J. V., Bigler, E. D., Yallampalli, R., et al. (2009). Diffsuion tensor imaging of hemispheric asymmetries in the developing brain. J. Clin. Exp. Neuropsychol. 31, 205-218. doi: 10. 1080/13803390802098118.
60. Woods, R. P., Grafton, S. T., Holmes, C. J., Cherry, S. R., and Mazziotta, J. C. (1998). Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 22, 139-152. doi: 10. 1097/00004728-199801000-00027.
61. Yushkevich, P. A., Zhang, H., Simon, T. J., and Gee, J. C. (2008). Structure-specific statistical mapping of white matter tracts. Neuroimage 41, 448-461. doi: 10. 1016/j. neuroimage. 2008. 01. 013.
62. Zhan, L., Leow, A. D., Jahanshad, N., Chiang, M. C., Barysheva, M., Lee, A. D., et al. (2010). How does angular resolution affect diffusion imaging measures. Neuroimage49, 1357-1371. doi: 10. 1016/j. neuroimage. 2009. 09. 057.
63. Zhang, Y., Zhang, J., Oishi, K., Faria, A. V., Jiang, H., Li, X., et al. (2010). Atlas-guided tract reconstruction for automated and comprehensive examination of the white matter anatomy. Neuroimage 52, 1289-1301. doi: 10. 1016/j. neuroimage. 2010. 05. 049.