One diffusion acquisition and different white matter models: How does microstructure change in human early development based on WMTI and NODDI?

NeuroImage

Volumn 107, Issue , 2015, Pages 242-256

  Jelescu, Ileana O ^a   Veraart, Jelle ^a   Adisetiyo, Vitria ^a   Milla, Sarah S ^a   Novikov, Dmitry S ^a   Fieremans, Els ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Brain development; Diffusion MRI; DKI; Microstructure; Modeling; White matter

Indexed keywords

ARTICLE; BRAIN DEVELOPMENT; CHILD; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; DIFFUSIONAL KURTOSIS IMAGING; HUMAN; IMAGING AND DISPLAY; INFANT; INTERMETHOD COMPARISON; MALE; MEASUREMENT; NERVE TRACT; NEURITE ORIENTATION DISPERSION AND DENSITY IMAGING; NEUROIMAGING; NEWBORN; PRESCHOOL CHILD; QUANTITATIVE ANALYSIS; SIMULATION; WHITE MATTER; WHITE MATTER TRACT INTEGRITY METRICS; AGING; ANATOMY AND HISTOLOGY; BIOLOGICAL MODEL; CAPSULA INTERNA; COMPUTER SIMULATION; CORPUS CALLOSUM; DIFFUSION WEIGHTED IMAGING; FEMALE; GROWTH, DEVELOPMENT AND AGING; MYELIN SHEATH; MYELINATED NERVE; NERVE FIBER; NEURITE; PHYSIOLOGY;

AGING; AXONS; COMPUTER SIMULATION; CORPUS CALLOSUM; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; INTERNAL CAPSULE; MALE; MODELS, NEUROLOGICAL; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURITES; WHITE MATTER;

EID: 84920273672     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.12.009     Document Type: Article

References (50)

1. Alexander D.C., Hubbard P.L., Hall M.G., Moore E.A., Ptito M., Parker G.J.M., Dyrby T.B. Orientationally invariant indices of axon diameter and density from diffusion MRI. NeuroImage 2010, 52:1374-1389.
2. Assaf Y., Basser P.J. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. NeuroImage 2005, 27:48-58.
3. Assaf Y., Blumenfeld-Katzir T., Yovel Y., Basser P.J. AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn. Reson. Med. 2008, 59:1347-1354.
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 1996, 111:209-219.
5. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
6. Behrens T.E., Woolrich M.W., Jenkinson M., Johansen-Berg H., Nunes R.G., Clare S., Matthews P.M., Brady J.M., Smith S.M. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 2003, 50:1077-1088.
7. Ben-Amitay S., Jones D.K., Assaf Y. Motion correction and registration of high b-value diffusion weighted images. Magn. Reson. Med. 2012, 67:1694-1702.
8. Benitez A., Fieremans E., Jensen J.H., Falangola M.F., Tabesh A., Ferris S.H., Helpern J.A. White matter tract integrity metrics reflect the vulnerability of late-myelinating tracts in Alzheimer's disease. Neuroimage Clin. 2013, 4:64-71.
9. Benveniste H., Hedlund L.W., Johnson G.A. Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 1992, 23:746-754.
10. Colby J.B., Van Horn J.D., Sowell E.R. Quantitative in vivo evidence for broad regional gradients in the timing of white matter maturation during adolescence. NeuroImage 2011, 54:25-31.
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., Kulikova S., Poupon C., Huppi P.S., Hertz-Pannier L. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 2014, 276:48-71.
13. Duong T.Q., Ackerman J.J., Ying H.S., Neil J.J. Evaluation of extra- and intracellular apparent diffusion in normal and globally ischemic rat brain via 19F NMR. Magn. Reson. Med. 1998, 40:1-13.
14. Falangola M.F., Guilfoyle D.N., Tabesh A., Hui E.S., Nie X., Jensen J.H., Gerum S.V., Hu C., LaFrancois J., Collins H.R., Helpern J.A. Histological correlation of diffusional kurtosis and white matter modeling metrics in cuprizone-induced corpus callosum demyelination. NMR Biomed. 2014, 27:948-957.
15. Ferizi U., Schneider T., Tariq M., Wheeler-Kingshott C.A., Zhang H., Alexander D.C. The importance of being dispersed: a ranking of diffusion MRI models for fibre dispersion using in vivo human brain data. Med. Image Comput. Comput. Assist. Interv. 2013, 16:74-81.
16. Fieremans E., De Deene Y., Delputte S., Özdemir M.S., D'Asseler Y., Vlassenbroeck J., Deblaere K., Achten E., Lemahieu I. Simulation and experimental verification of the diffusion in an anisotropic fiber phantom. J. Magn. Reson. 2008, 190:189-199.
17. Fieremans E., Novikov D.S., Jensen J.H., Helpern J.A. Monte Carlo study of a two-compartment exchange model of diffusion. NMR Biomed. 2010, 23:711-724.
18. Fieremans E., Jensen J.H., Helpern J.A. White matter characterization with diffusional kurtosis imaging. NeuroImage 2011, 58:177-188.
19. Fieremans E., Jensen J.H., Helpern J.A., Kim S., Grossman R.I., Inglese M., Novikov D.S. Diffusion distinguishes between axonal loss and demyelination in brain white matter. Proc. Intl. Soc. Mag. Reson. Med. 2012, 20:465. (Melbourne, Australia).
20. Fieremans E., Benitez A., Jensen J.H., Falangola M.F., Tabesh A., Deardorff R.L., Spampinato M.V., Babb J.S., Novikov D.S., Ferris S.H., Helpern J.A. Novel white matter tract integrity metrics sensitive to Alzheimer disease progression. AJNR Am. J. Neuroradiol. 2013, 34:2105-2112.
21. Hermoye L., Saint-Martin C., Cosnard G., Lee S.-K., Kim J., Nassogne M.-C., Menten R., Clapuyt P., Donohue P.K., Hua K. Pediatric diffusion tensor imaging: normal database and observation of the white matter maturation in early childhood. NeuroImage 2006, 29:493-504.
22. Holland B.A., Haas D.K., Norman D., Brant-Zawadzki M., Newton T.H. MRI of normal brain maturation. AJNR Am. J. Neuroradiol. 1986, 7:201-208.
23. Horsfield M.A., Jones D.K. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases - a review. NMR Biomed. 2002, 15:570-577.
24. Hui E.S., Fieremans E., Jensen J.H., Tabesh A., Feng W., Bonilha L., Spampinato M.V., Adams R., Helpern J.A. Stroke assessment with diffusional kurtosis imaging. Stroke 2012, 43:2968-2973.
25. Hurvich C.M., Tsai C.-L. Regression and time series model selection in small samples. Biometrika 1989, 76:297-307.
26. Jensen J.H., Helpern J.A., Ramani A., Lu H., Kaczynski K. Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn. Reson. Med. 2005, 53:1432-1440.
27. Jespersen S.N., Kroenke C.D., Ostergaard L., Ackerman J.J., Yablonskiy D.A. Modeling dendrite density from magnetic resonance diffusion measurements. NeuroImage 2007, 34:1473-1486.
28. Jespersen S.N., Bjarkam C.R., Nyengaard J.R., Chakravarty M.M., Hansen B., Vosegaard T., Ostergaard L., Yablonskiy D., Nielsen N.C., Vestergaard-Poulsen P. Neurite density from magnetic resonance diffusion measurements at ultrahigh field: comparison with light microscopy and electron microscopy. NeuroImage 2010, 49:205-216.
29. Kemper T.L. Neuroanatomical and neuropathological changes during ageing. Clinical Neurology of Ageing 1994, 8-9. Oxford University Press, New York. M.L. Albert, J.E. Knoefel (Eds.).
30. Kiselev V.G., Il'yasov K.A. Is the "biexponential diffusion" biexponential?. Magn. Reson. Med. 2007, 57:464-469.
31. Kostović I., Jovanov-Milošević N. The development of cerebral connections during the first 20-45weeks' gestation. Seminars in Fetal and Neonatal Medicine 2006, 415-422. Elsevier.
32. Kroenke C.D., Ackerman J.J., Yablonskiy D.A. On the nature of the NAA diffusion attenuated MR signal in the central nervous system. Magn. Reson. Med. 2004, 52:1052-1059.
33. Kunz N., Zhang H., Vasung L., O'Brien K.R., Assaf Y., Lazeyras F., Alexander D.C., Huppi P.S. Assessing white matter microstructure of the newborn with multi-shell diffusion MRI and biophysical compartment models. NeuroImage 2014, 96:288-299.
34. Lamantia A.S., Rakic P. Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J. Comp. Neurol. 1990, 291:520-537.
35. Lourakis M.I.A. levmar: Levenberg - Marquardt Nonlinear Least Squares Algorithms in {C}/{C}++ http://www.ics.forth.gr/~lourakis/levmar/+.
36. Lu H., Jensen J.H., Ramani A., Helpern J.A. Three-dimensional characterization of non-Gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed. 2006, 19:236-247.
37. Mikula S., Binding J., Denk W. Staining and embedding the whole mouse brain for electron microscopy. Nat. Methods 2012, 9:1198-1201.
38. 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, 23:1445-1456.
39. Novikov D.S., Fieremans E. Relating extracellular diffusivity to cell size distribution and packing density as applied to white matter. Proc. Intl. Soc. Mag. Reson. Med. 2012, 20. (Melbourne, Australia).
40. Paydar A., Fieremans E., Nwankwo J.I., Lazar M., Sheth H.D., Adisetiyo V., Helpern J.A., Jensen J.H., Milla S.S. Diffusional kurtosis imaging of the developing brain. AJNR Am. J. Neuroradiol. 2014, 35:808-814.
41. Ronen I., Budde M., Ercan E., Annese J., Techawiboonwong A., Webb A. Microstructural organization of axons in the human corpus callosum quantified by diffusion-weighted magnetic resonance spectroscopy of N-acetylaspartate and post-mortem histology. Brain Struct. Funct. 2014, 219(5):1773-1785.
42. Stanisz G.J., Szafer A., Wright G.A., Henkelman R.M. An analytical model of restricted diffusion in bovine optic nerve. Magn. Reson. Med. 1997, 37:103-111.
43. Szafer A., Zhong J., Gore J.C. Theoretical model for water diffusion in tissues. Magn. Reson. Med. 1995, 33:697-712.
44. Veraart J., Rajan J., Peeters R.R., Leemans A., Sunaert S., Sijbers J. Comprehensive framework for accurate diffusion MRI parameter estimation. Magn. Reson. Med. 2013, 70:972-984.
45. Veraart J., Sijbers J., Sunaert S., Leemans A., Jeurissen B. Weighted linear least squares estimation of diffusion MRI parameters: strengths, limitations, and pitfalls. NeuroImage 2013, 81:335-346.
46. Wang Z., Wang Y., Zhang J., Yan X., Liu H., Xiao Z. The performance of NODDI estimation using a common 2-shell protocol. Proc. Intl. Soc. Mag. Reson. Med., Milan, Italy 2014, 2596.
47. Yakovlev P.I., Lecours A.R. The myelogenic cycles of regional maturation of the brain. Regional Development of the Brain Early in Life 1967, 3-70. Blackwell Scientific Publications Inc., Oxford. A. Minkowski (Ed.).
48. Young I.R., Hall A.S., Pallis C.A., Legg N.J., Bydder G.M., Steiner R.E. Nuclear magnetic resonance imaging of the brain in multiple sclerosis. Lancet 1981, 2:1063-1066.
49. Zhang H. NODDI Matlab toolbox http://www.nitrc.org/projects/noddi_toolbox/.
50. Zhang H., Schneider T., Wheeler-Kingshott C.A., Alexander D.C. NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. NeuroImage 2012, 61:1000-1016.