Assessing white matter microstructure of the newborn with multi-shell diffusion MRI and biophysical compartment models

NeuroImage

Volumn 96, Issue , 2014, Pages 288-299

  Kunz, Nicolas ^a   Zhang, Hui ^b   Vasung, Lana ^a   O'Brien, Kieran R ^c   Assaf, Yaniv ^d   Lazeyras, François ^c   Alexander, Daniel C ^b   Hüppi, Petra S ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

CHARMED; Corpus callosum; DTI; Internal capsule; Intra axonal space; Intra neurite space; Maturation; Microstructure; MRI; Myelin; Newborn; NODDI; Periventricular crossroads of pathways; White matter

Indexed keywords

MYELIN;

ARTICLE; BIOPHYSICAL COMPARTMENT MODEL; BIOPHYSICS; BRAIN MATURATION; BRAIN RADIOGRAPHY; BRAIN VENTRICLE; CAPSULA INTERNA; CELL STRUCTURE; CHARMED LIGHT MODEL; COMPARATIVE STUDY; COMPARTMENT MODEL; CONTROLLED STUDY; CORPUS CALLOSUM; CORRELATION ANALYSIS; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED IMAGING; EXTERNAL CAPSULE; HUMAN; IMAGE ANALYSIS; IMAGING SOFTWARE; IN VIVO STUDY; INTERMETHOD COMPARISON; INTRANEURITE VOLUME FRACTION; MYELINATION; NERVE TRACT; NEURITE ORIENTATION DISPERSION INDEX; NEWBORN; NODDI MODEL; NUCLEAR MAGNETIC RESONANCE SCANNER; PERIVENTRICULAR CROSSROADS OF PATHWAYS; PRIORITY JOURNAL; RADIOLOGICAL PARAMETERS; WHITE MATTER; ALGORITHM; BIOLOGICAL MODEL; BRAIN; COMPUTER ASSISTED DIAGNOSIS; COMPUTER SIMULATION; CYTOLOGY; FEMALE; IMAGE ENHANCEMENT; MALE; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

ALGORITHMS; BRAIN; COMPUTER SIMULATION; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; INFANT, NEWBORN; MALE; MODELS, NEUROLOGICAL; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; WHITE MATTER;

EID: 84899919601     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.03.057     Document Type: Article

References (59)

1. Alexander D.C. A general framework for experiment design in diffusion MRI and its application in measuring direct tissue-microstructure features. Magn. Reson. Med. 2008, 60:439-448.
2. Alexander D.C., Barker G.J., Arridge S.R. Detection and modeling of non-Gaussian apparent diffusion coefficient profiles in human brain data. Magn. Reson. Med. 2002, 48:331-340.
3. 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.
4. Assaf Y., Basser P.J. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage 2005, 27:48-58.
5. 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.
6. 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, 210:133-142.
7. Barazany D., Basser P.J., Assaf Y. In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 2009, 132:1210-1220.
8. Bashat D.B., Kronfeld-Duenias V., Zachor D.A., Ekstein P.M., Hendler T., Tarrasch R., Even A., Levy Y., Sira L.B. Accelerated maturation of white matter in young children with autism: a high b value DWI study. Neuroimage 2007, 37:40-47.
9. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994, 66:259-267.
10. Beaulieu C. Chapter 6 - the biological basis of diffusion anisotropy. Diffusion MRI 2009, 105-126. Academic Press, San Diego. J.-B. Heidi, E.J.B. Timothy (Eds.).
11. Behrens T.E.J., 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.
12. 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. Exp. Neurol. 1987, 46:283-301.
13. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 2009, 10:186-198.
14. Cook P.A., Bai Y., Nedjati-Gilani S., Seunarine K., Hall M.G., Park G.J., Alexander D.C. Camino: open-source diffusion-MRI reconstruction and processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine, Seatle 2006.
15. Deoni S.C.L., Dean D.C., O'Muircheartaigh J., Dirks H., Jerskey B.A. Investigating white matter development in infancy and early childhood using myelin water faction and relaxation time mapping. Neuroimage 2012, 63:1038-1053.
16. Dubois J., Hertz-Pannier L., Dehaene-Lambertz G., Cointepas Y., Bihan D.L. 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.
17. Dyrby T.B., Søgaard L.V., Hall M.G., Ptito M., Alexander D.C. Contrast and stability of the axon diameter index from microstructure imaging with diffusion MRI. Magn. Reson. Med. 2013, 70:711-721.
18. Flechsig Of Leipsic P. Developmental (myelogenetic) localisation of the cerebral cortex in the human subject. Lancet 1901, 158:1027-1030.
19. Forbes K.P.N., Pipe J.G., Bird C.R. Changes in brain water diffusion during the 1st year of life. Radiology 2002, 222:405-409.
20. Gilmore J.H., Lin W., Corouge I., Vetsa Y.S.K., 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. AJNR Am. J. Neuroradiol. 2007, 28:1789-1795.
21. Huang H., Jeon T., Sedmak G., Pletikos M., Vasung L., Xu X., Yarowsky P., Richards L.J., Kostovic I., Sestan N., Mori S. Coupling diffusion imaging with histological and gene expression analysis to examine the dynamics of cortical areas across the fetal period of human brain development. Cereb. Cortex 2013, 23:2620-2631.
22. Hüppi P.S. Immature white matter lesions in the premature infant. J. Pediatr. 2004, 145:575-578.
23. Hüppi P.S., Dubois J. Diffusion tensor imaging of brain development. Semin. Fetal Neonatal Med. 2006, 11:489-497.
24. Hüppi P.S., Maier S.E., Peled S., Zientara G.P., Barnes P.D., Jolesz F.A., Volpe J.J. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr. Res. 1998, 44:584-590.
25. Hüppi P.S., Murphy B., Maier S.E., Zientara G.P., Inder T.E., Barnes P.D., Kikinis R., Jolesz F.A., Volpe J.J. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 2001, 107:455-460.
26. Inder T., Huppi P.S., Zientara G.P., Maier S.E., Jolesz F.A., di Salvo D., Robertson R., Barnes P.D., Volpe J.J. Early detection of periventricular leukomalacia by diffusion-weighted magnetic resonance imaging techniques. J. Pediatr. 1999, 134:631-634.
27. Jespersen S.N., Leigland L.A., Cornea A., Kroenke C.D. Determination of axonal and dendritic orientation distributions within the developing cerebral cortex by diffusion tensor imaging. IEEE Trans. Med. Imaging 2012, 31:16-32.
28. Judaš M. Prenatal development of the human fetal telencephalon. Fetal MRI 2011, 81-146. Springer, Berlin Heidelberg. D. Prayer (Ed.).
29. Judas M., Rados M., Jovanov-Milosevic N., Hrabac P., Stern-Padovan R., Kostovic I. Structural, immunocytochemical, and MR imaging properties of periventricular crossroads of growing cortical pathways in preterm infants. AJNR Am. J. Neuroradiol. 2005, 26:2671-2684.
30. Judaš M., Šimić G., Petanjek Z., Jovanov-Milošević N., Pletikos M., Vasung L., Vukšić M., Kostović I. The Zagreb Collection of human brains: a unique, versatile, but underexploited resource for the neuroscience community. Ann. N. Y. Acad. Sci. 2011, 1225(Suppl. 1):E105-E130.
31. Kang H.J., Kawasawa Y.I., Cheng F., Zhu Y., Xu X., Li M., Sousa A.M., Pletikos M., Meyer K.A., Sedmak G., Guennel T., Shin Y., Johnson M.B., Krsnik Z., Mayer S., Fertuzinhos S., Umlauf S., Lisgo S.N., Vortmeyer A., Weinberger D.R., Mane S., Hyde T.M., Huttner A., Reimers M., Kleinman J.E., Sestan N. Spatio-temporal transcriptome of the human brain. Nature 2011, 478:483-489.
32. Kostovic I., Jovanov-Milosevic N. The development of cerebral connections during the first 20-45 weeks' gestation. Semin. Fetal Neonatal Med. 2006, 11:415-422.
33. Kostovic I., Rakic P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 1990, 297:441-470.
34. Kostović I., Jovanov-Milošević N., Radoš M., Sedmak G., Benjak V., Kostović-Srzentić M., Vasung L., Culjat M., Radoš M., Hüppi P., Judaš M. Perinatal and early postnatal reorganization of the subplate and related cellular compartments in the human cerebral wall as revealed by histological and MRI approaches. Brain Struct. Funct. 2014, 219:231-253.
35. Kunz N., Zhang H., Assaf Y., Lazeyras F., Alexander D., Huppi P.S. Brain Microstructure Assessed by CHARMED and NODDI in the Newborn 2013, 0796. In: Proceedings of the 21st International Society for Magnetic Resonance in Medicine, Utah.
36. LaMantia A.S., Rakic P. Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. J. Neurosci. 1990, 10:2156-2175.
37. Lopez-Bendito G., Cautinat A., Sanchez J.A., Bielle F., Flames N., Garratt A.N., Talmage D.A., Role L.W., Charnay P., Marin O., Garel S. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 2006, 125:127-142.
38. Metin C., Godement P. The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J. Neurosci. 1996, 16:3219-3235.
39. Miller D.J., Duka T., Stimpson C.D., Schapiro S.J., Baze W.B., McArthur M.J., Fobbs A.J., Sousa A.M., Sestan N., Wildman D.E., Lipovich L., Kuzawa C.W., Hof P.R., Sherwood C.C. Prolonged myelination in human neocortical evolution. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16480-16485.
40. 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.P., Conturo T.E. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 1998, 209:57-66.
41. Panagiotaki E., Schneider T., Siow B., Hall M.G., Lythgoe M.F., Alexander D.C. Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage 2012, 59:2241-2254.
42. Partridge S.C., Mukherjee P., Henry R.G., Miller S.P., Berman J.I., Jin H., Lu Y., Glenn O.A., Ferriero D.M., Barkovich A.J., Vigneron D.B. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 2004, 22:1302-1314.
43. 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, 54:255-266.
44. Penny W.D. Comparing dynamic causal models using AIC, BIC and free energy. Neuroimage 2012, 59:319-330.
45. Perlman J.M. White matter injury in the preterm infant: an important determination of abnormal neurodevelopment outcome. Early Hum. Dev. 1998, 53:99-120.
46. Pierpaoli C., Jezzard P., Basser P.J., Barnett A., Di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology 1996, 201:637-648.
47. Provenzale J.M., Isaacson J., Chen S., Stinnett S., Liu C. Correlation of apparent diffusion coefficient and fractional anisotropy values in the developing infant brain. AJR Am. J. Roentgenol. 2010, 195:W456-W462.
48. Reese T.G., Heid O., Weisskoff R.M., Wedeen V.J. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn. Reson. Med. 2003, 49:177-182.
49. 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.
50. Szafer A., Zhong J., Gore J.C. Theoretical model for water diffusion in tissues. Magn. Reson. Med. 1995, 33:697-712.
51. Vasung L., Huang H., Jovanov-Milošević N., Pletikos M., Mori S., Kostović I. Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging. J. Anat. 2010, 217:400-417.
52. Vasung L., Jovanov-Milošević N., Pletikos M., Mori S., Judaš M., Kostović I. Prominent periventricular fiber system related to ganglionic eminence and striatum in the human fetal cerebrum. Brain Struct. Funct. 2011, 215:237-253.
53. Vasung L., Fischi-Gomez E., Hüppi P.S. Multimodality evaluation of the pediatric brain: DTI and its competitors. Pediatr. Radiol. 2013, 43:60-68.
54. Wang Y., Gupta A., Liu Z., Zhang H., Escolar M.L., Gilmore J.H., Gouttard S., Fillard P., Maltbie E., Gerig G., Styner M. DTI registration in atlas based fiber analysis of infantile Krabbe disease. Neuroimage 2011, 55:1577-1586.
55. Winston G.P., Micallef C., Symms M.R., Alexander D.C., Duncan J.S., Zhang H. Advanced diffusion imaging sequences could aid assessing patients with focal cortical dysplasia and epilepsy. Epilepsy Research 2014, 108:336-339.
56. Yakovlev P.A., Lecours I.R. The myelogenetic cycles of regional maturation of the brain. Regional Development of the Brain in Early Life 1967, Blackwell, Oxford. A. Minkowski (Ed.).
57. 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, 10:764-785.
58. Zhang H., Hubbard P.L., Parker G.J.M., Alexander D.C. Axon diameter mapping in the presence of orientation dispersion with diffusion MRI. Neuroimage 2011, 56:1301-1315.
59. 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.