Structure of the fetal brain: What we are learning from diffusion tensor imaging

Neuroscientist

Volumn 16, Issue 6, 2010, Pages 634-649

  Huang, Hao ^a  

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

Author keywords

development; DTI; fetal brain; neonate; premature; structure

Indexed keywords

BRAIN; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN STEM; CONTRAST ENHANCEMENT; DIFFUSION COEFFICIENT; DIFFUSION TENSOR IMAGING; ENCEPHALOMALACIA; FRACTIONAL ANISOTROPY; HISTOLOGY; HUMAN; NERVE TRACT; NEUROIMAGING; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; PYRAMIDAL TRACT; REVIEW; WHITE MATTER;

BRAIN; DIFFUSION TENSOR IMAGING; HUMANS; INFANT, NEWBORN; INFANT, PREMATURE; REFERENCE STANDARDS;

EID: 78651518138     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858409356711     Document Type: Review

References (71)

1. Alexander DC 2005. Multiple-fiber reconstruction algorithms for diffusion MRI. Ann NY Acad Sci 1064: 113-33.
2. Barkovich AJ 2000. Pediatric neuroimaging. Philadelphia: Lippincott Wiliams & Wilkins.
3. Basser PJ, Jones DK 2002. Diffusion-tensor MRI: theory, experimental design and data analysis. A technical review. NMR Biomed 15: 456-67.
4. Basser PJ, Mattiello J., Le Bihan D. 1994. MR diffusion tensor spectroscopy and imaging, Biophys J 66: 259-67.
5. Basser PJ, Pajevic S., Pierpaoli C., Duda J., Aldroubi A. 2000. In vivo fiber tractography using DT-MRI data. Magn Reson Med 44: 625-32.
6. Bayer SA, Altman J. 2004. The human brain during the third trimester. Boca Raton (FL): CRC.
7. Bayer SA, Altman J. 2005. The human brain during the second trimester. Boca Raton (FL): CRC.
8. Beaulieu C. 2002. The basis of anisotropic water diffusion in the nervous system: a technical review. NMR Biomed 15: 435-55.
9. Beaulieu C., Allen PS 1994. Determinants of anisotropic water diffusion in nerves. Magn Reson Med 31: 394-400.
10. Behrens TE, Berg HJ, Jbabdi S., Rushworth MF, Woolrich MW 2006. Probabilistic diffusion tractography can add in clinical neuroscience. Curr Opin Neurol 19: 379-85.
11. Catani M., Howard RJ, Pajevic S., Jones DK 2002. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17: 77-94.
12. Chenevert TL, Brunberg JA, Pipe JG 1990. Anisotropic diffusion in human white matter: demonstration with MR technique in vivo. Radiology 177: 401-5.
13. Conturo TE, Lori NF, Cull TS, Akbudak E., Snyder AZ, Shimony JS, and others. 1999. Tracking neuronal fiber pathways n the living human brain. Proc Natl Acad Sci USA 96: 10422-7.
14. deIpolyi AR, Mukherjee P., Gill K., Henry RG, Partridge SC, Veeraraghavan S., and others. 2005. Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. NeuroImage 27: 579-86.
15. Frank LR 2001. Anisotropy in high angular resolution diffusion-weighted MRI. Magn Reson Med 45: 935-9.
16. Haynes RL, Borenstein NS, Desilva TM, Folkerth RD, Liu LG, Volpe JJ, and others. 2005. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol 484: 156-67.
17. Honig LS, Herrmann K., Shatz CJ 1996. Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb Cortex 6: 794-806.
18. Hoon AH Jr, Lawrie WT Jr, Melhem ER, Reinhardt EM, van Zijl PCM, Solaiyappan M., and others. 2002. Diffusion tensor imaging of periventricular leukomalacia shows affected sensory cortex white matter pathways. Neurology 59: 752-6.
19. Horsfield MA, Jones DK 2002. Application of diffusion weighted and diffusion tensor MRI to white matter diseases. NMR Biomed 15: 570-7.
20. Hsu EW, Mori S. 1995. Analytical interpretations of NMR diffusion measurement in an anisotropic medium and a simplified method for determining fiber orientation. Magn Reson Med 34: 194-200.
21. Huang H., Xue R., Zhang J., Ren T., Richards LJ, Yarowsky P., and others. 2009. Anatomical characterization of human fetal brain development with diffusion tensor MRI. J Neurosci 29: 4263-73.
22. Huang H., Zhang J., Wakana S., Zhang W., Ren T., Richards LJ, and others. 2006. White and gray matter development in human fetal, newborn and pediatric brains. Neuroimage 33: 27-38.
23. Huppi PS, Inder TE 2001. Magnetic resonance techniques in the evaluation of the perinatal brain: recent advances and future directions. Semin Neonatol 6: 195-210.
24. Huppi PS, Maier S., Peled S., Zientara G., Barnes P., Jolesz F., and others. 1998. Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44: 584-90.
25. Huppi PS, Murphy B., Maier SE, Zientara GP, Inder TE, Barnes PD, and others. 2001. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107: 455-60.
26. Jones DK, Simmons A., Williams SC, Horsfield MA 1999. Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 42: 37-41.
27. Kostovic I., Judas M., Rados M., Hrabac P. 2002. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12: 536-44.
28. Lazar M., Weinstein DM, Tsuruda JS, Hasan KM, Arfanakis K., Meyerand ME, and others. 2003. White matter tractography using diffusion tensor deflection. Hum Brain Mapp 18: 306-21.
29. Le Bihan D., Breton E., Lallemand D., Grenier P., Cabanis E., Laval-Jeantet M. 1986. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161: 401-7.
30. Maas LC, Mukherjee P., Carballido-Gamio J., Veeraraghavan S., Miller SP, Partridge SC, and others. 2004. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22: 1134-40.
31. Makris N., Worth AJ, Sorensen AG, Papadimitriou GM, Reese TG, Wedeen VJ, and others. 1997. Morphometry of in vivo human white matter association pathways with diffusion weighted magnetic resonance imaging. Ann Neurol 42: 951-62.
32. McKinstry RC, Mathur A., Miller JH, Ozcan A., Snyder AZ, Schefft GL, and others. 2002. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex 12: 1237-43.
33. Miller SP, Vigneron DB, Henry RG, Bohland MA, Ceppi-Cozzio C., Hoffman C., and others. 2002. Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging 16: 621-32.
34. Mori S., Crain BJ, Chacko VP, van Zijl PCM. 1999. Three dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annal Neurol 45: 265-9.
35. Mori S., Itoh R., Zhang J., Kaufmann WE, van Zijl PCM, Solaiyappan M., and others. 2001. Diffusion tensor imaging of the developing mouse brain. Magn Reson Med 46: 18-23. (Pubitemid 32592134)
36. Mori S., Wakana S., Nagae-Poetscher LM, van Zijl PC 2005. MRI atlas of human white matter. Amsterdam, the Netherlands: Elsevier.
37. Mori S., Zhang J. 2006. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51: 527-39.
38. Moseley ME, Cohen Y., Kucharczyk J., Mintorovitch J., Asgari HS, Wendland MF, and others. 1990. Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology 176: 439-45.
39. Mountcastle VB 1997. The columnar organization of the neocortex. Brain 120: 701-22.
40. Mukherjee P., Miller JH, Shimony JS, Philip JV, Nehra D., Snyder AZ, and others. 2002. Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol 23: 1445-56.
41. Neil JJ, Miller J., Mukherjee P., Huppi PS 2002. Diffusion tensor imaging of normal and injured developing human brain-a technical review. NMR Biomed 15: 543-52.
42. Neil JJ, Shiran S., McKinstry R., Schefft G., Snyder A., Almli C., and others. 1998. Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209: 57-66.
43. O'Rahilly R., Múller F. 2006. Embryonic human brain: an atlas of developmental stages. Hoboken (NJ): John Wiley & Sons Inc.
44. Pajevic S., Pierpaoli C. 1999. Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain. Magn Reson Med 42: 526-40.
45. Parker GJ, Wheeler-Kingshott CAM, Barker GJ 2002. Estimating distributed anatomical connectivity using fast marching methods and diffusion tensor imaging. IEEE Trans Med Imaging 21: 505-12.
46. Partridge SC, Mukherjee P., Henry RG, Miller SP, Berman JI, Jin H., and others. 2004. Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22: 1302-14.
47. Pierpaoli C., Basser PJ 1996. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36: 893-906.
48. Pierpaoli C., Jezzard P., Basser PJ, Barnett A., Di Chiro G. 1996. Diffusion tensor MR imaging of human brain. Radiology 201: 637-48.
49. Poupon C., Clark CA, Frouin V., Regis J., Bloch L., Le Bihan D., and others. 2000. Regularization of diffusion-based direction maps for the tracking of brain white matter fascicules. Neuroimage 12: 184-95.
50. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145: 61-83.
51. Rakic P. 1988. Specification of cerebral cortical areas. Science 241: 170-6.
52. Ren T., Anderson A., Shen WB, Huang H., Plachez C., Zhang J., and others. 2006. Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat Rec A Discov Mol Cell Evol Biol 288: 191-204.
53. Rilling JK, Glasser MF, Preuss TM, Ma X., Zhao T., Hu X., and others. 2008. The evolution of te arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11: 426-8.
54. Sidman RL, Rakic P. 1973. Neuronal migration, with specific reference to developing human brain: a review. Brain Res 62: 1-35.
55. Sidman RL, Rakic P. 1982. Development of the human central nervous system. In: Haymaker W, Adams RD, editors. Histology and histopathology of the nervous system. Spring-field (IL): C. C. Thomas. p 3-145.
56. Stejskal EO, Tanner JE 1965. Spin diffusion measurement: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42: 288.
57. Stieltjes B., Kaufmann WE, van Zijl PCM, Fredericksen K., Pearlson GD, Mori S. 2001. Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14: 723-35.
58. Sun SW, Liang HF, Trinkaus K., Cross AH, Armstrong RC, Song SK 2006. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 55: 302-8.
59. Sun SW, Neil JJ, Liang HF, He YY, Schmidt RE, Hsu CY, and others. 2005. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infracted brain. Magn Reson Med 53: 1447-51.
60. Thomas B., Eyssen M., Peeters R., Molenaers G., Van Hecke P., De Cock P., and others. 2005. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 128: 2562-77.
61. Thornton JS, Ordidge RJ, Penrice J., Cady EB, Amess PN, Punwani S., and others. 1997. Anisotropic water diffusion in white and gray matter on the neonatal piglet brain before and after transient hypoxia-ischaemia. Magn Res Imaging 15: 433-40.
62. Tiedemann F. 1816. Anatomie und bildungsgeschichte des gehirns im foetus des menschen. Núrnberg: Steinische Buchhandlung.
63. Tournier JD, Calamante F., Gadian DG, Connelly A. 2004. Direct estimation of the fiber orientation density function from diffusion-weighed MRI data using spherical deconvolution. NeuroImage 23: 1176-85.
64. Tuch DS 2004. Q-ball imaging. Magn Reson Med 52: 1358-72.
65. Tuch DS, Reese TG, Wiegell MR, Wedeen VJ 2003. Diffusion MRI of complex neural architecture. Neuron 40: 885-95.
66. Turner R., Le Bihan D., Maier J., Vavrek R., Hedges LK, Pekar J. 1990. Echo-planar imaging of intravoxel incoherent motion. Radiology 177: 407-14.
67. Volpe JJ 2001. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50: 553-62.
68. Wakana S., Jiang H., Nagae-Poetscher LM, Van Zijl PC, Mori S. 2004. Fiber tract-based atlas of human white matter anatomy. Radiology 230: 77-87.
69. Wedeen VJ, Hagmann P., Tseng WY, Reese TG, Weisskoff RM 2005. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54: 1377-86.
70. Zhang J., Evans A., Hermoye L., Lee SK, Wakana S., Zhang W., and others. 2007. Evidence of slow maturation of the superior longitudinal fasciculus in early childhood by diffusion tensor imaging. NeuroImage 38: 239-47.
71. Zhang J., Richards LJ, Yarowsky P., Huang H., van Zijl PC, Mori S. 2003. Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor micro-imaging. Neuroimage 20: 1639-48.