Radial coherence of diffusion tractography in the cerebral white matter of the human fetus: Neuroanatomic insights

Cerebral Cortex

Volumn 24, Issue 3, 2014, Pages 579-592

  Xu, Gang ^a   Takahashi, Emi ^a,b   Folkerth, Rebecca D ^a,c   Haynes, Robin L ^a   Volpe, Joseph J ^d   Grant, P Ellen ^a,b   Kinney, Hannah C ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Department of Neurology ^*  (United States)

Author keywords

axons; blood vessels; encephalopathy of prematurity; periventricular leukomalacia; radial glial fibers; vimentin

Indexed keywords

AXONS; BLOOD VESSELS; ENCEPHALOPATHY OF PREMATURITY; PERIVENTRICULAR LEUKOMALACIA; RADIAL GLIAL FIBERS; VIMENTIN;

AGE FACTORS; ANTIGENS, CD31; BRAIN MAPPING; CEREBRAL CORTEX; DIFFUSION MAGNETIC RESONANCE IMAGING; FETUS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROTUBULE-ASSOCIATED PROTEINS; NERVE FIBERS, MYELINATED; NEUROFILAMENT PROTEINS; NEUROGLIA; VIMENTIN;

EID: 84894264498     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs330     Document Type: Article

References (51)

1. Andiman SE, Haynes RL, Trachtenberg FL, Billiards SS, Folkerth RD, Volpe JJ, Kinney HC. 2010. The cerebral cortex overlying periventricular leukomalacia: analysis of pyramidal neurons. Brain Pathol. 20:803-814.
2. Banker BQ, Larroche JC. 1962. Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch Neurol. 7:386-410.
3. Bertossi M, Virgintino D, Errede M, Roncali L. 1999. Immunohistochemical and ultrastructural characterization of cortical plate microvasculature in the human fetus telencephalon. Microvasc Res. 58:49-61.
4. Brown MJ, Hallam JA, Colucci-Guyon E, Shaw S. 2001. Rigidity of Circulating Lymphocytes Is Primarily Conferred by Vimentin Intermediate Filaments. J Immunol. 166:6640-6646.
5. Buxton R. 2003. Introduction to functional magnetic resonance imaging. Principles and techniques. Cambridge (UK): Cambridge University Press. p. 181-183.
6. Campbell K, Gotz M. 2002. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25:235-238.
7. Catani M, Thiebaut de Schotten M. 2008. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex. 44:1105-1132.
8. Chiu IM, Touhalisky K, Liu Y, Yates A, Frostholm A. 2000. Tumorigenesis in transgenic mice in which the SV40 T antigen is driven by the brain-specific FGF1 promoter. Oncogene. 19:6229-6239.
9. D'Arceuil H, Liu C, Levitt P, Thompson B, Kosofsky B, de Crespigny A. 2008. Three dimensional high-resolution diffusion tensor imaging and tractography of the developing rabbit brain. Dev Neurosci. 30:262-275.
10. De Azevedo LC, Fallet C, Moura-Neto V, Daumas-Duport C, Hedin-Pereira C, Lent R. 2003. Cortical radial glial cells in human fetuses: depth-corrected transformation into astrocytes. J Neurobiol. 55:288-298.
11. Fazzi E, Bova S, Giovenzana A, Signorini S, Uggetti C, Bianchi P. 2009. Cognitive visual dysfunctions in preterm children with periventricular leukomalacia. Dev Med Child Neurol. 51:974-981.
12. Gray GE, Sane JR. 1992. Lineage of radial glia in the chicken optic tectum. Development. 114:271-283.
13. Gilles FH, Dooling E, Fulchicro A. 1976. Sequence of myelination in the human fetus. Tran Am Neurol Assoc. 101:244-246.
14. Haynes RL, Borenstein NS, DeSilva TM, Folkerth RD, Liu LG, Volpe JJ, Kinney HC. 2005. Axonal development in the cerebral white matter of the human fetus and infant. J Comp Neurol. 484:156-167.
15. Hess CP, Mukherjee P, Han ET, Xu D, Vigneron DB. 2006. Q-ball reconstruction of multimodal fiber orientations using the spherical harmonic basis. Magn Reson Med. 56:104-117.
16. Hevner RF. 2000. Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol. 59:385-392.
17. Honig LS, Herrmann K, Shatz CJ. 1996. Developmental changes revealed by immunohistochemical markers in human cerebral cortex. Cereb Cortex. 6:794-806.
18. Huang H, Xue R, Zhang J, Ren T, Richards L, Yarowsky P, Miller MIS, Mori S. 2009. Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci. 29:4263-4273.
19. Huang H, Zhang J, Wakana S, Zhang W, Ren T, Richards L, Yarowsky P, Donohue P, Graham E, van Zjil PCM, Mori S. 2006. White and gray matter development in human fetal, newborn and pediatric brains. NeuroImage. 33:27-38.
20. Kinney HC. 2009. The encephalopathy of prematurity: one pediatric neuropathologist's perspective. Semin Pediatr Neurol. 16:179-190.
21. Kinney HC, Volpe JJ. 2009. "Perinatal Panencephalopathy in the Premature Infant: Is It due to Hypoxia-Ischemia?" In: Haddad GG, Ping Yu S, editors. Perinatal Brain Hypoxia and Ischemia. Contemporary Clinical Neuroscience. New York (NY): Humana Press. p 153-185.
22. Kostovic I, Judas M. 2002. Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec. 267:1-6.
23. Letinic K, Rakic P. 2001. Telencephalic origin of human thalamic GABAergic neurons. Nat Neurosci. 4:931-936.
24. Lu P, Li L, Kuno K, Wu Y, Baba T, Li YY, Zhang X, Mukaida N. 2008. Protective roles of the fractalkine/CX3CL1-CX3CR1 interactions in alkali-induced corneal neovascularization through enhanced antiangiogenic factor expression. J Immunol. 180:4283-4291.
25. Marin-Padilla M. 2011. The Human Brain: Prenatal Development and Structure. Heidelberg (Germany): Springer. p. 1-145.
26. McLendon RE, Burger PC, Pegram CN, Eng LF, Bigner DD. 1986. The immunohistochemical application of three anti-GFAP monoclonal antibodies to formalin-fixed, paraffin-embedded, normal and neoplastic brain tissues. J Neuropathol Exp Neurol. 45:692-703.
27. McNab JA, Jbabdi S, Deoni SC, Douaud G, Behrens TE, Miller KL. 2009. High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. Neuroimage. 46(3):775-785.
28. McNab JA, Miller KL. 2008. Sensitivity of diffusion weighted steady state free precession to anisotropic diffusion. Magn Reson Med. 60 (2):405-413.
29. Mori S, Crain BJ, Chacko VP, van Zijl PC. 1999. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol. 45:265-269.
30. Mori S, Van Zijl PCM, Wakana S. 2005. MRI Atlas of Human White Matter. Amsterdam (The Netherlands): Elsevier Science & Technology.
31. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature. 409:714-720.
32. Rakic P. 2006. A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex. Suppl 1: i3-i17.
33. Rakic P. 1988. Specification of cerebral cortical areas. Science. 241:170-176.
34. Rakic P, Ayoub AE, Breunig JJ, Dominguez MH. 2009. Decision by division: making cortical maps. Trends Neurosci. 32:291-301.
35. Rubenstein JL. 2011. Annual research review: development of the cerebral cortex: implications for neurodevelopmental disorders. J Child Psychol Psychiatry. 52:339-355.
36. Schmahmann JD, Pandya DN, Wang R, Dai G, D'Arceuil HE, de Crespigny AJ, Wedeen VJ. 2007. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain. 130:630-653.
37. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP. 2004. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci USA. 101:10901-10906.
38. Shemesh N, Cohen Y. 2011. Microscopic and compartment shape anisotropies in gray and white matter revealed by angular bipolar double-PFG MR. Magn Reson Med. 65:1216-12127.
39. Steindler DA. 1993. Glial boundaries in the developing nervous system. Annu Rev Neurosci. 16:445-470.
40. Takahashi E, Dai G, Rosen GD, Wang R, Ohki K, Folkerth RD, Galaburda A, Wedeen VJ, Grant PE. 2011. Developing neocortex organization and connectivity in cats revealed by direct correlation of diffusion tractography and histology. Cereb Cortex. 21:200-211.
41. Takahashi E, Dai G, Wang R, Ohki K, Rosen GD, Galaburda A, Grant PE, Wedeen VJ. 2010. Development of cerebral fiber pathways in cats revealed by diffusion spectrum imaging. Neuroimage. 49:1231-1240.
42. Takahashi E, Folkerth RD, Galaburda A, Grant PE. 2012. Emerging cerebrain connectivity in the human fetal brain: an MR tractography study. Cereb Cortex. 22:455-464.
43. Tuch DS, Reese TG, Wiegell MR, Wedeen VJ. 2003. Diffusion MRI of complex neural architecture. Neuron. 40:885-895.
44. Ulfig N, Briese M. 2004. Evidence for the presence of the sphingosine-1-phosphate receptor Edg-8 in human radial glial fibers. Acta Histochem. 106:373-378.
45. Virgintino D, Maiorano E, Errede M, Vimercati A, Greco P, Selvaggi L, Roncali L, Bertossi M. 1998. Astroglia-microvessel relationship in the developing human telencephalon. Int J Dev Biol. 42:1165-1168.
46. Vishwas M, Chitnis T, Pienaar R, Healy BC, Grant PE. 2010. Tract based analysis of callosal, projection and association pathways in pediatric patients with multiple sclerosis: a preliminary study. Am J Neuroradiol. 31:121-128.
47. Volpe JJ. 2001. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res. 50:553-562.
48. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA. 2011. The developing oligodendrocyte: key cellular target of brain injury in the premature infant. Int J Dev Neurosci. 29:423-440.
49. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D'Arceuil H, de Crespigny AJ. 2008. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage. 41:1267-1277.
50. Xu G, Broadbelt KG, Haynes RL, Folkerth RD, Borenstein NS, Belliveau RA, Trachtenberg FS, Volpe JJ, Kinney HC. 2011. Late development of the GABAergic system in the human cerebral cortex. J Neuropathol Exp Neurol. 70:841-858.
51. Zhang J, Evans A, Hermoye L, Lee SK, Wakana S, Zhang W, Donohue P, Miller MI, Huang H, Wang X, van Zijl PC, Mori S. 2007. Evidence of slow maturation of the superior longitudinal fasciculus in early childhood by diffusion tensor imaging. Neuroimage. 38:239-247.