Sonographic assessment of normal and abnormal patterns of fetal cerebral lamination

Ultrasound in Obstetrics and Gynecology

Volumn 40, Issue 6, 2012, Pages 642-651

  Pugash, D ^a   Hendson, G ^a   Dunham, C P ^a   Dewar, K ^b   Money, D M ^a   Prayer, D ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BC Women's Hospital   (Canada)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

cerebral lamination; cortical development; cytomegalovirus; fetal magnetic resonance imaging; fetal white matter; intermediate zone; lissencephaly; malformations of cortical development; prenatal ultrasound; subplate zone

Indexed keywords

ARTICLE; BRAIN; BRAIN DISEASE; CONGENITAL MALFORMATION; ECHOGRAPHY; FETUS; FETUS DEVELOPMENT; FETUS ECHOGRAPHY; GESTATIONAL AGE; HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETROSPECTIVE STUDY;

BRAIN DISEASES; CEREBRUM; FETAL DEVELOPMENT; FETUS; GESTATIONAL AGE; HUMANS; MAGNETIC RESONANCE IMAGING; RETROSPECTIVE STUDIES; ULTRASONOGRAPHY, PRENATAL;

EID: 84866090925     PISSN: 09607692     EISSN: 14690705     Source Type: Journal    
DOI: 10.1002/uog.11164     Document Type: Article

References (59)

1. Rakic P,. Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 2003; 13: 541-549.
2. Volpe JJ,. Encephalopathy of prematurity includes neuronal abnormalities. Pediatrics 2005; 116: 221-225.
3. McQuillen PS, Ferriero DM,. Perinatal subplate neuron injury: implications for cortical development and plasticity. Brain Pathol 2005; 15: 250-260.
4. Toi A, Lister WS, Fong KW,. How early are fetal cerebral sulci visible at prenatal ultrasound and what is the normal pattern of early fetal sulcal development? Ultrasound Obstet Gynecol 2004; 24: 706-715.
5. Garel C, Chantrel E, Elmaleh M, Brisse H, Sebag G,. Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst 2003; 19: 422-425.
6. Kostovic I, Judas M, Rados M, Hrabac P,. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 2002; 12: 536-544.
7. Rados M, Judas M, Kostovic I,. In vitro MRI of brain development. Eur J Radiol 2006; 57: 187-198.
8. Kostovic I, Judas M, Rados M, Hrabac P,. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 2002; 12: 536-544.
9. Pearlman AL, Sheppard AM,. Extracellular matrix in early cortical development. Prog Brain Res 1996; 108: 117-134.
10. Margolis RU, Margolis RK,. Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res 1997; 290: 343-348.
11. Sheppard AM, Hamilton SK, Pearlman AL,. Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. J Neurosci 1991; 11: 3928-3942.
12. Bicknese AR, Sheppard AM, O'Leary DD, Pearlman AL,. Thalamocortical axons extend along a chondroitin sulfate proteoglycan-enriched pathway coincident with the neocortical subplate and distinct from the efferent path. J Neurosci 1994; 14: 3500-3510.
13. Miller B, Sheppard AM, Bicknese AR, Pearlman AL,. Chondroitin sulfate proteoglycans in the developing cerebral cortex: the distribution of neurocan distinguishes forming afferent and efferent axonal pathways. J Comp Neurol 1995; 355: 615-628.
14. Emerling DE, Lander AD,. Inhibitors and promoters of thalamic neuron adhesion and outgrowth in embryonic neocortex: functional association with chondroitin sulfate. Neuron 1996; 17: 1089-1100.
15. Kostovic I,. Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. Prog Brain Res 1990; 85: 223-239; discussion 39-40.
16. Ayoub AE, Kostovic I,. New horizons for the subplate zone and its pioneering neurons. Cereb Cortex 2009; 19: 1705-1707.
17. Kanold PO, Luhmann HJ,. The subplate and early cortical circuits. Annu Rev Neurosci 2010; 33: 23-48.
18. Wang WZ, Hoerder-Suabedissen A, Oeschger FM, Bayatti N, Ip BK, Lindsay S, Supramaniam V, Srinivasan L, Rutherford M, Møllgård K, Clowry GJ, Molnár Z,. Subplate in the developing cortex of mouse and human. J Anat 2010; 217: 368-380.
19. Molliver ME, Kostovic I, van der Loos H,. The development of synapses in cerebral cortex of the human fetus. Brain Res 1973; 50: 403-407.
20. Kostovic I, Rakic P,. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 1980; 9: 219-242.
21. Rakic P,. Principles of neural cell migration. Experientia 1990; 46: 882-891.
22. Allendoerfer KL, Shatz CJ,. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci 1994; 17: 185-218.
23. Maas LC, Mukherjee P, Carballido-Gamio J, Veeraraghavan S, Miller SP, Partridge SC, Henry RG, Barkovich AJ, Vigneron DB,. Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 2004; 22: 1134-1140.
24. Brisse H, Fallet C, Sebag G, Nessmann C, Blot P, Hassan M,. Supratentorial parenchyma in the developing fetal brain: in vitro MR study with histologic comparison. AJNR Am J Neuroradiol 1997; 18: 1491-1497.
25. Childs AM, Ramenghi LA, Cornette L, Tanner SF, Arthur RJ, Martinez D, Levene MI,. Cerebral maturation in premature infants: quantitative assessment using MR imaging. AJNR Am J Neuroradiol 2001; 22: 1577-1582.
26. Prayer D, Brugger PC, and, Mittermayer C,. OC009: Assessment of intrauterine brain maturation using Diffusion Weighted Imaging. Ultrasound Obstet Gynecol 2003; 22 (Suppl 1): 3.
27. Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury JF, Sebag G, Hassan M,. Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJNR Am J Neuroradiol 2001; 22: 184-189.
28. Huppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD, Kikinis R, Jolesz FA, Volpe JJ,. Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 2001; 107: 455-460.
29. Garel C., MRI of the Fetal Brain: Normal Development and Cerebral Pathologies. Springer-Verlag: Berlin Heidelberg, 2004.
30. Garel C, Chantrel E, Elmaleh M, Brisse H, Sebag G,. Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst 2003; 19: 422-425.
31. Chong BW, Babcook CJ, Salamat MS, Nemzek W, Kroeker D, Ellis WG,. A magnetic resonance template for normal neuronal migration in the fetus. Neurosurgery 1996; 39: 110-116.
32. Girard NJ, Raybaud CA,. In vivo MRI of fetal brain cellular migration. J Comput Assist Tomogr 1992; 16: 265-267.
33. Prayer D, Kasprian G, Krampl E, Ulm B, Witzani L, Prayer L, Brugger PC,. MRI of normal fetal brain development. Eur J Radiol 2006; 57: 199-216.
34. Glenn OA, Barkovich AJ,. Magnetic resonance imaging of the fetal brain and spine: an increasingly important tool in prenatal diagnosis, part 1. AJNR Am J Neuroradiol 2006; 27: 1604-1611.
35. Widjaja E, Geibprasert S, Mahmoodabadi SZ, Blaser S, Brown NE, Shannon P,. Alteration of human fetal subplate layer and intermediate zone during normal development on MR and diffusion tensor imaging. AJNR Am J Neuroradiol 2010; 31: 1091-1099.
36. Kostovic I, Judas M,. Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 2002; 267: 1-6.
37. Widjaja E, Geibprasert S, Mahmoodabadi SZ, Brown NE, Shannon P,. Corroboration of normal and abnormal fetal cerebral lamination on postmortem MR imaging with postmortem examination. AJNR Am J Neuroradiol 2010; 31: 1987-1993.
38. Prayer D, Brugger PC, Kasprian G, Witzani L, Helmer H, Dietrich W, Eppel W, Langer M,. MRI of fetal acquired brain lesions. Eur J Radiol 2006; 57: 233-249.
39. Castillo M, Scatliff JH, Kwock L, Green JJ, Suzuki K, Chancellor K, Smith JK,. Postmortem MR imaging of lobar cerebral infarction with pathologic and in vivo correlation. Radiographics 1996; 16: 241-250.
40. McKinney AM, Teksam M, Felice R, Casey SO, Cranford R, Truwit CL, Kieffer S,. Diffusion-weighted imaging in the setting of diffuse cortical laminar necrosis and hypoxic-ischemic encephalopathy. AJNR Am J Neuroradiol 2004; 25: 1659-1665.
41. Fink AM, Hingston T, Sampson A, Ng J, Palma-Dias R,. Malformation of the fetal brain in thanatophoric dysplasia: US and MRI findings. Pediatr Radiol 2010; 40 (Suppl 1): S134-S137.
42. Miller E, Blaser S, Shannon P, Widjaja E,. Brain and bone abnormalities of thanatophoric dwarfism. AJR Am J Roentgenol 2009; 192: 48-51.
43. McLendon RE, Crain BJ, Oakes WJ, Burger PC,. Cerebral polygyria in the Chiari Type II (Arnold-Chiari) malformation. Clin Neuropathol 1985; 4: 200-205.
44. Wolpert SM, Anderson M, Scott RM, Kwan ES, Runge VM,. Chiari II malformation: MR imaging evaluation. AJR Am J Roentgenol 1987; 149: 1033-1042.
45. Miller E, Widjaja E, Blaser S, Dennis M, Raybaud C,. The old and the new: supratentorial MR findings in Chiari II malformation. Childs Nerv Syst 2008; 24: 563-575.
46. Landrieu P, Husson B, Pariente D, Lacroix C,. MRI-neuropathological correlations in type 1 lissencephaly. Neuroradiology 1998; 40: 173-176.
47. Pilz D, Stoodley N, Golden JA,. Neuronal migration, cerebral cortical development, and cerebral cortical anomalies. J Neuropathol Exp Neurol 2002; 61: 1-11.
48. Prayer D,. Indications for, fetal MRI,. In Fetal MRI, Prayer D, (ed). Springer-Verlag: Berlin Heidelberg, 2011; 1-17.
49. Marques Dias MJ, Harmant-van Rijckevorsel G, Landrieu P, and Lyon G. Prenatal cytomegalovirus disease and cerebral microgyria: evidence for perfusion failure, not disturbance of histogenesis, as the major cause of fetal cytomegalovirus encephalopathy. Neuropediatrics 1984; 15: 18.
50. Perlman JM, Argyle C,. Lethal cytomegalovirus infection in preterm infants: clinical, radiological, and neuropathological findings. Ann Neurol 1992; 31: 64-68.
51. Odeberg J, Wolmer N, Falci S, Westgren M, Seiger A, Soderberg-Naucler C,. Human cytomegalovirus inhibits neuronal differentiation and induces apoptosis in human neural precursor cells. J Virol 2006; 80: 8929-8939.
52. Shinmura Y, Kosugi I, Aiba-Masago S, Baba S, Yong LR, Tsutsui Y,. Disordered migration and loss of virus-infected neuronal cells in developing mouse brains infected with murine cytomegalovirus. Acta Neuropathol 1997; 93: 551-557.
53. Barkovich AJ, Lindan CE,. Congenital cytomegalovirus infection of the brain: imaging analysis and embryologic considerations. AJNR Am J Neuroradiol 1994; 15: 703-715.
54. Malinger G, Lev D, Zahalka N, Ben Aroia Z, Watemberg N, Kidron D, Sira LB, Lerman-Sagie T. Fetal cytomegalovirus infection of the brain: the spectrum of sonographic findings. AJNR Am J Neuroradiol 2003; 24: 28-32.
55. de Vries LS, Gunardi H, Barth PG, Bok LA, Verboon-Maciolek MA, Groenendaal F,. The spectrum of cranial ultrasound and magnetic resonance imaging abnormalities in congenital cytomegalovirus infection. Neuropediatrics 2004; 35: 113-119.
56. Hilgetag CC, Barbas H,. Developmental mechanics of the primate cerebral cortex. Anat Embryol (Berl) 2005; 210: 411-417.
57. Guibaud L, Selleret L, Larroche JC, Buenerd A, Alias F, Gaucherand P, Des Portes V, Pracros JP. Abnormal Sylvian fissure on prenatal cerebral imaging: significance and correlation with neuropathological and postnatal data. Ultrasound Obstet Gynecol 2008; 32: 50-60.
58. Fong KW, Ghai S, Toi A, Blaser S, Winsor EJ, Chitayat D,. Prenatal ultrasound findings of lissencephaly associated with Miller-Dieker syndrome and comparison with pre- and postnatal magnetic resonance imaging. Ultrasound Obstet Gynecol 2004; 24: 716-723.
59. Malinger G, Lev D, Lerman-Sagie T,. Abnormal sulcation as an early sign for migration disorders. Ultrasound Obstet Gynecol 2004; 24: 704-705.