Display options
Share it on

Front Neuroanat. 2016 Feb 24;10:11. doi: 10.3389/fnana.2016.00011. eCollection 2016.

Quantitative and Qualitative Analysis of Transient Fetal Compartments during Prenatal Human Brain Development.

Frontiers in neuroanatomy

Lana Vasung, Claude Lepage, Milan Radoš, Mihovil Pletikos, Jennifer S Goldman, Jonas Richiardi, Marina Raguž, Elda Fischi-Gómez, Sherif Karama, Petra S Huppi, Alan C Evans, Ivica Kostovic

Affiliations

  1. Department of Developmental Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of ZagrebZagreb, Croatia; Division of Development and Growth, Department of Pediatrics, University of GenevaGeneva, Switzerland.
  2. Ludmer Centre for Neuroinformatics, McGill Centre for Integrative Neuroscience, Department of Biomedical Engineering, Montreal Neurological Institute, Montreal, McGill University Montreal, QC, Canada.
  3. Department of Developmental Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb Zagreb, Croatia.
  4. Department of Developmental Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of ZagrebZagreb, Croatia; Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of MedicineNew Haven, CT, USA.
  5. Laboratory of Neurology and Imaging of Cognition, Department of Neuroscience, University of Geneva Geneva, Switzerland.
  6. Division of Development and Growth, Department of Pediatrics, University of Geneva Geneva, Switzerland.

PMID: 26941612 PMCID: PMC4764715 DOI: 10.3389/fnana.2016.00011

Abstract

The cerebral wall of the human fetal brain is composed of transient cellular compartments, which show characteristic spatiotemporal relationships with intensity of major neurogenic events (cell proliferation, migration, axonal growth, dendritic differentiation, synaptogenesis, cell death, and myelination). The aim of the present study was to obtain new quantitative data describing volume, surface area, and thickness of transient compartments in the human fetal cerebrum. Forty-four postmortem fetal brains aged 13-40 postconceptional weeks (PCW) were included in this study. High-resolution T1 weighted MR images were acquired on 19 fetal brain hemispheres. MR images were processed using in-house software (MNI-ACE toolbox). Delineation of fetal compartments was performed semi-automatically by co-registration of MRI with histological sections of the same brains, or with the age-matched brains from Zagreb Neuroembryological Collection. Growth trajectories of transient fetal compartments were reconstructed. The composition of telencephalic wall was quantitatively assessed. Between 13 and 25 PCW, when the intensity of neuronal proliferation decreases drastically, the relative volume of proliferative (ventricular and subventricular) compartments showed pronounced decline. In contrast, synapse- and extracellular matrix-rich subplate compartment continued to grow during the first two trimesters, occupying up to 45% of telencephalon and reaching its maximum volume and thickness around 30 PCW. This developmental maximum coincides with a period of intensive growth of long cortico-cortical fibers, which enter and wait in subplate before approaching the cortical plate. Although we did not find significant age related changes in mean thickness of the cortical plate, the volume, gyrification index, and surface area of the cortical plate continued to exponentially grow during the last phases of prenatal development. This cortical expansion coincides developmentally with the transformation of embryonic cortical columns, dendritic differentiation, and ingrowth of axons. These results provide a quantitative description of transient human fetal brain compartments observable with MRI. Moreover, they will improve understanding of structural-functional relationships during brain development, will enable correlation between in vitro/in vivo imaging and fine structural histological studies, and will serve as a reference for study of perinatal brain injuries.

Keywords: cerebral cortex; cortical plate; human fetal brain; subplate

References

  1. Brain Res. 1978 Sep 8;152(3):451-85 - PubMed
  2. Neuroimage. 2004 Sep;23(1):84-97 - PubMed
  3. Neuroimage. 2011 Feb 14;54(4):2750-63 - PubMed
  4. Stain Technol. 1978 Mar;53(2):107-12 - PubMed
  5. J Comp Neurol. 1992 Feb 22;316(4):485-96 - PubMed
  6. Nature. 2011 Oct 26;478(7370):483-9 - PubMed
  7. Cereb Cortex. 2012 Feb;22(2):455-64 - PubMed
  8. Curr Opin Obstet Gynecol. 2009 Apr;21(2):180-6 - PubMed
  9. Neuroimage. 2007 Feb 15;34(4):1535-44 - PubMed
  10. J Comp Neurol. 1983 Oct 1;219(4):431-47 - PubMed
  11. Acta Paediatr. 2010 Aug;99(8):1119-27 - PubMed
  12. AJNR Am J Neuroradiol. 2010 Jun;31(6):1091-9 - PubMed
  13. Cereb Cortex. 1999 Oct-Nov;9(7):754-63 - PubMed
  14. Hum Brain Mapp. 2010 Sep;31(9):1348-58 - PubMed
  15. Brain Struct Funct. 2014 Jan;219(1):231-53 - PubMed
  16. Cereb Cortex. 2002 Jan;12(1):37-53 - PubMed
  17. Nat Rev Neurosci. 2006 Nov;7(11):883-90 - PubMed
  18. Med Image Anal. 2009 Apr;13(2):203-14 - PubMed
  19. Acta Radiol. 1992 Sep;33(5):400-4 - PubMed
  20. IEEE Trans Med Imaging. 1998 Feb;17(1):87-97 - PubMed
  21. Neuroimage. 2004 Jul;22(3):1134-40 - PubMed
  22. Trends Neurosci. 1995 Sep;18(9):383-8 - PubMed
  23. Cereb Cortex. 2016 Jul;26(7):3023-35 - PubMed
  24. Trends Neurosci. 2009 May;32(5):291-301 - PubMed
  25. Neuroimage. 2000 Sep;12(3):340-56 - PubMed
  26. Radiology. 1999 Sep;212(3):876-84 - PubMed
  27. Semin Perinatol. 2009 Aug;33(4):220-33 - PubMed
  28. Cereb Cortex. 2002 Dec;12(12):1237-43 - PubMed
  29. IEEE Trans Med Imaging. 2014 Sep;33(9):1818-31 - PubMed
  30. Neuroimage. 2010 Nov 1;53(2):460-70 - PubMed
  31. J Neurosci. 1984 Jan;4(1):25-42 - PubMed
  32. Neurosci Res Program Bull. 1982 Apr;20(4):439-51 - PubMed
  33. Dev Neurosci. 2008;30(1-3):211-20 - PubMed
  34. Lancet Neurol. 2009 Jan;8(1):110-24 - PubMed
  35. Neurosci Biobehav Rev. 2007;31(8):1157-68 - PubMed
  36. PLoS One. 2015 Mar 05;10(3):e0119536 - PubMed
  37. Clin Linguist Phon. 2007 Nov-Dec;21(11-12):975-89 - PubMed
  38. J Comp Neurol. 1972 May;145(1):61-83 - PubMed
  39. Cereb Cortex. 2002 May;12(5):536-44 - PubMed
  40. AJNR Am J Neuroradiol. 2005 Nov-Dec;26(10 ):2671-84 - PubMed
  41. Neuroimage. 2005 Aug 1;27(1):210-21 - PubMed
  42. Cereb Cortex. 2006 Jul;16 Suppl 1:i3-17 - PubMed
  43. Anat Rec. 2002 May 1;267(1):1-6 - PubMed
  44. Cereb Cortex. 2013 Nov;23(11):2620-31 - PubMed
  45. Neuroimage. 2006 Nov 1;33(2):463-70 - PubMed
  46. Eur J Radiol. 2006 Feb;57(2):199-216 - PubMed
  47. Neuroradiology. 2009 Sep;51(9):567-76 - PubMed
  48. Ann Neurol. 1977 Jan;1(1):86-93 - PubMed
  49. Front Hum Neurosci. 2013 Aug 02;7:423 - PubMed
  50. Arch Dis Child. 1973 Oct;48(10):757-67 - PubMed
  51. J Comp Neurol. 1992 Jul 8;321(2):223-40 - PubMed
  52. J Comp Neurol. 1990 Jul 15;297(3):441-70 - PubMed
  53. Cereb Cortex. 2006 Jul;16 Suppl 1:i46-56 - PubMed
  54. Trends Neurosci. 2009 Sep;32(9):496-505 - PubMed
  55. Brain Struct Funct. 2012 Jan;217(1):127-39 - PubMed
  56. Nat Rev Neurosci. 2008 Feb;9(2):110-22 - PubMed
  57. Nat Rev Neurosci. 2015 Mar;16(3):133-46 - PubMed
  58. Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13281-6 - PubMed
  59. Am J Surg Pathol. 1996 Dec;20(12):1501-6 - PubMed
  60. Nat Rev Neurosci. 2009 Oct;10(10):724-35 - PubMed
  61. Int J Dev Neurosci. 2014 Feb;32:11-22 - PubMed
  62. Eur J Radiol. 2006 Feb;57(2):187-98 - PubMed
  63. Neuron. 2014 Jan 22;81(2):321-32 - PubMed
  64. Nature. 2011 Sep 28;478(7369):382-6 - PubMed
  65. J Comp Neurol. 2005 Oct 17;491(2):109-22 - PubMed
  66. Cereb Cortex. 2008 Apr;18(4):915-29 - PubMed
  67. Ann N Y Acad Sci. 2011 May;1225 Suppl 1:E105-30 - PubMed
  68. J Neurosci. 2009 Apr 1;29(13):4263-73 - PubMed
  69. J Comp Neurol. 1977 Nov 1;176(1):23-52 - PubMed
  70. J Comp Neurol. 1988 May 15;271(3):355-86 - PubMed
  71. Semin Fetal Neonatal Med. 2006 Dec;11(6):415-22 - PubMed
  72. Science. 1988 Jul 8;241(4862):170-6 - PubMed
  73. Int J Dev Biol. 1991 Sep;35(3):215-30 - PubMed
  74. Front Neurol. 2014 Jul 29;5:139 - PubMed
  75. Anat Rec. 1984 Jun;209(2):265-71 - PubMed
  76. Virchows Arch A Pathol Anat Histopathol. 1983;402(2):195-201 - PubMed
  77. Pediatr Radiol. 2004 Sep;34(9):694-9 - PubMed
  78. Nature. 1997 Jan 23;385(6614):313-8 - PubMed
  79. Brain Res. 1973 Feb 28;50(2):403-7 - PubMed

Publication Types