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PMID: 20979582 Published · ppublish English Journal Article Review

Renewed focus on the developing human neocortex.

Journal of anatomy ·Vol. 217 ·No. 4 ·2010-10-00 ·Pages 276-88

Clowry G, Molnár Z, Rakic P

Abstract

Many specifically human psychiatric and neurological conditions have developmental origins. Rodent models are extremely valuable for the investigation of brain development, but cannot provide insight into aspects that are specifically human. The human brain, and particularly the cerebral cortex, has some unique genetic, molecular, cellular and anatomical features, and these need to be further explored. Cortical expansion in human is not just quantitative; there are some novel types of neurons and cytoarchitectonic areas identified by their gene expression, connectivity and functions that do not exist in rodents. Recent research into human brain development has revealed more elaborated neurogenetic compartments, radial and tangential migration, transient cell layers in the subplate, and a greater diversity of early-generated neurons, including predecessor neurons. Recently there has been a renaissance of the study of human brain development because of these unique differences, made possible by the availability of new techniques. This review gives a flavour of the recent studies stemming from this renewed focus on the developing human brain.

MeSH Terms
Animals Brain Injuries/physiopathology Brain Mapping/methods Cerebral Cortex/anatomy & histology,embryology,growth & development Humans Magnetic Resonance Imaging Neurons/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Clowry Gavin
Institute of Neuroscience, Newcastle University, Framlington Place, Newcastle upon Tyne, UK. [email protected]
Molnár Zoltán
Rakic Pasko
References (110)
110 references, click to expand
  1. Assessment of brain tissue injury after moderate hypothermia in neonates with hypoxic-ischaemic encephalopathy: a nested substudy of a randomised controlled trial.
    Lancet Neurol. 2010 Jan;9(1):39-45 PMID: 19896902
  2. MRC-Wellcome Trust Human Developmental Biology Resource: enabling studies of human developmental gene expression.
    Trends Genet. 2005 Nov;21(11):586-90 PMID: 16154230
  3. Genetic control of neuronal migrations in human cortical development.
    Adv Anat Embryol Cell Biol. 2007;189:1 p preceding 1, 1-111 PMID: 17212070
  4. Evolution of the neocortex: a perspective from developmental biology.
    Nat Rev Neurosci. 2009 Oct;10(10):724-35 PMID: 19763105
  5. The human transient subpial granular layer: an optical, immunohistochemical, and ultrastructural analysis.
    J Comp Neurol. 1992 Oct 1;324(1):94-114 PMID: 1401263
  6. Abnormal development of the human cerebral cortex.
    J Anat. 2010 Oct;217(4):312-23 PMID: 20979584
  7. Contributions of cortical subventricular zone to the development of the human cerebral cortex.
    J Comp Neurol. 2005 Oct 17;491(2):109-22 PMID: 16127688
  8. Imaging selective vulnerability in the developing nervous system.
    J Anat. 2010 Oct;217(4):429-35 PMID: 20408904
  9. Imaging biomarkers of outcome in the developing preterm brain.
    Lancet Neurol. 2009 Nov;8(11):1042-55 PMID: 19800293
  10. The Allen Brain Atlas: 5 years and beyond.
    Nat Rev Neurosci. 2009 Nov;10(11):821-8 PMID: 19826436
  11. Perinatal subplate neuron injury: implications for cortical development and plasticity.
    Brain Pathol. 2005 Jul;15(3):250-60 PMID: 16196392
  12. Unravelling the development of the visual cortex: implications for plasticity and repair.
    J Anat. 2010 Oct;217(4):449-68 PMID: 20722872
  13. Telencephalic origin of pulvinar neurons in the fetal human brain.
    Z Anat Entwicklungsgesch. 1969;129(1):53-82 PMID: 4186810
  14. Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia.
    Cereb Cortex. 2009 Sep;19(9):2196-207 PMID: 19234067
  15. Decision by division: making cortical maps.
    Trends Neurosci. 2009 May;32(5):291-301 PMID: 19380167
  16. Neurovascular congruence during cerebral cortical development.
    Cereb Cortex. 2009 Jul;19 Suppl 1:i32-41 PMID: 19386634
  17. New horizons for the subplate zone and its pioneering neurons.
    Cereb Cortex. 2009 Aug;19(8):1705-7 PMID: 19293397
  18. From spatial-data to 3D models of the developing human brain.
    Methods. 2010 Feb;50(2):96-104 PMID: 19800406
  19. The Mouse Genome Database (MGD): mouse biology and model systems.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D724-8 PMID: 18158299
  20. Genome wide high density SNP-based linkage analysis of childhood absence epilepsy identifies a susceptibility locus on chromosome 3p23-p14.
    Epilepsy Res. 2009 Dec;87(2-3):247-55 PMID: 19837565
  21. From selective vulnerability to connectivity: insights from newborn brain imaging.
    Trends Neurosci. 2009 Sep;32(9):496-505 PMID: 19712981
  22. Patterning of frontal cortex subdivisions by Fgf17.
    Proc Natl Acad Sci U S A. 2007 May 1;104(18):7652-7 PMID: 17442747
  23. Is Pax6 critical for neurogenesis in the human fetal brain?
    Cereb Cortex. 2008 Jun;18(6):1455-65 PMID: 17947347
  24. Reorganization after pre- and perinatal brain lesions.
    J Anat. 2010 Oct;217(4):469-74 PMID: 20649910
  25. The dependence of spinal cord development on corticospinal input and its significance in understanding and treating spastic cerebral palsy.
    Neurosci Biobehav Rev. 2007;31(8):1114-24 PMID: 17544509
  26. Developmental plasticity connects visual cortex to motoneurons after stroke.
    Ann Neurol. 2010 Jan;67(1):132-6 PMID: 20186850
  27. Motor cortex plasticity in ischemic perinatal stroke: a transcranial magnetic stimulation and functional MRI study.
    Pediatr Neurol. 2009 Sep;41(3):171-8 PMID: 19664531
  28. Comparative aspects of cerebral cortical development.
    Eur J Neurosci. 2006 Feb;23(4):921-34 PMID: 16519657
  29. Tangential networks of precocious neurons and early axonal outgrowth in the embryonic human forebrain.
    J Neurosci. 2005 Mar 16;25(11):2781-92 PMID: 15772338
  30. Cortical ventricular zone progenitors and their progeny maintain spatial relationships and radial patterning during preplate development indicating an early protomap.
    Cereb Cortex. 2006 Jul;16 Suppl 1:i46-56 PMID: 16766707
  31. Neuroimaging of cortical development and brain connectivity in human newborns and animal models.
    J Anat. 2010 Oct;217(4):418-28 PMID: 20979587
  32. Subplate in the developing cortex of mouse and human.
    J Anat. 2010 Oct;217(4):368-80 PMID: 20727056
  33. Genetic regulation of arealization of the neocortex.
    Curr Opin Neurobiol. 2008 Feb;18(1):90-100 PMID: 18524571
  34. Corticospinal tract development and its plasticity after perinatal injury.
    Neurosci Biobehav Rev. 2007;31(8):1136-49 PMID: 18053875
  35. Anomia from pulvinar and subcortical parietal stimulation.
    Brain. 1968 Mar;91(1):99-116 PMID: 5643285
  36. Insights from in vitro fetal magnetic resonance imaging of cerebral development.
    Semin Perinatol. 2009 Aug;33(4):220-33 PMID: 19631083
  37. Specification of cerebral cortical areas.
    Science. 1988 Jul 8;241(4862):170-6 PMID: 3291116
  38. Stroke in the developing brain and intractable epilepsy: effect of timing on hippocampal sclerosis.
    Dev Med Child Neurol. 2003 Sep;45(9):580-5 PMID: 12948324
  39. The subplate and early cortical circuits.
    Annu Rev Neurosci. 2010;33:23-48 PMID: 20201645
  40. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling.
    Nat Neurosci. 2010 Jun;13(6):690-9 PMID: 20436478
  41. Transient fetal structure, the gangliothalamic body, connects telencephalic germinal zone with all thalamic regions in the developing human brain.
    J Comp Neurol. 1997 Aug 4;384(3):373-95 PMID: 9254034
  42. Deciphering the disease process of schizophrenia: the contribution of cortical GABA neurons.
    Int Rev Neurobiol. 2007;78:109-31 PMID: 17349859
  43. Emx2 patterns the neocortex by regulating FGF positional signaling.
    Nat Neurosci. 2003 Aug;6(8):825-31 PMID: 12872126
  44. Proliferation but not migration is associated with blood vessels during development of the rostral migratory stream.
    Dev Neurosci. 2010 Aug;32(3):163-72 PMID: 20616553
  45. Gene expression in cortical interneuron precursors is prescient of their mature function.
    Cereb Cortex. 2008 Oct;18(10):2306-17 PMID: 18250082
  46. Neurogenic radial glia in the outer subventricular zone of human neocortex.
    Nature. 2010 Mar 25;464(7288):554-561 PMID: 20154730
  47. Characterization of nodular neuronal heterotopia in children.
    Brain. 1999 Feb;122 ( Pt 2):219-38 PMID: 10071051
  48. Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon.
    J Neurocytol. 1980 Apr;9(2):219-42 PMID: 7441294
  49. Common cortical and thalamic mechanisms for language and motor functions.
    Am J Physiol. 1984 Jun;246(6 Pt 2):R901-3 PMID: 6742166
  50. Building a human cortex: the evolutionary differentiation of Cajal-Retzius cells and the cortical hem.
    J Anat. 2010 Oct;217(4):334-43 PMID: 20626498
  51. Populations of subplate and interstitial neurons in fetal and adult human telencephalon.
    J Anat. 2010 Oct;217(4):381-99 PMID: 20979586
  52. Progressive loss of PAX6, TBR2, NEUROD and TBR1 mRNA gradients correlates with translocation of EMX2 to the cortical plate during human cortical development.
    Eur J Neurosci. 2008 Oct;28(8):1449-56 PMID: 18973570
  53. Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system?
    Ann Neurol. 2007 Nov;62(5):493-503 PMID: 17444535
  54. Origin of GABAergic neurons in the human neocortex.
    Nature. 2002 Jun 6;417(6889):645-9 PMID: 12050665
  55. Embryonic vertebrate central nervous system: revised terminology. The Boulder Committee.
    Anat Rec. 1970 Feb;166(2):257-61 PMID: 5414696
  56. Neuro-archaeology: pre-symptomatic architecture and signature of neurological disorders.
    Trends Neurosci. 2008 Dec;31(12):626-36 PMID: 18951639
  57. Neurons in the white matter of the adult human neocortex.
    Front Neuroanat. 2009 Jun 09;3:7 PMID: 19543540
  58. Supravital DNA synthesis in the developing human and mouse brain.
    J Neuropathol Exp Neurol. 1968 Apr;27(2):246-76 PMID: 5646196
  59. Disruption of interneuron development.
    Epilepsia. 2005;46 Suppl 7:22-8 PMID: 16201992
  60. Making bigger brains-the evolution of neural-progenitor-cell division.
    J Cell Sci. 2008 Sep 1;121(Pt 17):2783-93 PMID: 18716282
  61. Genome-wide analyses of human perisylvian cerebral cortical patterning.
    Proc Natl Acad Sci U S A. 2007 Nov 6;104(45):17849-54 PMID: 17978184
  62. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone.
    Cereb Cortex. 2008 Jul;18(7):1536-48 PMID: 17965125
  63. Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction?
    Front Neuroanat. 2008 Nov 12;2:5 PMID: 19127284
  64. Exploring cortical subplate evolution using magnetic resonance imaging of the fetal brain.
    Dev Neurosci. 2008;30(1-3):211-20 PMID: 18075267
  65. The HUDSEN Atlas: a three-dimensional (3D) spatial framework for studying gene expression in the developing human brain.
    J Anat. 2010 Oct;217(4):289-99 PMID: 20979583
  66. Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging.
    J Anat. 2010 Oct;217(4):400-17 PMID: 20609031
  67. Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis.
    Proc Natl Acad Sci U S A. 2009 Jan 13;106(2):641-6 PMID: 19129494
  68. Functional and evolutionary insights into human brain development through global transcriptome analysis.
    Neuron. 2009 May 28;62(4):494-509 PMID: 19477152
  69. Development of non-phosphorylated neurofilament protein expression in neurones of the New World monkey dorsolateral frontal cortex.
    Eur J Neurosci. 2007 Mar;25(6):1767-79 PMID: 17432964
  70. Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT).
    Cereb Cortex. 2006 Mar;16(3):405-14 PMID: 15944371
  71. Formation of cortical fields on a reduced cortical sheet.
    J Neurosci. 1999 Nov 15;19(22):9939-52 PMID: 10559402
  72. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain.
    J Comp Neurol. 1990 Jul 15;297(3):441-70 PMID: 2398142
  73. A novel cytoarchitectonic area induced experimentally within the primate visual cortex.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2083-7 PMID: 2006147
  74. Magnetic resonance spectroscopic imaging of human brain development.
    Neuroimaging Clin N Am. 2006 Feb;16(1):75-85, viii PMID: 16543086
  75. Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex.
    J Neuropathol Exp Neurol. 2007 May;66(5):372-82 PMID: 17483694
  76. Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants.
    J Anat. 2010 Oct;217(4):436-48 PMID: 20557401
  77. The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas.
    Cereb Cortex. 2006 Jul;16 Suppl 1:i26-34 PMID: 16766704
  78. Five cases of brain injury following amniocentesis in mid-term pregnancy.
    Dev Med Child Neurol. 2000 Aug;42(8):554-60 PMID: 10981934
  79. Structural asymmetries of perisylvian regions in the preterm newborn.
    Neuroimage. 2010 Aug 1;52(1):32-42 PMID: 20362679
  80. Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974).
    J Anat. 2010 Oct;217(4):344-67 PMID: 20979585
  81. Neuronal migration, with special reference to developing human brain: a review.
    Brain Res. 1973 Nov 9;62(1):1-35 PMID: 4203033
  82. High quality RNA from multiple brain regions simultaneously acquired by laser capture microdissection.
    BMC Mol Biol. 2009 Jul 06;10:69 PMID: 19580671
  83. Do cortical areas emerge from a protocortex?
    Trends Neurosci. 1989 Oct;12(10):400-6 PMID: 2479138
  84. Human-specific transcriptional regulation of CNS development genes by FOXP2.
    Nature. 2009 Nov 12;462(7270):213-7 PMID: 19907493
  85. Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex.
    Cereb Cortex. 2009 Aug;19(8):1738-50 PMID: 19008461
  86. Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging.
    Cereb Cortex. 2002 May;12(5):536-44 PMID: 11950771
  87. Mechanisms of cortical development: a view from mutations in mice.
    Annu Rev Neurosci. 1978;1:297-326 PMID: 386903
  88. Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options.
    Trends Neurosci. 2008 Mar;31(3):154-62 PMID: 18262290
  89. Primary cortical folding in the human newborn: an early marker of later functional development.
    Brain. 2008 Aug;131(Pt 8):2028-41 PMID: 18587151
  90. An RNA gene expressed during cortical development evolved rapidly in humans.
    Nature. 2006 Sep 14;443(7108):167-72 PMID: 16915236
  91. The origins of cortical interneurons: mouse versus monkey and human.
    Cereb Cortex. 2009 Sep;19(9):1953-6 PMID: 19429862
  92. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes.
    Anat Embryol (Berl). 1979 Jun 5;156(2):115-52 PMID: 111580
  93. Mosaic organization of neural stem cells in the adult brain.
    Science. 2007 Jul 20;317(5836):381-4 PMID: 17615304
  94. A stem cell niche for intermediate progenitor cells of the embryonic cortex.
    Cereb Cortex. 2009 Jul;19 Suppl 1:i70-7 PMID: 19346271
  95. The importance of the blood-brain barrier in fetuses and embryos.
    Trends Neurosci. 1991 Jan;14(1):14-5 PMID: 1709526
  96. A long, remarkable journey: tangential migration in the telencephalon.
    Nat Rev Neurosci. 2001 Nov;2(11):780-90 PMID: 11715055
  97. Adult structure and development of the human fronto-opercular cerebral cortex (Broca's region).
    Clin Linguist Phon. 2007 Nov-Dec;21(11-12):975-89 PMID: 17972193
  98. Barriers in the brain: a renaissance?
    Trends Neurosci. 2008 Jun;31(6):279-86 PMID: 18471905
  99. Development of the human cerebral cortex: Boulder Committee revisited.
    Nat Rev Neurosci. 2008 Feb;9(2):110-22 PMID: 18209730
  100. Investigating gradients of gene expression involved in early human cortical development.
    J Anat. 2010 Oct;217(4):300-11 PMID: 20579172
  101. Prenatal exposure to ultrasound waves impacts neuronal migration in mice.
    Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12903-10 PMID: 16901978
  102. Comparative analysis of extra-ventricular mitoses at early stages of cortical development in rat and human.
    Brain Struct Funct. 2007 Jul;212(1):37-54 PMID: 17717697
  103. Development of layer I neurons in the primate cerebral cortex.
    J Neurosci. 2001 Aug 1;21(15):5607-19 PMID: 11466432
  104. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey.
    Cereb Cortex. 2002 Jan;12(1):37-53 PMID: 11734531
  105. When cortical development goes wrong: schizophrenia as a neurodevelopmental disease of microcircuits.
    J Anat. 2010 Oct;217(4):324-33 PMID: 20408906
  106. Telencephalic origin of human thalamic GABAergic neurons.
    Nat Neurosci. 2001 Sep;4(9):931-6 PMID: 11528425
  107. The subpial granular layer of the foetal cerebral cortex in man. Its ontogeny and significance in congenital cortical malformations.
    Acta Pathol Microbiol Scand. 1965;:Suppl 179:3-98 PMID: 5854018
  108. Transient patterns of cortical lamination during prenatal life: do they have implications for treatment?
    Neurosci Biobehav Rev. 2007;31(8):1157-68 PMID: 17586047
  109. The first neurons of the human cerebral cortex.
    Nat Neurosci. 2006 Jul;9(7):880-6 PMID: 16783367
  110. Origins of cortical GABAergic neurons in the cynomolgus monkey.
    Cereb Cortex. 2009 Feb;19(2):249-62 PMID: 18477686
Article Info
Journal
Journal of anatomy
Abbr.
J Anat
ISSN
1469-7580
Published
2010-10-00
Pages
276-88
Language
English
Region
England
NLM ID
0137162
PMCID
PMC2992407
Subset
IM
Grants
Medical Research Council · G0700089 · United Kingdom
Medical Research Council · G0900901 · United Kingdom
Medical Research Council · G9900837 · United Kingdom
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