Skip to main content
SpringerLink
Log in
Book cover

Pediatric Hydrocephalus pp 19–45Cite as

Development of the Cerebrospinal Fluid Pathways During Embryonic and Fetal Life in Humans

  • Chapter

Abstract

Trying to understand the mechanisms involved in human development is both a complex and fascinating problem. It is also the absolute prerequisite for an analysis of human malformations. Self-evidently, the genesis of malformation syndromes cannot be understood without a knowledge of the normal steps of development. This contradicts the classical works of human embryology, which were devoted to the analysis of malformation syndromes in the attempt to decipher the normal steps of human development — a method that may be called “reverse embryology”. Nowadays, this old method is of no value and it has been necessary to develop new paradigms to discover the normal pathways of development.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adinolfi M, Beck SE, Haddad SA, et al: Permeability of the blood-cerebrospinal fluid barrier to plasma proteins during foetal and perinatal life. Nature 259:140–141, 1976

    PubMed  CAS  Google Scholar 

  2. Alcolado R, Weiler RO, Parrish EP, et al: The cranial arachnoid and pia mater in man: anatomical and ultra-structural observations. Neuropathol Appl Neurobiol 14:1–17, 1988

    PubMed  CAS  Google Scholar 

  3. Alksne JF, Lovings ET: Functional ultrastructure of the arachnoid villus. Arch Neurol 27:371–377, 1972

    PubMed  CAS  Google Scholar 

  4. Allen C, Sievers J, Berry M, et al: Experimental studies on cerebellar foliation. II. A morphometric analysis of cerebellar fissuration defects and growth retardation after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 203:771–783, 1981

    PubMed  CAS  Google Scholar 

  5. Alper SL, Stuart-Tilley A, Simmons CF, et al: The fodrinankyrin cytoskeleton of choroid plexus preferentially colocalizes with apical Na+K+-ATPase rather than with basolateral anion exchanger AE2. J Clin Invest 93:1430–1438, 1994

    PubMed  CAS  Google Scholar 

  6. Alvarez IS, Schoenwolf GC: Expansion of surface epithelium provides the major extrinsic force for bending the neural plate. J Exp Zool 261:340–348, 1992

    PubMed  CAS  Google Scholar 

  7. Angelov DN: Distribution of activity of alkaline phosphatase and Mg-dependent adenosine triphosphatase in the cranial dura mater-arachnoid interface zone of the rat. Cell Tissue Res 260:595–600, 1990

    PubMed  CAS  Google Scholar 

  8. Ashby W, Butler E: Carbonic anhydrase in the central nervous system of the developing fetus. J Biol Chem 175:425–432, 1948

    PubMed  CAS  Google Scholar 

  9. Ayer-Le Lièvre C, Ståhlbom P-A, Sara VR: Expression of IGF-I and-II mRNA in the brain and craniofacial region of the rat fetus. Development 111:105–115, 1991

    PubMed  Google Scholar 

  10. Bagnall KM: The migration and distribution of somite cells after labelling with the carbocyanine dye, DiI: the relationship of this distribution to segmentation in the vertebrate body. Anat Embryol 185:317–324, 1992

    PubMed  CAS  Google Scholar 

  11. Bagnall KM, Higgins SJ, Sanders EJ: The contribution made by a single somite to the vertebral column: experimental evidence in support of resegmentation using the quail-chick chimaera model. Development 103:69–85, 1988

    PubMed  CAS  Google Scholar 

  12. Bagnall KM, Higgins SJ, Sanders EJ: The contribution made by cells from a single somite to tissues within a body segment and assessment of their integration with similar cells from adjacent segments. Development 107:931–943, 1989

    PubMed  CAS  Google Scholar 

  13. Baker J, Liu J-P, Robertson EJ, et al: Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73–82, 1993

    PubMed  CAS  Google Scholar 

  14. Banks WA, Kastin AJ: Saturable transport of peptides across the blood-brain barrier. Life Sci 41:1319–1338, 1987

    PubMed  CAS  Google Scholar 

  15. Barakat I, Wittendorp-Rechenmann E, Rechenmann RV, et al: Influence of meningeal cells on the proliferation of neuroblasts in culture. Dev Neurosci 4:363–372, 1981

    PubMed  CAS  Google Scholar 

  16. Basmajian JV: The depressions for the arachnoid granulations as a criterion of age. Anat Rec 112:843–846, 1952

    PubMed  CAS  Google Scholar 

  17. Beck F, Samani NJ, Byrne S, et al: Histochemical localization of IGF-I and IGF-II mRNA in the rat between birth and adulthood. Development 104:29–39, 1988

    PubMed  CAS  Google Scholar 

  18. Becker NH, Novikoff AB, Zimmerman HM: Fine structure of the uptake of intravenously injected peroxidase by the rat choroid plexus. J Histochem Cytochem 15:160–165, 1967

    PubMed  CAS  Google Scholar 

  19. Birge WJ, Rose AD, Haywood JR, et al: Development of the blood-cerebrospinal fluid barrier to proteins and differentiation of cerebrospinal in the chick embryo. Dev Biol 41:245–254, 1974

    PubMed  CAS  Google Scholar 

  20. Born G: Über Verwachsungsversuche mit Amphibienlarven. Archiv Entwickelungsmechanik der Organismen 4:349–465 (quoted by Harrison 1908), 1897

    Google Scholar 

  21. Boulton M, Flessner M, Amstrong D, et al: Lymphatic drainage of the CNS: effects of lymphatic diversion / ligation on CSF protein transport to plasma. Am J Physiol 272:1613–1619, 1997

    Google Scholar 

  22. Boulton M, Flessner M, Amstrong D, et al: Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am J Physiol 274:88–96, 1998

    Google Scholar 

  23. Boulton M, Flessner M, Amstrong D, et al: Contribution of extracranial lymphatics and arachnoid villi to the clearance of a CSF tracer in the rat. Am J Physiol 276:818–823, 1999

    Google Scholar 

  24. Boulton M, Young A, Hay J, et al: Drainage of CSF through lymphatic pathways and arachnoid villi in sheep: measurement of 125I-albumin clearance. Neuropathol Appl Neurobiol 22: 325–333, 1996

    PubMed  CAS  Google Scholar 

  25. Brightman MW, Reese TS: Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677, 1969

    PubMed  CAS  Google Scholar 

  26. Brissenden JE, Ullrich A, Francke U: Human chromosomal mapping of genes for insulin-like growth factors I and II and epidermal growth factor. Nature 310:781–784, 1984

    PubMed  CAS  Google Scholar 

  27. Brocklehurst G: The development of the human cerebrospinal fluid pathway with particular reference to the roof of the fourth ventricle. J Anat 105:467–475, 1969

    PubMed  CAS  Google Scholar 

  28. Brooks PJ, Funabashi T, Kleopoulos SP, et al: Prolactin receptor messenger RNA is synthesized by the epithelial cells of the choroid plexus. Mol Brain Res 16:163–167, 1992

    PubMed  CAS  Google Scholar 

  29. Cam Y, Sensenbrenner M, Mandel P: A comparative study of the effects of brain extracts and mesodermal membrane extracts on nerve cell differentiation. Experientia 31:1430–1431, 1975

    PubMed  CAS  Google Scholar 

  30. Catala M: Carbonic anhydrase activity during development of the choroid plexus in the human fetus. Childs Nerv Syst 13:364–368, 1997

    PubMed  CAS  Google Scholar 

  31. Catala M: Embryonic and fetal development of structures associated with the cerebro-spinal fluid in man and other species. Part I: the ventricular system, meninges and choroid plexuses. Arch Anat Cytol Pathol 46:153–169, 1998

    PubMed  CAS  Google Scholar 

  32. Cavanagh ME, Cornelis MEP, Dziegielewska KM, et al: Comparison of proteins in CSF of lateral and IVth ventricles during early development of fetal sheep. Dev Brain Res 11:159–167, 1983

    CAS  Google Scholar 

  33. Chamberlain JG: Analysis of developing ependymal and choroidal surfaces in rat brains using scanning electron microscopy. Dev Biol 31:22–30, 1973

    PubMed  CAS  Google Scholar 

  34. Chang M, Zhang L, Tarn JP, et al: Dissecting G protein-coupled receptor signalling pathways with membrane-permeable blocking peptides. Endogeneous 5-HT(2C) receptors in the choroids plexus epithelial cells. J Biol Chem 275:7021–7029, 2000

    PubMed  CAS  Google Scholar 

  35. Chodobski A, Wojcik BE, Loh YP, et al: Vasopressin gene expression in rat choroid plexus. Adv Exp Med Biol 449:59–65, 1998

    PubMed  CAS  Google Scholar 

  36. Cohen LA: Absence of a foramen of Magendie in the dog, cat, rabbit and goat. Arch Neurol 16:524–528, 1967

    Google Scholar 

  37. Cooper ERA: Arachnoid granulations in man. Acta Anat (Basel) 34:187–200, 1958

    CAS  Google Scholar 

  38. Coulombre AJ, Coulombre JL: The role of mechanical factors in brain morphogenesis. Anat Rec 130:289–290, 1958

    Google Scholar 

  39. Couly G: Concepts nouveaux de la biologie du développement céphalique humain, observations et hypothèses. Ann Genet 25:201–206, 1982

    PubMed  CAS  Google Scholar 

  40. Couly G: Concepts nouveaux de la biologie du développement céphalique humain, observations et hypothèses. Semin Hop Paris 59:1699–1704, 1983

    CAS  Google Scholar 

  41. Couly GF, Coltey PM, Eichmann A, et al: The angiogenic potentials of the cephalic mesoderm and the origin of brain and head blood vessels. Mech Dev 53:97–112, 1995

    PubMed  CAS  Google Scholar 

  42. Couly GF, Coltey PM, Le Douarin NM: The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15, 1992

    PubMed  CAS  Google Scholar 

  43. Couly GF, Le Douarin NM: Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev Biol 120:198–214, 1987

    PubMed  CAS  Google Scholar 

  44. Dandy WE: Experimental hydrocephalus. Ann Surg 70:129–142, 1919

    PubMed  CAS  Google Scholar 

  45. Dandy WE, Blackfan KD: Internal hydrocephalus. An experimental, clinical and pathological study. Am J Dis Child 8:406–482, 1914

    Google Scholar 

  46. Davis DA, Milhorat TH: The blood-brain barrier of the rat choroid plexus. Anat Rec 181:779–790, 1975

    PubMed  CAS  Google Scholar 

  47. De Chiara TM, Efstratiadis A, Robertson EJ: A growth-deficiency phenotype in heterozygotous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345:78–80, 1990

    Google Scholar 

  48. Decker JF, Quay WB: Stimulatory effects of melatonin on ependymal epithelium of choroid plexuses in golden hamsters. J Neural Transm 55:53–67, 1982

    PubMed  CAS  Google Scholar 

  49. Desmond ME: Description of the occlusion of the spinal cord lumen in early human embryos. Anat Rec 204:89–93, 1982

    PubMed  CAS  Google Scholar 

  50. Desmond ME: Reduces number of brain cells in so-called neural overgrowth. Anat Rec 212:195–198, 1985

    PubMed  CAS  Google Scholar 

  51. Desmond ME, Duzy MJ, Federici BD: Second messenger regulation of occlusion of the spinal neurocoel in the chick embryo. Dev Dyn 197:291–306, 1993

    PubMed  CAS  Google Scholar 

  52. Desmond ME, Jacobson AG: Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev Biol 57:188–198, 1977

    PubMed  CAS  Google Scholar 

  53. Desmond ME, Schoewolf GC: Timing and positioning of occlusion of the spinal neurocele in the chick embryo. J Comp Neurol 235:479–487, 1985

    PubMed  CAS  Google Scholar 

  54. Desmond ME, Schoenwolf GC: Evaluation of the roles of intrinsic and extrinsic factors in occlusion of the spinal neurocoel during rapid brain enlargement in the chick embryo. J Embryol Exp Morphol 97:25–46, 1986

    PubMed  CAS  Google Scholar 

  55. Dickson PW, Aldred AR, Marley PD, et al: Rat choroid plexus specializes in the synthesis and the secretion of transthyretin (prealbumin). Regulation of transthyretin synthesis in choroid plexus is independent from that in liver. J Biol Chem 261:3475–3478, 1986

    PubMed  CAS  Google Scholar 

  56. Dontchev N, Hadjioloff A-I: Histogénèse et histochimie du plexus choroïde du télencéphale chez l’embryon humain. Bull Assoc Anatom 146:480–485, 1971

    Google Scholar 

  57. Dziegielewska KM, Evans CAN, Fossan G, et al: Proteins in CSF and plasma of fetal sheep during development. J Physiol 300:441–455, 1980

    PubMed  CAS  Google Scholar 

  58. Dziegielewska KM, Evans CAN, Lai PCW, et al: Proteins in cerebrospinal fluid and plasma of fetal rats during development. Dev Biol 83:193–200, 1981

    PubMed  CAS  Google Scholar 

  59. Dziegielewska KM, Evans CAN, New H, et al: Synthesis of plasma proteins by rat fetal brain and choroid plexus. Int J Dev Neurosci 2:215–222, 1984

    CAS  Google Scholar 

  60. Ekström TJ, Cui H, Li X, et al: Promoter-specific IGF2 imprinting status and its plasticity during human liver development. Development 121:309–316, 1995

    PubMed  Google Scholar 

  61. el-Gammal S: The development of the diencephalic choroid plexus in the chick, a scanning electron-microscopic study. Cell Tissue Res 219:297–311, 1981

    PubMed  CAS  Google Scholar 

  62. el-Gammal S: Regional surface changes during the development of the telencephalic choroid plexus in the chick, a scanning-electron microscopic study. Cell Tissue Res 231:251–263, 1983

    PubMed  CAS  Google Scholar 

  63. Ernst SA, Palacios JR, Siegel GJ: Immunocytochemical localization of Na+, K+-ATPase catalytic polypeptide in mouse choroid plexus. J Histochem Cytochem 34:189–195, 1986

    PubMed  CAS  Google Scholar 

  64. Faraci FM, Mayhan WG, Heistad DD: Effect of vasopressin on production of cerebrospinal fluid: possible role of vasopressin (V1)-receptors. Am J Physiol 258(1Pt2):94–98, 1990

    Google Scholar 

  65. Fawcett DW. Bloom and Fawcett, a Textbook of Histology, 12th edn. Chapman and Hall. New York, 1994

    Google Scholar 

  66. Feeney JF, Watterson RL: The development of the vascular pattern within the walls of the central nervous system of the chick embryo. J Morphol 78:231–303, 1946

    PubMed  Google Scholar 

  67. Flexner LB: Changes in the chemistry and nature of the cerebrospinal fluid during fetal life in the pig. Am J Physiol 124:131–135, 1938

    CAS  Google Scholar 

  68. Foley F: Resorption of the cerebrospinal fluid by the choroid plexuses under the influence of intravenous injection of hypertonic salt solutions. Arch Neurol Psychiatry 5744–5745, 1921

    Google Scholar 

  69. Frazier CH, Peet MM: Factors of influence in the origin and circulation of the cerebrospinal fluid. Am J Physiol 35:268–282, 1914

    Google Scholar 

  70. Gensburger C, Labourdette G, Sensenbrenner M: Influence of meningeal cells on the proliferation and maturation of rat neuroblasts in culture. Exp Brain Res 63:321–330, 1986

    PubMed  CAS  Google Scholar 

  71. Ghandour MS, Langley OK, Zhu XL, et al: Carbonic anhydrase IV on brain capillary endothelial cells: a marker associated with the blood-brain barrier. Proc Natl Acad Sci USA 89:6823–6827, 1992

    PubMed  CAS  Google Scholar 

  72. Giannoukakis N, Deal C, Paquette J, et al: Parental genomic imprinting of the human IGF2 gene. Nature Genet 4:98–101, 1993

    PubMed  CAS  Google Scholar 

  73. Gomez DG, Di Benedetto AT, Pavese AM, et al: Development of arachnoid villi and granulations in man. Acta Anat 111:247–258, 1981

    Google Scholar 

  74. Gomez DG, Ehrmann JE, Gordon-Potts D, et al: The arachnoid granulations of the newborn human: an ultrastructural study. Int J Dev Neurosci 1:138–147, 1983

    Google Scholar 

  75. Gomez DG, Potts G: The surface characteristics of arachnoid granulations. A scanning electron microscopical study. Arch Neurol 31:88–93, 1974

    PubMed  CAS  Google Scholar 

  76. Gomez DG, Potts G, Deonarine V, et al: Effects of pressure gradient changes on the morphology of arachnoid villi and granulations of the monkey. Lab Invest 28:648–657, 1973

    PubMed  CAS  Google Scholar 

  77. Gonzalez-Martinez LM, Avila J, Marti E, et al: Expression of the b-subunit isoforms of the Na, K-ATPase in rat embryo tissues, inner ear and choroid plexus. Biol Cell 81:215–222, 1994

    PubMed  CAS  Google Scholar 

  78. Grasset P-P. Traité de Zoologie. Tome XL Les procordés. Masson, Paris 1948

    Google Scholar 

  79. Grossman CB, Potts DG: Arachnoid granulations: radiology and anatomy. Radiology 113:95–100, 1974

    PubMed  CAS  Google Scholar 

  80. Hagen GA, Elliott WJ: Transport of thyroid hormones in serum and cerebrospinal fluid. J Clin Endocrinol Metab 37:415–422, 1973

    PubMed  CAS  Google Scholar 

  81. Halata Z, Grim M, Christ B: Origin of spinal cord meninges, sheaths of peripheral nerves, and cutaneous receptors including Merkel cells. An experimental and ultrastructural study with avian chimeras. Anat Embryol 182:529–537, 1990

    PubMed  CAS  Google Scholar 

  82. Hamel E, Assumel Lurdin C, Fage D, et al: Small pial vessels, but not choroid plexus, exhibit specific biochemical correlates of functional cholinergic innervation. Brain Res 516:301–309, 1990

    PubMed  CAS  Google Scholar 

  83. Harrison RG: Embryonic transplantation and the development of the nervous system. Anat Rec 2:385–410, 1908

    Google Scholar 

  84. Hartmann D, Sievers J, Pehlemann FW et al: Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus. J Comp Neurol 320:33–61, 1992

    PubMed  CAS  Google Scholar 

  85. Hartmann D, Schulze M, Sievers J: Meningeal cells stimulate and direct the migration of cerebellar external granule cells in vitro. J Neurocytol 27:395–409, 1998 a

    PubMed  CAS  Google Scholar 

  86. Hartmann D, Ziegenhagen MW, Sievers J: Meningeal cells stimulate neuronal migration and the formation of radial glial fascicles from the cerebellar external granular layer. Neurosci Lett 244:129–132, 1998 b

    PubMed  CAS  Google Scholar 

  87. Harvey MB, Kaye PL: IGF-2 stimulates growth and metabolism of early mouse embryos. Mech Dev 38:169–174, 1992

    PubMed  CAS  Google Scholar 

  88. Harvey SC, Burr HS: An experimental study of the origin of the meninges. Proc Soc Exp Biol Med 22:52–53, 1924

    Google Scholar 

  89. Harvey SC, Burr HS: The development of the meninges. Arch Neurol Psychiatry 15:545–567, 1926

    Google Scholar 

  90. Haywood JR, Vogh BP: Some measurements of autonomic nervous system influence on production of cerebrospinal fluid in the cat. J Pharmacol Exp Ther 208:341–346, 1979

    PubMed  CAS  Google Scholar 

  91. Holash JA, Noden DM, Stewart PA: Re-evaluating the role of astrocytes in blood-brain barrier induction. Dev Dyn 197:14–25, 1993

    PubMed  CAS  Google Scholar 

  92. Jacobsen M, Møllgård K, Reynolds ML, et al: The choroid plexus in fetal sheep during development with special reference to intracellular plasma protein. Dev Brain Res 8:77–88, 1983

    Google Scholar 

  93. Janzer RC, Raff MC: Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325:253–257, 1987

    PubMed  CAS  Google Scholar 

  94. Jefferies WA, Brandon MR, Hunt SV, et al: Transferrin receptor on endothelium of brain capillaries. Nature 312:62–163, 1984

    Google Scholar 

  95. Jelínek R, Pexieder T: Pressure of the CSF and the morphogenesis of the CNS. Folia Morphol (Praha) 18:102–110, 1970

    Google Scholar 

  96. Johnston MC: A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 156:143–156, 1966

    PubMed  CAS  Google Scholar 

  97. Jones HC: Continuity between the ventricular and subarachnoid cerebrospinal fluid in an amphibian, Rana pipiens. Cell Tissue Res 195:153–167, 1978

    PubMed  CAS  Google Scholar 

  98. Jones HC: The ultrastructure of the roof of the rhombencephalic posterior tela and adjacent tissues in an amphibian, Rana pipiens. J Anat 134:91–102, 1982

    PubMed  CAS  Google Scholar 

  99. Jones HC, Dolman GS: The structure of the roof of the fourth ventricle in pigeon and chick brains by light and electron microscopy. J Anat 28:13–39, 1979

    Google Scholar 

  100. Jones HC, Jopling CA: The development of interependymal pores in the rhombencephalic posterior tela in late embryonic, larval and metamorphosing stages of Rana pipiens. Brain Res 283:121–130, 1983

    PubMed  CAS  Google Scholar 

  101. Jones HC, Sellars RA: The movement of fluid out of the cerebral ventricles in fetal and neonatal rats. Z Kinderchir 37:130–133, 1982

    Google Scholar 

  102. Junghans U, Koops A, Westmeyer A, et al: Purification of a meningeal cell-derived chondroitin sulphate proteoglycan with neurotrophic activity for brain neurons and its identification as biglycan. Eur J Neurosci 7:2341–2350, 1995

    PubMed  CAS  Google Scholar 

  103. Kamiryo T, Orita T, Nishizaki T, et al: Development of the rat meninx: experimental study using bromodeoxyuridine. Anat Rec 227:207–210, 1990

    PubMed  CAS  Google Scholar 

  104. Kaplan GP, Hartman BK, Creveling CR: Localization of catechol-O-methyltransferase in the leptomeninges, choroid plexus and ciliary epithelium: implications for the separation of central and peripheral catechols. Brain Res 204:353–360, 1981

    PubMed  CAS  Google Scholar 

  105. Kaufman MH: Occlusion of the neural lumen in early mouse embryos analysed by light and electron microscopy. J Embryol Exp Morphol 78:211–228, 1983

    PubMed  CAS  Google Scholar 

  106. Key EAH, Retzius MG: Studien in der Anatomie des Nervensystems und des Bindegewebes. Samson and Wallin. Stockholm. (Quoted by Zenker et al. 1994), 1875

    Google Scholar 

  107. Kitazawa T, Hosoya K, Takahashi T, et al: In-vivo and in-vitro evidence of a carrier-mediated afflux transport system for oestrone-3-sulphate across the blood-cerebrospinal fluid barrier. J Pharm Pharmacol 52:281–288, 2000

    PubMed  CAS  Google Scholar 

  108. Kitraki E, Alexis MN, Papalopoulou M, et al: Glucocorticoid receptor gene expression in the embryonic rat brain. Neuroendocrinology 63:305–317, 1996

    PubMed  CAS  Google Scholar 

  109. Klika E: L’ultrastructure des méninges en ontogénèse chez l’homme. Z Mikrosk Anat Forsch 79:209–222, 1968

    PubMed  CAS  Google Scholar 

  110. Krisch B, Leonhardt H, Oksche A: The meningeal compartments of the median eminence and the cortex. A comparative analysis in the rat. Cell Tissue Res 228:597–640, 1983

    PubMed  CAS  Google Scholar 

  111. Krisch B, Leonhardt H, Oksche A: Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res 238:459–474, 1984

    PubMed  CAS  Google Scholar 

  112. Kuhlenbeck H. The central nervous system of vertebrates. Volume 3 part 1: Structural elements: biology of nervous tissue. Karger, Basel, 1970

    Google Scholar 

  113. Kusaka H, Hirano A, Bornstein MB, et al: The organization of astrocytes in organotypic mouse spinal cord culture: an electron microscope study. Neuropathol Appl Neurobiol 10:411–422, 1984

    PubMed  CAS  Google Scholar 

  114. Kusaka H, Hirano A, Bornstein MB, et al: Basal lamina formation by astrocytes in organotypic cultures of mouse spinal cord tissue. J Neuropath Exp Neurol 44:295–303, 1985

    PubMed  CAS  Google Scholar 

  115. Le Douarin NM: Particularités du noyau interphasique chez la Caille japonaise (Coturnix coturnix japonica). Utilisation de ces particularités comme “marquage biologique” dans les recherches sur les interactions tissulaires et les migrations cellulaires au cours de l’ontogénèse. Bull Biol Fr Belg 103:435–452, 1969

    PubMed  Google Scholar 

  116. Le Gros Clark WE: On the Pacchionian bodies. J Anat 55:40–48, 1920

    PubMed  Google Scholar 

  117. Lenoir D, Honegger P: Insulin-like growth factor I (IGF I) stimulates DNA synthesis in fetal rat brain cell cultures. Dev Brain Res 7:205–213, 1983

    CAS  Google Scholar 

  118. Li E, Beard C, Jaenisch R: Role for DNA methylation in genomic imprinting. Nature 366:362–365, 1993

    PubMed  CAS  Google Scholar 

  119. Li E, Bestor TH, Jaenisch R: Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926, 1992

    PubMed  CAS  Google Scholar 

  120. Lindvall M: Fluorescence histochemical study on regional differences in the sympathetic nerve supply from various laboratory animals. Cell Tissue Res 198:261–267, 1979

    PubMed  CAS  Google Scholar 

  121. Lindvall M, Alumets J, Edvinsson L, et al: Peptidergic (VIP) nerves in the mammalian choroid plexus. Neurosci Lett 9:77–82, 1978

    PubMed  CAS  Google Scholar 

  122. Lindvall M, Edvinsson L, Owman C: Sympathetic nervous control of cerebrospinal fluid production from the choroid plexus. Science 201:176–178, 1978

    PubMed  CAS  Google Scholar 

  123. Lindvall M, Edvinsson L, Owman C: Effects of sympathomimetic drugs and corresponding receptor antagonists on the rate of cerebrospinal fluid production. Exp Neurol 64:132–145, 1979

    PubMed  CAS  Google Scholar 

  124. Lindvall M, Gustafson A, Hedner P, et al: Stimulation of cyclic adenosine 3′,5′-monophosphate formation in rabbit choroid plexus by b-receptor agonists and vasoactive intestinal polypeptide. Neurosci Lett 54:153–157, 1985

    PubMed  CAS  Google Scholar 

  125. Lindvall M, Owman C: Evidence for the presence of two types of monoamine oxidase in rabbit choroid plexus and their role in breakdown of amines influencing cerebrospinal fluid formation. J Neurochem 34:518–522, 1980

    PubMed  CAS  Google Scholar 

  126. Lindvall M, Owman C, Winbladh B: Sympathetic influence on transport functions in the choroid plexus of rabbit and rat. Brain Res 223:160–164, 1981

    PubMed  CAS  Google Scholar 

  127. Lindvall M, Owman C, Winbladh B: Sympathetic influence on sodium-potassium activated adenosine triphosphatase activity of rabbit and rat choroid plexus. Brain Res Bull 9:761–763, 1982

    PubMed  CAS  Google Scholar 

  128. Lindvall-Axelsson M, Hedner P, Owman C: Corticosteroid action on choroids plexus: reduction in Na+-K+-ATPase activity, choline transport capacity, and rate of CSF formation. Exp Brain Res77: 605–610, 1989

    PubMed  CAS  Google Scholar 

  129. Lindvall-Axelsson M, Hedner P, Owman C, et al: Influence of thyroid hormones on transport function and Na+-K-l-ATPase activity in the rat choroid plexus. Acta Physiol Scand 125:627–632, 1985

    PubMed  CAS  Google Scholar 

  130. Lindvall-Axelsson M, Owman C: Changes in transport functions of isolated rabbit choroid plexus under the influence of oestrogene and progesterone. Acta Physiol Scand 136:107–111, 1989

    PubMed  CAS  Google Scholar 

  131. Lindvall-Axelsson M, Owman C: Actions of sex steroids and corticosteroids on rabbit choroid plexus as shown by changes in transport capacity and rate of cerebrospinal fluid formation. Neurol Res 12:181–186, 1990

    PubMed  CAS  Google Scholar 

  132. Liu J-P, Baker J, Perkins AS, et al: Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igfir). Cell 75:59–72, 1993

    PubMed  CAS  Google Scholar 

  133. Login IS, Mac Leod RM: Prolactin in human serum and cerebrospinal fluid. Brain Res 132: 477–483, 1977

    PubMed  CAS  Google Scholar 

  134. Lopes CAS, Mair WGP: Ultrastructure of the outer cortex and the pia mater in man. Acta Neuropathol (Berl) 28:79–86, 1974 a

    CAS  Google Scholar 

  135. Lopes CAS, Mair WGP: Ultrastructure of the arachnoid structure in man. Acta Neuropathol (Berl) 28:167–173, 1974b

    CAS  Google Scholar 

  136. Lopez-Gimenez JF, Mengod D, Palacios JM, et al: Regional distribution and cellular localization of 5-HT2C receptor m RNA in monkey brain: comparison with [3H mesulergine binding site and choline acetyltransferase mR-NA. Synapse 42:12–26, 2001 a

    PubMed  CAS  Google Scholar 

  137. Lopez-Gimenez JF, Vilaro MT, Palacios JM, et al: Mapping of 5-HT2A receptors and their mRNA in monkey brain: [3H] MD2 100, 907 autoradiography and in situ hybridization studies. J Comp Neurol 429:571–598, 2001 b

    PubMed  CAS  Google Scholar 

  138. Lossinsky AS, Vorbrodt AW, Wisniewski HM: Characterization of endothelial cell transport in the developing mouse blood-brain barrier. Dev Neurosci 8:61–75, 1986

    PubMed  CAS  Google Scholar 

  139. Maars JA, Napolitano EW, Murphy-Erdosh C, et al: Distinguishing roles of the membrane-cytoskeleton and Cadherin mediated cell-cell adhesion in generating different Na+, K+-ATPase distributions in polarized ep-ithelia. J Cell Bio 123:149–164, 1993

    Google Scholar 

  140. Mantyth CR, Kruger L, Brecha NC, et al: Localization of specific sites for atrial natriuretic factor in the central nervous system of rat, guinea pig, cat and human. Brain Res 412:329–342, 1987

    Google Scholar 

  141. Masuzawa T, Ohta T, Kawamura M, et al: Immunohisto-chemical localization of Na+, K+-ATPase in the choroid plexus. Brain Res 302:357–362, 1984

    PubMed  CAS  Google Scholar 

  142. Masuzawa T, Ohta T, Kawakami K, et al: Immunocyto-chemical localization of Na+, K+-ATPase in the canine choroid plexus. Brain 108:625–646, 1985

    PubMed  Google Scholar 

  143. Masuzawa T, Sato F: The enzyme histochemistry of the choroid plexus. Brain 106:55–99, 1983

    PubMed  Google Scholar 

  144. Matsuoka Y, Okazaki M, Kitamura Y, et al: Developmental expression of P-glycoprotein (multidrug resistance gene product) in the rat brain. J Neurobiol 39:383–392, 1999

    PubMed  CAS  Google Scholar 

  145. Matthews SG, Parrott RF, Sirinathsinghji DJ: Distribution and cellular localization of vasopressin mRNA in the ovine brain, pituitary and pineal glands. Neuropeptides 25:11–17, 1993

    PubMed  CAS  Google Scholar 

  146. Matthiessen HP, Schmalenbach C, Müller HW: Identification of meningeal cell released neurite promoting activities for embryonic hippocampal neurons. J Neurochem 56:759–768, 1991

    PubMed  CAS  Google Scholar 

  147. Milhorat TH: Choroid plexus and cerebrospinal fluid production. Science 166:1514–1516, 1969

    PubMed  CAS  Google Scholar 

  148. Milhorat TH: Structure and function of the choroid plexus and other sites of cerebrospinal fluid formation. Int Rev Cytol 47:225–288, 1976

    PubMed  CAS  Google Scholar 

  149. Milhorat TH, Davis DA, Lloyd BJ: Two morphologically distinct blood-brain barriers preventing entry of cytochrome c into cerebrospinal fluid. Science 180:76–78, 1973

    CAS  Google Scholar 

  150. Milhorat TH, Hammock MK, Fenstermacher JD, et al: Cerebrospinal fluid production by the choroid plexus and brain. Science 173:330–332, 1971

    PubMed  CAS  Google Scholar 

  151. Mitchell W, Kim CS, O’Tuama LA, et al: Choroid plexus, brain and kidney Na+,K+-ATPase: comparative activities in fetal, newborn and young adult rabbits. Neurosci Lett 31:37–40, 1982

    PubMed  CAS  Google Scholar 

  152. Møllgård K, Dziegielewska KM, Saunders NR, et al: Synthesis and localization of plasma proteins in the developing human brain. Integrity of the fetal blood-brain barrier to endogeneous proteins of hepatic origin. Dev Biol 128:207–221, 1988

    PubMed  Google Scholar 

  153. Møllgård K, Saunders NR: The development of the human blood-brain and blood-CSF barriers. Neuropathol Applied Neurobiol 12:337–358, 1986

    Google Scholar 

  154. Mott FW: The Oliver-Sharpey lectures on the cerebrospinal fluid. Lecture I: the physiology of the cerebrospinal fluid. Lancet ii 1–8, 1910

    Google Scholar 

  155. Müller F, O’Rahilly R: The development of the human brain and the closure of the rostral neuropore at stage 11. Anat Embryol 175:205–222, 1986

    PubMed  Google Scholar 

  156. Müller F, O’Rahilly R: The development of the human brain, the closure of the caudal neuropore, and the beginning of secondary neurulation at stage 12. Anat Embryol 176:413–430, 1987

    PubMed  Google Scholar 

  157. Müller F, O’Rahilly R: The human brain at stages 18–20, including the choroid plexuses and the amygdaloid and septal nuclei. Anat Embryol 182:285–306, 1990

    PubMed  Google Scholar 

  158. Murakami M: An electron microscopic study of the choroid plexus in the lizard, Gecko japonicus. J Electron-microsc 10:77–86, 1961

    Google Scholar 

  159. Nabeshima S, Reese TS, Landis DMD, et al: Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170, 1975

    PubMed  CAS  Google Scholar 

  160. Nathanson JA: b-adrenergic-sensitive adenylate cyclase in secretory cells of choroid plexus. Science 204:843–844, 1979

    PubMed  CAS  Google Scholar 

  161. Nelson E, Blinzinger K, Hager H: Electron microscopic observations on subarachnoid and perivascular spaces of the Syrian hamster brain. Neurology 11:285–295, 1961

    PubMed  Google Scholar 

  162. New H, Dziegielewska KM, Saunders NR: Transferrin in fetal rat brain and cerebrospinal fluid. Int J Dev Neurosci 1:396–373, 1983

    Google Scholar 

  163. Nilsson C, Billa SF: Vasoactive intestinal polypeptide (VIP): effects in the eye and on regional blood flow. Acta Physiol Scand 121:385–392, 1984

    PubMed  CAS  Google Scholar 

  164. Nilsson C, Ekman R, Lindvall-Axelsson M, et al: Distribution of peptidergic nerves in the choroid plexus, focusing on coexistence of neuropeptide Y, vasoactive intestinal polypeptide and peptide histidine isoleucine. Regul Pept 27:11–26, 1990

    PubMed  CAS  Google Scholar 

  165. Nilsson C, Fahrenkrug J, Lindvall-Axelsson M, et al: Epithelial cells purified from choroid plexus have receptors for vasoactive intestinal polypeptide. Brain Res 542:241–247, 1991 a

    PubMed  CAS  Google Scholar 

  166. Nilsson C, Lindvall-Axelsson M, Owman C: Simultaneous and continuous measurement of choroid plexus blood flow and cerebrospinal fluid production. Effects of vasoactive intestinal polypeptide. J Cereb Blood Flow Metab 11:861–867, 1991 b

    PubMed  CAS  Google Scholar 

  167. Nilsson C, Lindvall-Axelsson M, Owman C: Neuroendocrine regulatory mechanisms in the choroid plexus-cerebrospinal fluid system. Brain Res Rev 17:109–138, 1992

    PubMed  CAS  Google Scholar 

  168. Nógrádi A, Kelly C, Carter ND: Localization of acetazolamide-resistant carbonic anhydrase III in human and rat choroid plexus by immunocytochemistry and in situ hybridisation. Neurosci Lett 151:162–165, 1993

    PubMed  Google Scholar 

  169. Oda Y, Nakanishi I: Ultrastructure of the mouse leptomeninx. J Comp Neurol 225:448–457, 1984

    PubMed  CAS  Google Scholar 

  170. Oda Y, Nakanishi I: Ultrastructure of the caudal portion of the fourth ventricular roof in the mouse. J Comp Neurol 256:299–307, 1987

    PubMed  CAS  Google Scholar 

  171. Ohlsson R, Hedborg F, Holmgren L, et al: Overlapping patterns of IGF2 and H19 expression during human development: biallelic IGF2 expression correlates with a lack of H19 expression. Development 120:361–368, 1994

    PubMed  CAS  Google Scholar 

  172. Ohlsson R, Nyström A, Pfeifer-Ohlsson S, et al: IGF2 is parentally imprinted during human embryogenesis and in the Beckwith-Wiedemann syndrome. Nature Genet 4:94–97, 1993

    PubMed  CAS  Google Scholar 

  173. O’Rahilly R, Müller F, Hutchins GM, et al: Computer ranking of the sequence of appearance of 73 features of the brain and related structures in staged human embryos during the sixth week of development. Am J Anat 180:69–86, 1987

    PubMed  Google Scholar 

  174. O’Rahilly R, Müller F, Hutchins GM, et al: Computer ranking of the sequence of appearance of 40 features of the brain and related structures in staged human embryos during the seventh week of development. Am J Anat 182:295–317, 1988

    PubMed  Google Scholar 

  175. O’Rahilly R, Müller F: Ventricular system and choroid plexuses of the human brain during the embryonic period proper. Am J Anat 189:285–302, 1990

    PubMed  Google Scholar 

  176. Osaka K, Handa H, Matsumoto S, et al: Development of the cerebrospinal fluid pathway in the normal and abnormal human embryos. Childs Brain 6:26–38, 1980

    PubMed  CAS  Google Scholar 

  177. Ostrowski NL, Lolait SJ, Young WS: Cellular localization of vasopressin Via receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. Endocrinology 135:1511–1528, 1994

    PubMed  CAS  Google Scholar 

  178. Osumi-Yamashita N, Ninomiya Y, Doi H, et al: The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev Biol 164:409–419, 1994

    PubMed  CAS  Google Scholar 

  179. Otani H, Tanaka O: Development of the choroid plexus anlage and supraependymal structures in the fourth ventricular roof plate of human embryos: scanning electron microscopic observations. Am J Anat 181:53–66, 1988

    PubMed  CAS  Google Scholar 

  180. Pacheco MA, Marks RW, Schoenwolf GC, et al: Quantification of the initial phases of rapid brain enlargement in the chick embryo. Am J Anat 175:403–411, 1986

    PubMed  CAS  Google Scholar 

  181. Palay SL, Chan-Palay V: Cerebellar cortex. Cytology and organization. Springer, New York, 1974.

    Google Scholar 

  182. Palha JA, Fernandes R, de Escobar GM, et al: Transthyretin regulates thyroid hormone levels in the choroid plexus, but not in the brain parenchyma: study in a transthyretin-null mouse model. Endocrinology 141:3267–3272, 2000

    PubMed  CAS  Google Scholar 

  183. Panrucker DE, Dziegielewska KM, Lorscheider FL, et al: Acute-phase a2-macroglobulin in CSF during development of the fetal rat. Int J Dev Neurosci 1:31–34, 1983

    CAS  Google Scholar 

  184. Paspalas CD, Papadopoulos GC, Michaloudi H: Serotoninergic supraependymal plexus in the ventricular system of the hedgehog: organization principles and functional implications. J Hirnforsch 35:333–342, 1994

    PubMed  CAS  Google Scholar 

  185. Pasqualetti M, Ori M, Castagna M, et al Distribution and cellular localization of the serotonin type 2C receptor messenger mRNA in human brain. Neuroscience 92:601–611, 1999

    PubMed  CAS  Google Scholar 

  186. Pehlemann FW, Sievers J, Berry M: Meningeal cells are involved in foliation, lamination, and neurogenesis of the cerebellum: evidence from 6-hydroxydopamine-in-duced destruction of meningeal cells. Dev Biol 110:136–146, 1985

    PubMed  CAS  Google Scholar 

  187. Pi X, Voogt JL, Grattam DR: Detection of prolactin receptor mRNA in the corpus striatum and substantia nigra of the rat. J Neurosci Res 67:551–558, 2002

    PubMed  CAS  Google Scholar 

  188. Platt JB: Ectodermic origin of the cartilages of the head. Anat Anz 8:506–509, 1893

    Google Scholar 

  189. Platt JB: The development of the cartilaginous skull and of the branchial and hypoglossal musculature in Necturus. Morphol Jahrb 25:375–465, 1898

    Google Scholar 

  190. Powell-Braxton L, Hollingshead P, Warburton C, et al: IGF-I is required for normal embryonic growth in mice. Genes Dev 7:2609–2617, 1993

    PubMed  CAS  Google Scholar 

  191. Puymirat J, Miehle M, Marchand R, et al: Immunocytochemical localization of thyroid hormone receptors in the adult rat brain. Thyroid 1:173–184, 1991

    PubMed  CAS  Google Scholar 

  192. Qin Y, Sato TN: Mouse multidrug resistance 1a/3 gene is the earliest known endothelial cell differentiation marker during blood-brain barrier development. Dev Dyn 202:172–180, 1995

    PubMed  CAS  Google Scholar 

  193. Raidoo DM, Narotam PK, van Dellen J, et al: Cellular orientation of atrial natriuretic peptide in the human brain. J Chem Neuroanat 14:207–213, 1998

    PubMed  CAS  Google Scholar 

  194. Ramsey HJ: Fine structure of the surface of the cerebral cortex of human brain. J Cell Biol 26:323–333, 1965

    PubMed  CAS  Google Scholar 

  195. Rao VV, Dahlheimer JL, Bardgett ME, et al: Choroid plexus epithelial expression of MDR1 P glycoprotein and multidrug resistance-associated protein contribute to the blood-cerebrospinal-fluid drug-permeability barrier. Proc Natl Acad Sci USA 96:3900–3905, 1999

    PubMed  CAS  Google Scholar 

  196. Rascol M, Izard J: The subdural neurothelium of the cranial meninges in rat. Anat Rec 186:429–436, 1976

    PubMed  CAS  Google Scholar 

  197. Rascol M, Izard J: Arachnoidea and subarachnoid spaces of the vault of the skull in man. Acta Neuropathol (Berl) 41:41–44, 1978

    CAS  Google Scholar 

  198. Reese TS, Karnovsky MJ: Fine structural localization of a blood-brain barrier to exogeneous peroxydase. J Cell Biol 34:207–217, 1967

    PubMed  CAS  Google Scholar 

  199. Risau W, Hallmann R, Albrecht U: Differentiation-dependent expression of proteins in brain endothelium during development of the blood-brain barrier. Dev Biol 117:537–545, 1986 a

    PubMed  CAS  Google Scholar 

  200. Risau W, Hallmann R, Albrecht U, et al: Brain induces the expression of an early cell surface marker for blood-brain barrier-specific endothelium. EMBO J 5:3179–3183, 1986 b

    PubMed  CAS  Google Scholar 

  201. Risau W, Wolburg H: Development of the blood-brain barrier. Trends Neurosci 13:174–178, 1990

    PubMed  CAS  Google Scholar 

  202. Risau W, Wolburg H: Reply. Trends Neurosci 14:15, 1991

    Google Scholar 

  203. Roky R, Paut-Pagano L, Goffin V, et al: Distribution of prolactin receptors in the rat forebrain. Immunohisto-chemical study. Neuroendocrinology 63:422–429, 1996

    PubMed  CAS  Google Scholar 

  204. Roussel G, Delaunoy J-P, Nussbaum J-L, et al: Demonstration of a specific localization of carbonic anhydrase C in the glial cells of rat CNS by an immunohistochemical method. Brain Res 160:47–55, 1979

    PubMed  CAS  Google Scholar 

  205. Saunders NR, Dziegielewska KM, Møllgård K: The importance of the blood-brain barrier in fetuses and embryos. Trends Neurosci 14:14, 1991

    PubMed  CAS  Google Scholar 

  206. Schinkel AH, Smit JJM, Van Tellingen O, et al: Disruption of the mouse mdr 1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77:491–502, 1994

    PubMed  CAS  Google Scholar 

  207. Schlosshauer B: Neurothelin: molecular characteristics and developmental regulation in the chick CNS. Development 113:129–140, 1991

    PubMed  CAS  Google Scholar 

  208. Schlosshauer B, Herzog K-H: Neurothelin: an inducible cell surface glycoprotein of blood-brain barrier-specific endothelial cells and distinct neurons. J Cell Biol 110:1261–1274, 1990

    PubMed  CAS  Google Scholar 

  209. Schoenwolf GC: Shaping and bending of the avian neuroepithelium: morphometric analyses. Dev Biol 109:127–139, 1985

    PubMed  CAS  Google Scholar 

  210. Schoenwolf GC: Microsurgical analyses of avian neurulation: separation of medial and lateral tissues. J Comp Neurol 276:498–507, 1988

    PubMed  CAS  Google Scholar 

  211. Schoenwolf GC: Cell movements during neurulation in avian embryos. Development S 2:157–168, 1991

    Google Scholar 

  212. Schoenwolf GC, Alvarez IS: Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106:427–439, 1989

    PubMed  CAS  Google Scholar 

  213. Schoenwolf GC, Desmond ME: Neural tube occlusion precedes rapid brain enlargement. J Exp Zool 230:405–407, 1984 a

    PubMed  CAS  Google Scholar 

  214. Schoenwolf GC, Desmond ME: Descriptive studies of occlusion and reopening of the spinal canal of the early chick embryo. Anat Rec 209:251–263, 1984 b

    PubMed  CAS  Google Scholar 

  215. Schoenwolf GC, Desmond ME: Timing and positioning of reopening of the occluded spinal neurocele in the chick embryo. J Comp Neurol 246:459–466, 1986

    PubMed  CAS  Google Scholar 

  216. Schoenwolf GC, Everaert S, Bortier H, et al: Neural plate-and neural tube-forming potential in isolated epiblast areas in avian embryos. Anat Embryol 179:541–549, 1989

    PubMed  CAS  Google Scholar 

  217. Schoenwolf GC, Sheard P: Shaping and bending of the avian neural plate as analyzed with a fluorescent-histochemical marker. Development 105:17–25, 1989

    PubMed  CAS  Google Scholar 

  218. Schreiber G, Richardson SJ, Prapunpoj P: Structure and expression of the transthyretin gene in the choroid plexus: a model for the study of the mechanisms of evolution. Microsc Res Tech 52:21–30, 2001

    PubMed  CAS  Google Scholar 

  219. Schulingkamp RJ, Pagano TC, Hung D, et al: Insulin receptors and insulin action in the brain: review and clinical implication. Neurosci Biobehav Res 24:855–872, 2000

    CAS  Google Scholar 

  220. Shabo AL, Maxwell DS: The morphology of the arachnoid villi: a light and electron microscopic study in the monkey. J Neurosurg 29:451–463, 1968

    Google Scholar 

  221. Shuangshoti S, Netsky MG: Histogenesis of choroid plexus in man. Am J Anat 118:283–316, 1966

    PubMed  CAS  Google Scholar 

  222. Siegel GJ, Holm C, Schreiber JH, et al: Purification of mouse brain Na+-K+-ATPase catalytic unit, characterization of antiserum, and immunocytochemical localization in cerebellum, choroid plexus, and kidney. J Histochem Cytochem 32:1309–1318, 1984

    PubMed  CAS  Google Scholar 

  223. Sievers J, Mangold U, Berry M: 6-OHDA-induced ectopia of external granule cells in the subarachnoid space covering the cerebellum. Genesis and topography. Cell Tissue Res 230:309–336, 1983

    PubMed  CAS  Google Scholar 

  224. Sievers J, Mangold U, Berry M, et al: Experimental studies on cerebellar foliation. I. A qualitative morphological analysis of cerebellar fissuration defects after neonatal treatment with 6-OHDA in the rat. J Comp Neurol 203:751–769, 1981

    PubMed  CAS  Google Scholar 

  225. Sievers J, Pehlemann F-W, Baumgarten H-G, et al: Selective destruction of meningeal cells by 6-hydroxy-dopamine: a tool to study meningeal-neuroepithelial interaction in brain development. Dev Biol 110:127–135, 1985

    PubMed  CAS  Google Scholar 

  226. Sievers J, Pehlemann FW, Gude S, et al: A time course study of the alterations in the development of the hamster cerebellar cortex after destruction of the overlying meningeal cells with 6-hydroxydopamine on the day of birth. J Neurocytol 23:117–134, 1994 a

    PubMed  CAS  Google Scholar 

  227. Sievers J, Pehlemann FW, Gude S, et al: Meningeal cells organize the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 23:135–149, 1994 b

    PubMed  CAS  Google Scholar 

  228. Sievers J, Von Knebel Doeberitz C, et al: Meningeal cells influence cerebellar development over a critical period. Anat Embryol 175:91–100, 1986

    PubMed  CAS  Google Scholar 

  229. Silverman WF, Walsh RJ, Posner BI: The ontogeny of specific prolactin binding sites in the rat choroid plexus. Dev Brain Res 24:11–19, 1986

    CAS  Google Scholar 

  230. Skinner DC, Malpaux B: High melatonin concentration in third ventricular cerebrospinal fluid are not due to Galen vein blood recirculating through the choroid plexus. Endocrinology 140:4399–4405, 1999

    PubMed  CAS  Google Scholar 

  231. Sly WS, Hu PY: Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem 64:375–401, 1995

    PubMed  CAS  Google Scholar 

  232. Smith JL, Schoenwolf GC: Notochordal induction of cell wedging in the chick neural plate and its role in neural tube formation. J Exp Zool 250:49–62, 1989

    PubMed  CAS  Google Scholar 

  233. Sousa RJ, Tannery NH, Lafer EM: In situ hybridisation mapping of glucocorticoid receptor messenger ribonucleic acid in rat brain. Mol Endocrinol 3:481–494, 1989

    PubMed  CAS  Google Scholar 

  234. Southwell BR, Duan W, Allorn D, et al: Thyroxine transport to the brain: role of protein by the choroid plexus. Endocrinology 133:2116–2126, 1993

    PubMed  CAS  Google Scholar 

  235. Stankov B, Cozzi B, Lucini V, et al: Localization and characterization of melatonin binding sites in the brain of rabbit (Oryctolagus cuniculus) by autoradiography and in vitro ligand-receptor binding. Neurosci Lett 133:68–72, 1991

    PubMed  CAS  Google Scholar 

  236. Stasny F, Lisy V: Cortisol regulation of gamma-glutamyltranspeptidase in liver, choroids plexus, blood plasma and cerebrospinal fluid of developing chick embryo. Dev Neurosci 4:408–415, 1981

    Google Scholar 

  237. Stasny F, Rychter Z: Effect of hydrocorticone on the growth of choroid plexus and composition of cerebrospinal fluid in the developing chick embryo. Acta Neurol Scand 53:260–274, 1976

    Google Scholar 

  238. Sternberger NH, Sternberger LA: Blood-brain barrier protein recognized by monoclonal antibody. Proc Natl Acad Sci USa 84:8169–8173, 1987

    PubMed  CAS  Google Scholar 

  239. Stewart PA, Hayakawa K: Early ultrastructural changes in blood-brain barrier vessels of the rat embryo. Dev Brain Res 78:25–34, 1994

    CAS  Google Scholar 

  240. Stewart PA, Wiley MJ: Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev Biol 84:183–192, 1981

    PubMed  CAS  Google Scholar 

  241. Struckhoff G, Turzynski A: Demonstration of parathyroid hormone-related protein in meninges and its receptor in astrocytes: evidence for a paracrine meningo-astrocytic loop. Brain Res 676:1–9, 1995

    PubMed  CAS  Google Scholar 

  242. Stylianopoulou F, Efstratiadis A, Herbert J, et al: Pattern of the insulin-like growth factor II gene expression during rat embryogenesis. Development 103:497–506, 1988

    PubMed  CAS  Google Scholar 

  243. Super H, Martinez A, Soriano E: Degeneration of Cajal-Retzius cells in the developing cerebral cortex of the mouse after ablation of meningeal cells by 6-hydroxydopamine. Brain Res Dev Brain Res 98:15–20, 1997

    PubMed  CAS  Google Scholar 

  244. Sussenbach JS, Steenbergh PH, Jansen E, et al: Structural and regulatory aspects of the human genes encoding IGF-I and-II. Adv Exp Med Biol 293:1–14, 1991

    PubMed  CAS  Google Scholar 

  245. Thomas T, Dziadek M: Capacity to form choroid plexuslike cells in vitro is restricted to specific regions of the mouse neural ectoderm. Development 117:253–262, 1993

    PubMed  CAS  Google Scholar 

  246. Thomas T, Schreiber G, Jaworowski A: Developmental patterns of gene expression of secreted proteins in brain and choroid plexus. Dev Biol 134:38–47, 1989

    PubMed  CAS  Google Scholar 

  247. Tong Y, Pelletier G: Ontogeny of atrial natriuretic factor (ANF) binding in various areas of rat brain. Neuropeptides 16:63–68, 1990

    PubMed  CAS  Google Scholar 

  248. Toyama E, Doi Y, Kudo H, et al: Diversity in distribution of Na+.K+ATPase of the choroid epithelium of prenatal rats; an immunocytochemical study. Arch Histol Cytol 60:235–244, 1997

    PubMed  CAS  Google Scholar 

  249. Tricoli JV, Rail LB, Scott J, et al: Localization of insulinlike growth factor genes to human chromosome 11 and 12. Nature 310:784–786, 1984

    PubMed  CAS  Google Scholar 

  250. Tsai CE, Daood MJ, Lane RH, et al: P-glycoprotein expression in mouse brain increases with maturation. Biol Neonate 81:58–64, 2002

    PubMed  CAS  Google Scholar 

  251. Tsutsumi M, Skinner MK, Sanders-Bush E: Transferrin gene expression and synthesis by cultured choroid plexus epithelial cells. J Biol Chem 264:9626–9631, 1989

    PubMed  CAS  Google Scholar 

  252. Van Deurs B: Structural aspects of brain barriers, with special reference to the permeability of the cerebral endothelium and choroidal epithelium. Int Rev Cytol 65: 117–191, 1980

    PubMed  Google Scholar 

  253. Van Dijk MA, Van Schaik FMA, Bootsma HJ, et al: Initial characterization of the four promoters of the human insulin-like growth factor II gene. Mol Cell Endocrinol 81:81–94, 1991

    PubMed  Google Scholar 

  254. Vanecek J: Melatonin binding sites. J Neurochem 51:1436–1440, 1988

    PubMed  CAS  Google Scholar 

  255. Vertongen P, Schiffmann SN, Gourlet P, et al: Autoradiographic visualization of the receptor subclasses for vasoactive intestinal poplypeptide (VIP) in rat brain. Peptides 18:1547–1554, 1997

    PubMed  CAS  Google Scholar 

  256. Von Knebel Doeberitz C, Sievers J, Sadler M., et al: Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum. Neuroscience 17:409–426, 1986

    Google Scholar 

  257. Von Schroeder HP, Nishimura E, Mc Intosh CH, et al: Autoradiographic localization of binding sites for atrial natriuretic factor. Can J Physiol Pharmacol 63:1373–1377, 1985

    Google Scholar 

  258. Vorbrodt AW, Lossinsky AS, Wisniewski HM: Localiza tion of alkaline phosphatase activity in endothelia of de veloping and mature mouse blood-brain barrier. Dev Neurosci 8:1–13, 1986

    PubMed  CAS  Google Scholar 

  259. Vulpian MA: Note sur les phénomènes de développement qui se manifestent dans la queue des très-jeunes embryons de grenouille, après qu’on l’a séparée du corps par une section transversale. C R Acad Sci 48:807–811, 1859

    Google Scholar 

  260. Wagner HJ, Pilgrim CH, Brandi J: Penetration and removal of cerebral horseradish peroxidase injected into the cerebrospinal fluid: role of cerebral perivascular spaces, endothelium, and microglia. Acta Neuropathol 27:299–315, 1974

    PubMed  CAS  Google Scholar 

  261. Wakai S, Hirokawa N: Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tissue Res 195:195–203, 1978

    PubMed  CAS  Google Scholar 

  262. Wakai S, Hirokawa N: Development of blood-cerebrospinal fluid barrier to horseradish peroxidase in the avian choroidal epithelium. Cell Tissue Res 214:271–278, 1981

    PubMed  CAS  Google Scholar 

  263. Walsh RJ, Posner BI, Kopri BM, et al: Prolactin binding sites in the rat brain. Science 201:1041–1043, 1978

    PubMed  CAS  Google Scholar 

  264. Watts AG, Sanchez-Watts G, Emanuel JR, et al: Cell-specific expression of mRNAs encoding Na+, K+-ATPase a-and b-subunit isoforms within the rat central nervous system. Proc Natl Acad Sci USa 88:7425–7429, 1991

    PubMed  CAS  Google Scholar 

  265. Weed LH: Studies on cerebro-spinal fluid. III. The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. J Med Res 31:51–91, 1914

    PubMed  CAS  Google Scholar 

  266. Weed LH: The establishment of the circulation of cerebro-spinal fluid. Anat Rec 10:256–258, 1916 a

    Google Scholar 

  267. Weed LH: The formation of the cranial subarachnoid spaces. Anat Rec 10:475–481, 1916 b

    Google Scholar 

  268. Weed LH: The development of the cerebro-spinal spaces in pig and man. Contrib Embryol Carnegie Inst 5:1–116, 1917

    Google Scholar 

  269. Weed LH: The absorption of cerebrospinal fluid into the venous system. Am J Anat 31:191–221, 1923

    CAS  Google Scholar 

  270. Weiss P: Secretory activity of the inner layer of the embryonic mid-brain of the chick as revealed by tissue culture. Anat Rec 58:299–302, 1934

    Google Scholar 

  271. Welch K: The principles of physiology of the cerebrospinal fluid in relation to hydrocephalus including normal pressure hydrocephalus. Adv Neurol 13:247–332, 1975

    PubMed  CAS  Google Scholar 

  272. Wijnholds J, de Lange ECM, Scheffer GL, et al: Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 105:279–285, 2000

    PubMed  CAS  Google Scholar 

  273. Williams LM, Hannah LT, Bassett JM: Melatonin receptors in neonatal pig brain and pituitary gland. J Pineal Res 26:43–49, 1999

    PubMed  CAS  Google Scholar 

  274. Wilting J, Christ B: An experimental and ultrastructural study on the development of the avian choroid plexus. Cell Tissue Res 255:487–494, 1989

    PubMed  CAS  Google Scholar 

  275. Winkelman NW, Fay T: The Pacchionian system, histologic and pathologic changes with particular reference to the idiopathic and symptomatic convulsive states. Arch Neurol Psychiatry 23:44–64, 1930

    Google Scholar 

  276. Wray GA. Echinoderms. In: Gilbert SF, Raunio AM (eds) Embryology, constructing the organism. Sinauer, Sunderland pp. 309–329, 1997

    Google Scholar 

  277. Wright DE, Seroogy RB, Lundgren KH, et al: Comparative localization of serotonin 1A, 1C, and 2 receptor subtype mRNAs in rat brain. J Comp Neurol 351:357–373, 1995

    PubMed  CAS  Google Scholar 

  278. Yamashima T: Functional ultrastructure of cerebrospinal fluid drainage channels in human arachnoid villi. Neurosurgery 22:633–641, 1988

    PubMed  CAS  Google Scholar 

  279. Yoshida Y, Yamada M, Wakabayashi K, et al: Endothelial fenestrae in the rat fetal cerebrum. Dev Brain Res 44:211–219, 1988

    CAS  Google Scholar 

  280. Zaki W: Développement des granulations arachnoïdiennes. Bull Assoc Anat 61:131–138, 1977

    Google Scholar 

  281. Zenker W, Bankoul S, Braun JS: Morphological indications for considerable diffuse reabsorption of cerebrospinal fluid in spinal meninges particularly in the areas of meningeal funnels. Anat Embryol 189:243–258, 1994

    PubMed  CAS  Google Scholar 

  282. Zervas NT, Lisczak TM, Meyberg MR, et al: Cerebrospinal fluid may nourish cerebral vessels through pathways in the adventitia that may be analogous to systemic vasa va-sorum. J Neurosurg 56:475–481, 1982

    PubMed  CAS  Google Scholar 

  283. Zlokovic BV, Mackic JB, Wang L, et al: Differential expression of Na,K-ATPase alpha and beta subunits isoforms at the blood-brain barrier and the choroid plexus. J Biol Chem 268:8019–8025, 1993

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire d’Histologie et Embryologie / UMR CNRS 7000, Faculté de Médecine Pitié-Salpêtrière, Université Paris 6, Paris, France

    Martin Catala

Authors
  1. Martin Catala
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Pediatric Neurosurgery, Santobono-Pausilipon Children’s Hospital, Naples, Italy

    Giuseppe Cinalli MD

  2. Pediatric Neurosurgery, Hôpital Necker-Enfants Malades, Paris, France

    Christian Sainte-Rose MD

  3. Pediatric Neurosurgery, Royal Children’s Hospital, Melbourne, Australia

    Wirginia June Maixner MD

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer-Verlag Italia

About this chapter

Cite this chapter

Catala, M. (2005). Development of the Cerebrospinal Fluid Pathways During Embryonic and Fetal Life in Humans. In: Cinalli, G., Sainte-Rose, C., Maixner, W.J. (eds) Pediatric Hydrocephalus. Springer, Milano. https://doi.org/10.1007/978-88-470-2121-1_2

Download citation

  • DOI: https://doi.org/10.1007/978-88-470-2121-1_2

  • Publisher Name: Springer, Milano

  • Print ISBN: 978-88-470-2173-0

  • Online ISBN: 978-88-470-2121-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation