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The development of the human brain from a closed neural tube at stage 13

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Summary

Twenty-five embryos of stage 13 (28 days) were studied in detail and graphic reconstructions of seven of them were prepared. Thirty or more somitic paris are present, and the maximum is possibly 39. The notochord is almost entirely separated from the neural tube and the alimentary epithelium, and its rostral tip is closely related to the adenohypophysial pocket. Caudal to the cloacal membrane, the caudal eminence is the site of secondary neurulation. The eminence, which usualy contains isolated somites, in the area where new notochord, hindgut, and neural tube are forming. The neural cord develops into neural tube without the intermediate phase of a neural plate (secondary neurulation). Canalization is regular and the lumen is continuous with the central canal. The neural tube is now a closed system, filled with that may be termed “ependymal fluid.” The brain is widening in a dorsoventral direction. Neuromeres are still detectable. The following features are distinguishable: infundibular area of D 2, chiasmatic plate of D 1, “adult” lamina terminalis, and commissural plate (at levels of nasal plates). The beginning of the synencephalon of D 2 can be discerned. The retinal and lens discs are being defined. The mesencephalic flexure continnues to diminish. The midbrain possesses a sulcus limitans, and the tegmentum may show the medial longitudinal fasciculus. The isthmic segment is clearly separated from rhombomere 1. Lateral and ventral longitudinal fasciculi are usually present in the hindbrain, and the common afferent tract is beginning. Somatic and visceral efferent fibres are seen in certain nerves: 6, 12, 5, 7, 9–11. The first indication of the cerebellum may be visible in the alar lamina of rhombomere 1. The terminal-vomeronasal crest appears. Various cranial ganglia (e.g., vestibular, superior ganglia of 9, 10) are forming. The trigeminal ganglion may show its three major divisions. Epipharyngeal placodes of pharyngeal arches 2 to 5 contribute to cranial ganglia 7, 9, and 10. The spinal neural crest is becoming segregated, and the spinal ganglia are in series with the somites. Ventral spinal roots are beginning to develop.

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References

  • Altman J, Bayer SA (1981) Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J Comp Neurol 198:677–716

    Google Scholar 

  • Altman J, Bayer SA (1982) Development of the cranial nerve ganglia and related nuclei in the rat. Adv Anat Embryol Cell Biol 74:1–90

    Google Scholar 

  • Altman J, Bayer SA (1984) The development of the rat spinal cord. Adv Anat Embryol Cell Biol 85:1–166

    Google Scholar 

  • Bartelmez GW, Dekaban AS (1962) The early development of the human brain. Contrib Embryol Carnegie Inst 37:13–32

    Google Scholar 

  • Blechschmidt E (1963) Der menschliche Embryo. Dokumentationen zur kinetischen Anatomie. Schattauer, Stuttgart

    Google Scholar 

  • Blechschmidt E, Gasser RF (1978) Biokinetics and biodynamics of human differentiation. Principles and applications. Thomas, Springfield, II.

    Google Scholar 

  • Bok ST (1915) Die Entwicklung der Hirnnerven und ihrer zentralen Bahnen. Die stimulogene Fibrillation. Folia Neuro Biol 9:475–565

    Google Scholar 

  • Bolli P (1966) Sekundäre Lumenbildungen im Neuralrohr und Rückenmark memschlicher Embryonen. Inaug. Diss. Zürich, Acta Anat 64:48–81

    Google Scholar 

  • Bossy J (1966) Diverticule télencéphalique de la région du neuropore antérieur chez un embryon humain de 35 mm V.C. Bull Assoc Anat 50:200–210

    Google Scholar 

  • Bossy J (1980) Development of olfactory and related structures in staged human embryos. Anat Embryol 161:225–236

    Google Scholar 

  • Brocklehurst G (1978) Spina bifida. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology. North-Holland, Amsterdam, 32:519–578

    Google Scholar 

  • Butler H, Juurlink BHJ (1987) An atlas for staging mammalian and chick embryos. CRC, Boca Raton, Florida

    Google Scholar 

  • Buxton BH (1899) Photographs of a series of section of an early human embryo. J Anat Physiol 33:381–385

    Google Scholar 

  • Cheuk WL, Van de Water TR, Ruben RJ (1978) The fate mapping of the eleventh and twelfth day mouse otocyst: an in vitro study of the sites of origin of the embryonic inner ear sensory structures. J Morphol 157:249–267

    Google Scholar 

  • Couly GF, Le Douarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110:422–439

    Google Scholar 

  • Crosby CE, Humphrey T, Lauer EW (1962) Correlative anatomy of the nervous system. Macmillan, New York

    Google Scholar 

  • D'Amico-Martel A (1982) Temporal patterns of neurogensis in avian cranial sensory and autonomic ganglia. Am J Anat 163:351–372

    Google Scholar 

  • D'Amico-Martel A, Noden DM (1983) Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat 166:445–468

    Google Scholar 

  • Daikoku S (1958) Studies on the human foetal pituitary. 2. on the form and histological development, especially that of the anterior pituitary. Tokushima J Exp Med 5:214–231

    Google Scholar 

  • Davies AM, Lindsay RM (1985) The cranial sensory ganglia in culture: Differences in the response of placode-derived and neural crest-derived neurons to nerve growth factor. Dev Biol 111:62–72

    Google Scholar 

  • Deol MS (1964) The abnormalities of the inner ear in kreisler mice. J Embryol Exp Morphol 12:485–490

    Google Scholar 

  • Ferrand R (1972) Etude expérimentale des facteurs de la différenciation cytologique de l'adénohypophyse chez l'embryon de poulet. Arch Biol 83:297–371

    Google Scholar 

  • Ferrand R (1973) Origine exclusivement ectodermique de l'adénohypophyse chez la Caille: démonstrations par la méthode des associations tissulaires interspécifiques. CR Soc Biol 167:740–743

    Google Scholar 

  • Fol H (1884) L'anatomie d'un embryon humain d'un peu plus de trois semaines. Rec Méd Suisse Rom 4:177–201

    Google Scholar 

  • Fol H (1884) Description d'un embryon humain de cinq millimètres et six dixièmes. Rec Zool Suisse 1:357–401

    Google Scholar 

  • Gage SP (1905) A three weeks' human embryo, with especial reference to the brain and the nephric system. Am J Anat 4:409–443

    Google Scholar 

  • Gilbert MS (1935) Some factors influencing the early development of the mammalian hypophysis. Anat Rec 62:337–359

    Google Scholar 

  • Gilbert PW (1957) The origin and development of the human extrinsic ocular muscles. Contrib Embryol Carnegie Inst 36:59–78

    Google Scholar 

  • Goodrum GR, Jacobson AG (1981) Cephalic flexure formation in the chick embryo. J Exp Zool 216:399–408

    Google Scholar 

  • Gould BB, Rakic P (1981) The total number, time of origin and kinetics of proliferation of neurons comprising the deep cerebellar nuclei in the rhesus monkey. Exp Brain Res 144:195–206

    Google Scholar 

  • His W (1890) Die Entwickelung des menschlichen Rautenhirns vom Ende des ersten bis zum Beginn des dritten Monats. I. Verlängertes Mark. Leipzig

    Google Scholar 

  • His W (1893) Vorschläge zur Einteilung des Gehirns. Arch Anat Entw 172–179

  • Hochstetter F (1939) Über die Entwicklung und Differenzierung der Hüllen des menschlichen Gehirns. Morphol Jahrb 83:359–494

    Google Scholar 

  • Holmdahl DE (1926) Die erste Entwicklung des Körpers bei den Vögeln und Säugetieren, inkl. dem Menschen, besonders mit Rücksicht auf die Bildung des Rückenmarks, des Zöloms und der entodermalen Kloake nebst einem Exkurs über die Entstehung der Spina bifida in der Lumbosacralregion. II–V. Morphol Jahrb 55:112–208

    Google Scholar 

  • Holmdahl DE (1934) Neuralleiste und Ganglienleiste beim Menschen. Z Mikr Anat Forsch 36:137–178

    Google Scholar 

  • Ingalls NW (1907) Beschreibung eines menschlichen Embryos von 4:9 mm. Arch Mikr Anat Entw 70:506–576

    Google Scholar 

  • Jacobson AG, Miyamoto DM, Mai S-H (1979) Rathke's pouch morphogenesis in the chick embryo. J Exp Zool 207:351–365

    Google Scholar 

  • Källén B (1953) On the significance of the neuromeres and similar structures in vertebrate embryos. J Embryol Exp Morphol 1:393–398

    Google Scholar 

  • Kuhlenbeck H (1973) Medulla oblongata (and Pons). Ch. IX vol. 4. In: The central nervous system of vertebrates, vol 4, ch 9. Karger, Basel

    Google Scholar 

  • Kupffer von C (1906) Die Morphogenie des Centralnervensystems. In: Hertwig O (ed) Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere. Fischer, Jena

    Google Scholar 

  • McGrath P (1978) Aspects of the human pharyngeal hypophysis in normal and anencephalic fetuses and neonates and their posible significance in the mechanism of its control. J Anat 127:65–81

    Google Scholar 

  • McPhee JR, Van de Water TR (1986) Epithelial-mesenchymal tissue interactions guiding otic capsule formation: the role of the otocyst. J Embryol Exp Morphol 97:1–24

    Google Scholar 

  • Miale I, Sidman RL (1961) An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4:277–296

    Google Scholar 

  • Morriss-Kay GM (1981) Growth and development of pattern in the cranial neural epithelium of rat embryos during neurulation. J Embryol Exp Morphol 65:225–241

    Google Scholar 

  • Morriss-Kay GM, Tuckett F, Solursch M (1986) The effects of Streptomyces hyaluronidase on tissue organization and cell cycle time in rat embryos. J Embryol Exp Morphol 98:59–70

    Google Scholar 

  • Müller F, O'Rahilly R (1983) The first appearance of the major divisions of the human brain at stage 9. Anat Embryol 168:419–432

    Google Scholar 

  • Müller F, O'Rahilly R (1984) Cerebral dysraphia (future anencephaly) in a human twin embryo at stage 13. Teratology 30:167–177

    Google Scholar 

  • Müller F, O'Rahilly R (1985) The first appearance of the neural tube and optic primordium in the human embryo at stage 10. Anat Embryol 172:157–169

    Google Scholar 

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

    Google Scholar 

  • Müller F, O'Rahilly R (1986b) Somitic-vertebral correlation and vertebral levels in the human embryo. Am J Anat 177:1–19

    Google Scholar 

  • Müller F, O'Rahilly R (1987) The development of the human brain, the closure of the caudal neuropore, and the beginning of secondary neurulation at stage 12. Anat Embryol (in press)

  • Narayanan CH Narayanan Y (1978) Determination of the embryonic origin of the mesencephalic nucleus of the trigeminal nerve in birds. J Embryol Exp Morphol 43:85–105

    Google Scholar 

  • Noden DM (1986) Origins and patterning of craniofacial mesenchymal tissues. J Craniof Genet Dev Biol [Suppl], 2:15–31

    Google Scholar 

  • O'Rahilly R (1963) The early development of the otic vesicle in staged human embryos. J Embryol Exp Morphol 11:741–755

    Google Scholar 

  • O'Rahilly R (1965) The optic, vestibulocochlear, and terminal-vomeronasal neural crest in staged human embryos. In: Rohen JW (ed) Second symposium on eye structure. Schattauer, Stuttgart

    Google Scholar 

  • O'Rahilly R (1966) The early development of the eye in staged human embryos. Contrib Embryol Carnegie Inst 38:1–42

    Google Scholar 

  • O'Rahilly R (1973) The early development of the hypophysis cerebri in staged human embryos. Anat Rec 175:511

    Google Scholar 

  • O'Rahilly R (1983a) The timing and sequence of events in the development of the human endocrine system during the embryonic period proper. Anat Embryol 166:439–451

    Google Scholar 

  • O'Rahilly R (1983b) The timing and sequence of events in the development of the human eye and ear during the embryonic period proper. Anat Embryol 168:87–99

    Google Scholar 

  • O'Rahilly R, Muecke EC (1972) The timing and sequence of events in the development of the human urinary system during the embryonic period proper. Z Anat Entwickl Gesch 138:99–109

    Google Scholar 

  • O'Rahilly R, Müller F (1984a) The early development of the hypoglossal nerve and occipital somites in staged human embryos. Am J Anat 169:237–257

    Google Scholar 

  • O'Rahilly R, Müller F (1984b) Respiratory and alimentary relations in staged human embryos. New embryological data and congenital anomalies. Ann Otol Rhinol Laryngol 93:421–429

    Google Scholar 

  • O'Rahilly R, Müller F (1985) The origin of the ectodermal ring in staged human embryos of the first 5 weeks. Acta Anat 122:145–157

    Google Scholar 

  • O'Rahilly R, Müller F (1986) The meninges in human development. J Neuropath Exp Neurol 45:588–608

    Google Scholar 

  • O'Rahilly R, Müller F (1987) Developmental Stages in Human Embryos, Including a Revision of Streeter's “Horizons” and a Survey of the Carnegie Collection. Carnegie Inst Wash Publication 637

  • O'Rahilly R, Müller F, Hutchins GM, Moore GW (1984) Computer ranking of the sequence of appearance of 100 features of the brain and related structures in staged human embryos during the first 5 weeks of development. Am J Anat 171:243–257

    Google Scholar 

  • O'Rahilly R, Müller F, Hutchins GM, Moore GW (1987) 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

    Google Scholar 

  • Padget DH (1948) The development of the cranial arteries in the human embryo. Contrib Embryol Carnegie Inst 32:205–261

    Google Scholar 

  • Padget DH (1957) The development of the cranial venous system in man, from the viewpoint of comparative anatomy. Contrib Embryol Carnegie Inst 36:79–140

    Google Scholar 

  • Peach R, Koch WE (1977) Morphological observation on mammalian neural crest. J Anat 123:249

    Google Scholar 

  • Pearson AA, Sauter RW, Herrin GR (1964) The accessory nerve and its relation to the upper spinal nerves. Am J Anat 114:371–391

    Google Scholar 

  • Politzer G (1956) Die Entstehung des Ganglion acusticum beim Menschen. Acta Anat 26:1–13

    Google Scholar 

  • Rhines R, Windle WF (1941) The early development of the fasciculus longitudinalis medialis and associated neurons in the rat, cat and man. J Comp Neurol 75:165–189

    Google Scholar 

  • Schoenwolf GC (1977) Tail (end) bud contributions of the posterior region of the chick embryo. J Exp Zool 201:227–245

    Google Scholar 

  • Schoenwolf GC (1984) Histological and ultrastructural studies of secondary neurulation in mouse embryos. Am J Anat 169:361–376

    Google Scholar 

  • Schoenwolf GC, Nichols DH (1984) Histological and ultrastructural studies on the origin of caudal neural crest cells in mouse embryos. J Comp Neurol 222:496–505

    Google Scholar 

  • Seinsch W (1976) Der “Surface-Coat” embryonaler Hohlräume (Rathke-Tasche und Neuralrohr) der Maus. Acta Anat 95:537–544

    Google Scholar 

  • Smits-van Prooije AE (1986) Processes involved in normal and abnormal fusion of the neural walls in murine embryos. Profeschrift, Leiden

  • Streeter GL (1904) The development of the cranial and spinal nerves in the occipital region of the human embryo. Am J Anat 4:83–116

    Google Scholar 

  • Streeter GL (1918a) The histogenesis and growth of the otic capsule and its contained periotic tissue-spaces in the human embryo. Contrib Embryol Carnegie Inst 7:5–54

    Google Scholar 

  • Streeter GL (1918b) The developmental alterations in the vascular system of the brain of the human embryo. Contrib Embryol Carnegie Inst 8:5–38

    Google Scholar 

  • Streeter GL (1942) Developmental horizons in human embryos. Description of age group XI, 13 to 20 somites, and age group-XII, 21 to 29 somites. Contrib Embryol Carnegie Inst 30:211–245

    Google Scholar 

  • Streeter GL (1945) Developmental horizons in human embryos. Description of age group XIII, embryos about 4 or 5 millimeters long, and age group XIV, period of indentation of the lens vesicle. Contrib Embryol Carnegie Inst 31:27–63

    Google Scholar 

  • Svajger A, Kostovic-Knezevic L, Bradamante Z, Wrischer M (1985) Tail gut formation in the rat embryo. Wilhelm Roux's Arch 194:429–432

    Google Scholar 

  • Tam PPL (1984) The histogenetic capacity of tissues in the caudal end of the embryonic axis of the mouse. J Embryol Exp Morphol 82:253–266

    Google Scholar 

  • Tam PPL, Kwong WH (1987) A study on the pattern of alkaline phosphatase activity correlated with observations on silver-impregnated structures in the developing mouse brain. J Anat 150:169–180

    Google Scholar 

  • Tello JF (1923) Les differenciations neuronales dens l'embryon du poulet pendant les premiers jours de l'incubation. Trab Lab Invest Biol (Madrid) 21:1–93

    Google Scholar 

  • Tuckett F, Lim L, Morriss-Kay GM (1985) The ontogenesis of cranial neuromeres in the rat embryo. I. A scanning electron microscope and kinetic study. J Embryol Exp Morphol 87:215–228

    Google Scholar 

  • Tuckett F, Morriss-Kay GM (1985) The ontogenesis of cranial neuromeres in the rat embryo. II. A transmission electron microscope study. J Embryol Exp Morphol 88:231–247

    Google Scholar 

  • Van Campenhout E (1948) La contribution des placodes épiblastiques au développement des ganglions des nerfs crâniens chez l'embryon humain. Arch Biol (Liège) 59:253–266

    Google Scholar 

  • Van de Water TR, Cheuk WL, Ruben RJ, Shea CA (1980) Ontogenic aspects of mammalian inner ear development. Birth Defects: Original Article Series 16:5–45

    Google Scholar 

  • Verbout AJ (1971) Die segmentalen Wellen der Chorda dorsalis. Ein intravitales oder ein postmortales Phänomen? Z Anat Entwickl Gesch 133:172–183

    Google Scholar 

  • Verwoerd CNA, Oostrom CG (1979) Cephalic neural crest and placodes. Adv Anat Embryol Cell Biol 58:1–75

    Google Scholar 

  • Waterson D (1926) The development of the hypophysis cerebri in man, with a note upon its structure in the human adult. Trans R Soc (Edinb) 55:125–145

    Google Scholar 

  • Wentworth LE (1984a) The development of the cervical spinal cord of the mouse embryo. I. A Golgi analysis of ventral root neuron differentiation. J Comp Neurol 222:81–95

    Google Scholar 

  • Wentworth LE (1984b) The development of the cervical spinal cord of the mouse embryo: II. A Golgi analysis of sensory, commissural, and association cell differentiation. J Comp Neurol 222:95–115

    Google Scholar 

  • Wilson DB (1980) Pattern of proliferation in the hypophysis of the mouse embryo. A quantitative autoradiographic study. Anat Embryol 159:101–113

    Google Scholar 

  • Wilson DB (1983) Early development of the otocyst in an exencephalic mutant of the mouse. Acta Anat 117:217–224

    Google Scholar 

  • Wilson DB, Hendrickx AG (1981) Incorporation of tritiated thymidine in the hypophysis of the rhesus monkey (Macaca mulatta) embryo. J Anat 132:19–28

    Google Scholar 

  • Windle WF (1932) The neurofibrillar structure of the 7-mm cat embryo. J Comp Neurol 55:99–138

    Google Scholar 

  • Windle WF (1933) Neurofibrillar development in the central nervous system of cat embryos between 8 and 12 mm long. J Comp Neurol 58:643–723

    Google Scholar 

  • Windle WF (1970) Development of neural elements in human embryos of four to seven weeks gestation. Exp Neurol [Suppl] 5:44–83

    Google Scholar 

  • Windle WF, Baxter RE (1936) The first neurofibrillar development in albino rat embryos. J Comp Neurol 63:173–185

    Google Scholar 

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Supported by research grant No. HD-16702, Institute of Child Health and Human Development, National Institutes of Health (USA)

Herrn Professor Dr. Johannes Lang zu seinem 65. Geburtstag gewidmet in Anerkennung seiner wertvollen Beiträge zur klinischen Anatomie von Kopf und Gehirn

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Müller, F., O'Rahilly, R. The development of the human brain from a closed neural tube at stage 13. Anat Embryol 177, 203–224 (1988). https://doi.org/10.1007/BF00321132

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