Olfactory Structures in Staged Human EmbryosMüller F. · O'Rahilly R.
School of Medicine, University of California, Davis, Calif., USA
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
The olfactory region was investigated in 303 serially sectioned human embryos, 23 of which were controlled by precise graphic reconstructions. The following findings in the embryonic period are new for the human. (1) The nasal plates arise at the neurosomatic junction, as do also the otic placodes. (2) Crest comes from the nasal plates later (stage 13) than the maximum production in the neural folds (stage 10). (3) The crest arises and migrates during a much longer time (at least until the end of the embryonic period) than the neural crest of the head, where origin and migration end at stage 12. (4) Olfactory nerve fibres enter the brain at stage 17, the vomeronasal fibres and those of the nervus terminalis at stages 17 and 18. (5) Fibre connections between the olfactory tubercle and the olfactory bulb, as well as those to the amygdaloid nuclei, forebrain septum, and hippocampus, develop during and after stage 17. (6) Mitral cells appear late in the embryonic period. (7) Localized, although incomplete, lamination of the olfactory bulb is detectable at the embryonic/fetal transition. (8) Tangential migratory streams of neurons, from stage 22 to the early fetal period, proceed from the subventricular zone of the olfactory bulb towards the future claustrum; they remain within the insular region but are separated from the cortical plate. (9) In future cebocephaly morphological indications may be visible as early as stage 13. The various findings are integrated by means of staging, and current information for the fetal period is tabulated from the literature.
© 2004 S. Karger AG, Basel
Alheid, G.F., L. Heimer, R.C. Switzer (1990) Basal ganglia; in Paxinos, G. (ed): The Human Nervous System. San Diego, Academic Press.
Andersen, O., A. Mendoza, W. Kühnel (1995) Der Bulbus olfactorius and der Bulbus olfactorius accessorius bei Nagern and beim Menschen. Verh Anat Ges 90: 198–199.
Bartelmez, G.W., M.P. Blount (1954) The formation of nasal crest from the primary optic vesicle in man. Contrib Embryol Carnegie Inst 35: 55–71.
- Bhatnagar, K.P., R. Kennedy, G. Bar, G.R. Greenberg, et al (1987) Number of mitral cells and the bulb volume in the aging human olfactory bulb: A quantitative morphological study. Anat Rec 218: 73–87.
- Bhatnagar, K.P., T.D. Smith (2001) The human vomeronasal organ. III. Postnatal development from infancy to the ninth decade. J Anat 199: 289–302.
- Bhatnagar, K.P., T.D. Smith (2003) The human vomeronasal organ. V. An interpretation of its discovery by Ruysch, Jacobson, or Kölliker, with an English translation of Kölliker (1877). Anat Rec 270B: 4–15.
- Boehm, N., B. Gasser (1993) Sensory receptor-like cells in the human foetal vomeronasal organ. Neuroreport 4: 867–870.
- Boehm, N., J. Roos, B. Gasser (1994) Luteinizing hormone releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses. Dev Brain Res 82: 175–180.
- Bossy, J. (1980) Development of olfactory and related structures in staged human embryos. Anat Embryol 161: 225–236.
Bossy, J., J. Katz (1964) Note sur la cytoarchitectonie du bulbe olfactif chez l’homme adulte. Bull Assoc Anat 121: 40.
- Boyd, J.G., V.S.M. Kawaja, R. Doucette (2003) Olfactory ensheathing cells: Historical perspective and therapeutic potential. Anat Rec 271B: 49–60.
- Brown, J.W. (1987) The nervus terminalis in insectivorous bat embryos and notes on its presence during human ontogeny. Ann NY Acad Sci 287: 184–200.
- Choi, B.H. (1988) Developmental events during the early stages of cerebral cortical neurogenesis in man. Acta Neuropathol 75: 441–447.
- Chuah, M.I., D.R. Zheng (1987) Olfactory marker protein is present in olfactory receptor cells of human fetuses. Neuroscience 23: 363–370.
- Chuah, M.I., D.R. Zheng (1992) The human primary olfactory pathway: Fine structural and cytochemical aspects during development and in adults. Microsc Res Tech 23: 76–85.
Crosby, C.E., T. Humphrey, E.W. Lauer (1962) Correlative Anatomy of the Nervous System. New York, Macmillan.
- Doucette, R. (1993) Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microsc Res Tech 24: 113–130.
- Dutton, R., P.F. Bartlett (2000) Precursor cells in the subventricular zone of the adult mouse are actively inhibited from differentiating into neurons. Dev Neurosci 22: 96–105.
Feess-Higgins, A., J.-C. Larroche (1987) Le développement du cerveau foetal humain. Atlas anatomique. Paris, INSERM-CNRS, Masson.
- Franklin, R.J.M. (2003) Remyelination by transplanted olfactory ensheathing cells. Anat Rec 271B: 71–76.
- Gadisseux, J.-F., A.M. Goffinet, G. Lyon, P. Evrard (1992) The human transient subpial granular layer. J Comp Neurol 324: 94–114.
Gaunt, P.N., W.A. Gaunt (1978) Three Dimensional Reconstruction in Biology. Tunbridge Wells, Pitman Medical.
- Geuna, S., P. Borrione, M. Fornaro, M.G. Giacobini-Robecchi (2001) Adult stem cells and neurogenesis: Historical roots and state of the art. Anat Rec 265: 132–141.
- Goodman, F.R. (2003) Congenital abnormalities of body patterning: Embryology revisited. Lancet 362: 651–662.
- Halpern, M., A. Marinez-Marcos (2003) Structure and function of the vomeronasal system: An update. Prog Neurobiol 70: 245–318.
- Hinds, J.W. (1968) Autoradiographic study of histogenesis in the mouse olfactory bulb. J Comp Neurol 134: 305–322.
- Hinds, J.W. (1972a) Early neuron differentiation in the mouse olfactory bulb. J Comp Neurol 146: 233–252.
- Hinds, J.W. (1972b) Early neuron differentiation in the mouse olfactory bulb. II. Electron microscopy. J Comp Neurol 146: 253–276.
- Hinrichsen, K. (1985) The early development of morphology and patterns of the face in the human embryo. Adv Anat Embryol Cell Biol 98: 1–79.
His, W. (1904) Die Entwicklung des menschlichen Gehirns während der ersten Monate. Untersuchungsergebnisse. Leipzig, Hirzel.
Hochstetter, F. (1919) Beiträge zur Entwicklungsgeschichte des menschlichen Gehirns. Part 1. Vienna, Deuticke.
- Hongo, T., A. Hakuba, K. Shiota, I. Naruse (2000) Suckling dysfunction caused by defects in the olfactory system in genetic arhinencephalic mice. Biol Neonate 78: 293–299.
- Humphrey, T. (1940) The development of the olfactory and the accessory olfactory formations in human embryos and fetuses. J Comp Neurol 73: 431–468.
- Humphrey, T. (1963) The development of the anterior olfactory nucleus of human fetuses. Prog Brain Res 3: 170–190.
- Humphrey, T. (1967). The development of the human tuberculum olfactorium during the first three months of embryonic life. J Hirnforsch 9: 437–469.
- Humphrey, T. (1968). The development of the human amygdala during early embryonic life. J Comp Neurol 132: 135–165.
- Johnson, E.W., P.M. Eller, B.W. Jafek (1994) Calbindin-like immunoreactivity in epithelial cells of the newborn and adult human vomeronasal organ. Brain Res 638: 329–333.
Keibel, F. (1912) The development of the sense-organs; in Keibel, F., F.P. Mall (eds):Manual of Human Embryology. Philadelphia, Lippincott, vol 2, pp 180–290.
- Kjaer, I., B. Fischer Hansen (1996a) The human vomeronasal organ: Prenatal developmental stages and distribution of luteinizing hormone-releasing hormone. Eur J Oral Sci 104: 34–40.
- Kjaer, I., B. Fischer Hansen (1996b) Luteinizing hormone-releasing hormone and innervation pathways in human prenatal nasal submucosa: Factors of importance in evaluating Kallmann’s syndrome. APMIS 104: 680–688.
- Kordower, J.H., P. Piecinski, P. Rakic (1992) Neurogenesis of the amygdaloid nuclear complex in the rhesus monkey. Dev Brain Res 68: 9–15.
Koya, T. (1963) The forebrain angle of the human embryo (in Japanese). Hirosaki Med J 15: 250–263.
- Kreutzer, E.W., B.W. Jafek (1980) The vomeronasal organ of Jacobson in the human embryo and fetus. Otolaryngol Head Neck Surg 88: 119–123.
Kuhlenbeck H. (1977) Derivatives of the prosencephalon: Diencephalon and telencephalon; in The Central Nervous System of Vertebrates. Basel, Karger, vol 5.
- Liebetanz, D., M.A. Nitsche, C. Fromm, C.K. Reyher (2002) Central olfactory connections in the microsmatic marmoset monkey (Callithrix jacchus). Cells Tissues Organs 172: 53–69.
- Lois, C., A. Alvarez-Buylla (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145–1148.
- Lois, C., J. Garcia-Verdugo, A. Alvarez-Buylla (1996) Chain migration of neuronal precursors. Science 271: 978–981.
- Macchi, G. (1951) The ontogenetic development of the olfactory telencephalon in man. J Comp Neurol 95: 245–305.
- Matsutani, S., N. Yamamoto (2000) Differentiation of mitral cell dendrites in the developing main olfactory bulbs of normal and naris-occluded rats. J Comp Neurol 418: 402–410.
- Menezes, J.R.L., F. Dias, A.V.B. Garson (1998) Restricted distribution of S-phase cells in the anterior subventricular zone of the postnatal mouse forebrain. Anat Embryol 198: 205–211.
- Meyer, G., P. Wahle (1999) The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur J Neurosci 11: 3937–3944.
- Morys, J., M. Bobinski, P. Kozlowski, et al (1993) The pathology of the claustrum in Galloway syndrome indicates the existence of claustro-entorhinal pathway. Folia Morphol 52: 1–9.
- Müller, F., R. O’Rahilly (2002) The two sites of fusion of the neural folds and the two neuropores in the human embryo. Teratology 65: 162–170.
O’Rahilly, R. (1965) The optic, vestibulocochlear, and terminal-vomeronasal neural crest in staged human embryos; in Rohen, J.W. (ed): Eye Structure. Stuttgart, Schattauer, pp 557–664.
O’Rahilly, R. (1967) The early development of the nasal pit in staged human embryos. Anat Rec 157: 380.
- O’Rahilly, R., F. Müller (1985) The origin of the ectodermal ring in staged human embryos of the first 5 weeks. Acta Anat 122: 145–157.
O’Rahilly, R., F. Müller (1987) Developmental Stages in Human Embryos Including a Revision of Streeter’s ‘Horizons’ and a Survey of the Carnegie Collection. Washington, Carnegie Institution of Washington, Publication No 637.
O’Rahilly, R., F. Müller (1999) The Embryonic Human Brain, ed 2. New York, Wiley-Liss.
- O’Rahilly, R., F. Müller (2000) Prenatal ages and stages: Measures and errors. Teratology 61: 382–384.
- Pearson, A.A. (1941a) The development of the nervus terminalis in man. J Comp Neurol 75: 39–66.
- Pearson, A.A. (1941b) The development of the olfactory nerve in man. J Comp Neurol 75: 199–217.
Price, J.L. (1990) Olfaction; in Paxinos, G. (ed): The Human Nervous System.San Diego, Academic Press, pp 979–998.
Price, J.L. (2004) Olfaction; in Paxinos, G., J.D. Mai (eds): The Human Nervous System, ed 2. Amsterdam, Elsevier, pp 1198–1211.
- Pyatkina, G.A. (1982) Development of the olfactory epithelium in man. Z Mikrosk Anat Forsch 96: 361–372.
- Quanbeck, C., N.M. Sherwood, R.P. Millar, E. Terasawa (1997) Two populations of luteinizing hormone-releasing hormone neurons in the forebrain of the rhesus macaque during embryonic development. J Comp Neurol 380: 293–309.
Redmond, L., S. Hockfiled, M. Morabito (1995) Homeobox gene PBX1 is continuously expressed in neurons migrating from the subventricular zone to the olfactory bulb. Experientia 51: 17–28.
- Riddley, A.J., M.A. Schwartz, K. Burridge, et al (2003) Cell migration: Integrating signals from front to back. Science 302: 1704–1709.
- Roslinski, D.L., K.P. Bhatnagar, A.M. Burrows, T.D. Schmith (2000) Comparative morphology and histochemistry of glands associated with the vomeronasal organ in human, mouse lemurs, and voles. Anat Rec 260: 92–101.
Saylam C., R. Besli, A. Veral, B. Karci (2003) The existence of the vomeronasal organ in humans (abstract). Verh Anat Ges Anat Anz Suppl 185: 114.
- Schambra, U.R., K.K. Sulik, P. Petrusz, J.M. Lauder (1989) Ontogeny of cholinergic neurons in the mouse forebrain. J Comp Neurol 288: 101–122.
- Schwanzel-Fukuda, M., D. Blick, D.W. Pfaff (1989) Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome. Mol Brain Res 6: 311–326.
- Schwanzel-Fukuda, M., K.L. Crossin, D.W. Pfaff, et al (1996) Migration of luteinizing hormone-releasing hormone (LHRH) neurons in early human embryos. J Comp Neurol 366: 547–557.
- Shingo, T., C. Gregg, E. Enwere, et al (2003) Pregnancy stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299: 117–120.
Sidman, R.L., P. Rakic (1982) Development of the human central nervous system; in Haymaker, W., R.D. Adams (eds): Histology and Histopathology of the Nervous System. Springfield, Thomas, pp 348–353.
Siebert, J.R., M.M. Cohen, K.K. Sulik, et al (1990) Holoprosencephaly. Craniofacial Embryogenesis and Dysmorphogenesis. New York, Wiley-Liss, pp 59–98.
- Smart, I. (1961) The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116: 325–347.
- Smith, R.L., H. Baker, K. Kolstad, D.C. Spencer, C.A. Greer (1991) Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulb. Brain Res 548: 140–148.
- Smith, T.D, K.P. Bhatnagar (2000) The human vomeronasal organ. II. Prenatal development. J Anat 197: 421–436.
- Smith, T.E., K.P. Bhatnagar, K.L. Shimp, et al (2002) Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates. Anat Rec 267: 166–176.
- Smith, T.E., M.K. Siegel, K.P. Bhatnagar (2001) Reappraisal of the vomeronasal system of catarrhine primates: Ontogeny, morphology, functionality, and persisting questions. Anat Rec 265: 176–192.
Streeter, G.L. (1948) Developmental horizons in human embryos. Description of age groups XV, XVI, XVII, and XVIII. Contrib Embryol 32: 133–203.
- Takahashi, S., T. Iwanaga, Y. Takahashi, et al (1984) Neuron-specific enolase, neurofilament protein and S-100 protein in the olfactory mucosa of human fetuses. Cell Tissue Res 238: 231–234.
- Tarozzo, G., P. Peretto, A. Fasolo (1995) Cell migration from the olfactory placode and the ontogeny of the neuroendocrine compartments. Zoolog Sci 12: 367–383.
- Verney, C., A.E. Amraoui, N. Zecevic (1996) Comigration of tyrosine hydroxylase- and gonadotropin-releasing hormone-immunoreactive neurons in the nasal area of human embryos. Dev Brain Res 97: 251–259.
- Verney, C., C. Lebrand, P. Gaspar (2002) Changing distribution of monoaminergic markers in the developing human cerebral cortex with special emphasis on the serotonin transporter. Anat Rec 267: 87–93.
- Verwoerd, C.D.A, C.G. van Oostrom (1979) Cephalic neural crest and placodes. Adv Anat Embryol Cell Biol 58: 1–75.
- Zecevic, N., C. Verney (1995) Development of the catecholamine neurons in human embryos and fetuses, with special emphasis on the innervation of the cerebral cortex. J Comp Neurol 351: 509–535.
Zilles, K. (2004) Architecture of the human cerebral cortex; in Paxinos, G., J.D. Mai (eds): The Human Nervous System, ed 2. Amsterdam, Elsevier, pp 997–1055.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.