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. 2000 Oct;197(Pt 3):421–436. doi: 10.1046/j.1469-7580.2000.19730421.x

The human vomeronasal organ. Part II: prenatal development

TIMOTHY D SMITH 1 ,, KUNWAR P BHATNAGAR 2
PMCID: PMC1468143  PMID: 11117628

Abstract

During the 20th century, the human vomeronasal organ (VNO) has been controversial regarding its structure, function, and even identity. Despite reports that provide evidence for its presence throughout prenatal and postnatal ontogeny, some studies and numerous textbooks declare its absence in late fetal and postnatal humans. To that end, the present study was designed to establish firmly whether the human VNO is homologous with that of other mammals and whether it degenerates (partially or completely) or persists throughout prenatal development. Fifty human embryos and fetuses (33 d to 32 wk fertilisation age) and 2 neonates were examined by light microscopy. Four embryonic primates (mouse lemurs) were examined for a comparison of VNO embryogenesis. The presence or absence and structural characteristics of the VNO and supporting tissues are described. The first appearance of the VNO was in the form of bilateral epithelial thickenings of the nasal septum, the vomeronasal primordium. The primordia invaginated between 37 and 43 d of age and formed the tubular VNO. The tubular VNO was located dorsally at a variable distance from, but was always spatially separated from the paraseptal cartilages. The mouse lemurs examined in this study and other reports from the literature indicate that the human VNO resembles that of primates having functional VNOs until just after a tubular VNO is formed. Examination of the VNO and adjacent tissues suggested that the VNO may lose receptor cells and corresponding vomeronasal nerves and become a ciliated, pseudostratified epithelium between ∼ 12 and 14 wk of age. Our findings indicate the prenatal human VNO goes through 3 successive stages: early morphogenesis, transformation (of the epithelium), and growth. These observations indicated that (1) all embryonic humans develop a vomeronasal organ which is homologous with the VNOs of other mammals, but which has become displaced and highly variable in relative location during embryogenesis; (2) the human vomeronasal organ does not degenerate prenatally, but very likely loses the functional components of the vomeronasal complex of other mammals; and (3) the remnant of the human VNO persists until birth and beyond.

Keywords: Human vomeronasal organ, Jacobson's organ, craniofacial development, Microcebus murinus , Microcebus myoxinus

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Selected References

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  1. Bhatnagar K. P., Kallen F. C. Morphology of the nasal cavities and associated structures in Artibeus jamaicensis and Myotis lucifugus. Am J Anat. 1974 Feb;139(2):167–189. doi: 10.1002/aja.1001390203. [DOI] [PubMed] [Google Scholar]
  2. Bhatnagar K. P., Kennedy R. C., Baron G., Greenberg R. A. Number of mitral cells and the bulb volume in the aging human olfactory bulb: a quantitative morphological study. Anat Rec. 1987 May;218(1):73–87. doi: 10.1002/ar.1092180112. [DOI] [PubMed] [Google Scholar]
  3. Bhatnagar K. P., Meisami E. Vomeronasal organ in bats and primates: extremes of structural variability and its phylogenetic implications. Microsc Res Tech. 1998 Dec 15;43(6):465–475. doi: 10.1002/(SICI)1097-0029(19981215)43:6<465::AID-JEMT1>3.0.CO;2-1. [DOI] [PubMed] [Google Scholar]
  4. Bhatnagar K. P., Wible J. R., Karim K. B. Development of the vomeronasal organ in Rousettus leschenaulti (Megachiroptera, Pteropodidae). J Anat. 1996 Feb;188(Pt 1):129–135. [PMC free article] [PubMed] [Google Scholar]
  5. Boehm N., Gasser B. Sensory receptor-like cells in the human foetal vomeronasal organ. Neuroreport. 1993 Jul;4(7):867–870. doi: 10.1097/00001756-199307000-00007. [DOI] [PubMed] [Google Scholar]
  6. Boehm N., Roos J., Gasser B. Luteinizing hormone-releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses. Brain Res Dev Brain Res. 1994 Oct 14;82(1-2):175–180. doi: 10.1016/0165-3806(94)90160-0. [DOI] [PubMed] [Google Scholar]
  7. Bossy J. Development of olfactory and related structures in staged human embryos. Anat Embryol (Berl) 1980;161(2):225–236. doi: 10.1007/BF00305346. [DOI] [PubMed] [Google Scholar]
  8. Breipohl W., Bhatnagar K. P., Blank M., Mendoza A. S. Intraepithelial blood vessels in the vomeronasal neuroepithelium of the rat. A light and electron microscopic study. Cell Tissue Res. 1981;215(3):465–473. doi: 10.1007/BF00233523. [DOI] [PubMed] [Google Scholar]
  9. Breipohl W., Bhatnagar K. P., Mendoza A. Fine structure of the receptor-free epithelium in the vomeronasal organ of the rat. Cell Tissue Res. 1979 Sep 1;200(3):383–395. doi: 10.1007/BF00234850. [DOI] [PubMed] [Google Scholar]
  10. Brown J. W. The nervus terminalis in insectivorous bat embryos and notes on its presence during human ontogeny. Ann N Y Acad Sci. 1987;519:184–200. doi: 10.1111/j.1749-6632.1987.tb36297.x. [DOI] [PubMed] [Google Scholar]
  11. Burdi A. R. Cephhalometric growth analyses of the human upper face region during the last two trimesters of gestation. Am J Anat. 1969 May;125(1):113–122. doi: 10.1002/aja.1001250106. [DOI] [PubMed] [Google Scholar]
  12. Burdi A. R., Kusnetz A. B., Venes J. L., Gebarski S. S. The natural history and pathogenesis of the cranial coronal ring articulations: implications in understanding the pathogenesis of the Crouzon craniostenotic defects. Cleft Palate J. 1986 Jan;23(1):28–39. [PubMed] [Google Scholar]
  13. Chouard C. H., Peytral C., Zaouche A. L'organe voméro-nasal de Jacobson. Ann Otolaryngol Chir Cervicofac. 1972 Jun;89(6):341–348. [PubMed] [Google Scholar]
  14. Ciges M., Labella T., Gayoso M., Sanchez G. Ultrastructure of the organ of Jacobson and comparative study with olfactory mucosa. Acta Otolaryngol. 1977 Jan-Feb;83(1-2):47–58. doi: 10.3109/00016487709128812. [DOI] [PubMed] [Google Scholar]
  15. Cooper J. G., Bhatnagar K. P. Comparative anatomy of the vomeronasal organ complex in bats. J Anat. 1976 Dec;122(Pt 3):571–601. [PMC free article] [PubMed] [Google Scholar]
  16. GOMORI G. A rapid one-step trichrome stain. Am J Clin Pathol. 1950 Jul;20(7):661–664. doi: 10.1093/ajcp/20.7_ts.661. [DOI] [PubMed] [Google Scholar]
  17. Garrosa M., Gayoso M. J., Esteban F. J. Prenatal development of the mammalian vomeronasal organ. Microsc Res Tech. 1998 Jun 15;41(6):456–470. doi: 10.1002/(SICI)1097-0029(19980615)41:6<456::AID-JEMT2>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  18. Garrosa M., Iñiguez C., Fernandez J. M., Gayoso M. J. Developmental stages of the vomeronasal organ in the rat: a light and electron microscopic study. J Hirnforsch. 1992;33(2):123–132. [PubMed] [Google Scholar]
  19. ISHIMITSU K. Uber die Entwicklung der Drüsen des Vomeronasalorgans beim Menschen. Yokohama Med Bull. 1958 Jun;9(3):148–156. [PubMed] [Google Scholar]
  20. Johnson A., Josephson R., Hawke M. Clinical and histological evidence for the presence of the vomeronasal (Jacobson's) organ in adult humans. J Otolaryngol. 1985 Apr;14(2):71–79. [PubMed] [Google Scholar]
  21. Johnson E. W., Eller P. M., Jafek B. W. Calbindin-like immunoreactivity in epithelial cells of the newborn and adult human vomeronasal organ. Brain Res. 1994 Feb 28;638(1-2):329–333. doi: 10.1016/0006-8993(94)90666-1. [DOI] [PubMed] [Google Scholar]
  22. Keverne E. B. The vomeronasal organ. Science. 1999 Oct 22;286(5440):716–720. doi: 10.1126/science.286.5440.716. [DOI] [PubMed] [Google Scholar]
  23. Kjaer I., Fischer Hansen B. The human vomeronasal organ: prenatal developmental stages and distribution of luteinizing hormone-releasing hormone. Eur J Oral Sci. 1996 Feb;104(1):34–40. doi: 10.1111/j.1600-0722.1996.tb00043.x. [DOI] [PubMed] [Google Scholar]
  24. Kjaer I., Hansen B. F. Luteinizing hormone-releasing hormone and innervation pathways in human prenatal nasal submucosa: factors of importance in evaluating Kallmann's syndrome. APMIS. 1996 Sep;104(9):680–688. doi: 10.1111/j.1699-0463.1996.tb04929.x. [DOI] [PubMed] [Google Scholar]
  25. Kreutzer E. W., Jafek B. W. The vomeronasal organ of Jacobson in the human embryo and fetus. Otolaryngol Head Neck Surg (1979) 1980 Mar-Apr;88(2):119–123. doi: 10.1177/019459988008800203. [DOI] [PubMed] [Google Scholar]
  26. Loo S. K. A comparative study of the nasal fossa of four nonhuman primates. Folia Primatol (Basel) 1973;20(5):410–422. doi: 10.1159/000155588. [DOI] [PubMed] [Google Scholar]
  27. Maier W. The nasopalatine duct and the nasal floor cartilages in catarrhine primates. Z Morphol Anthropol. 1997;81(3):289–300. [PubMed] [Google Scholar]
  28. Meisami E., Bhatnagar K. P. Structure and diversity in mammalian accessory olfactory bulb. Microsc Res Tech. 1998 Dec 15;43(6):476–499. doi: 10.1002/(SICI)1097-0029(19981215)43:6<476::AID-JEMT2>3.0.CO;2-V. [DOI] [PubMed] [Google Scholar]
  29. Meisami E., Mikhail L., Baim D., Bhatnagar K. P. Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann N Y Acad Sci. 1998 Nov 30;855:708–715. doi: 10.1111/j.1749-6632.1998.tb10649.x. [DOI] [PubMed] [Google Scholar]
  30. Mendoza A. S., Küderling I., Kuhn H. J., Kühnel W. The vomeronasal organ of the New World monkey Saguinus fuscicollis (Callitrichidae). A light and transmission electron microscopic study. Ann Anat. 1994 Jun;176(3):217–222. doi: 10.1016/s0940-9602(11)80481-4. [DOI] [PubMed] [Google Scholar]
  31. Monti-Bloch L., Diaz-Sanchez V., Jennings-White C., Berliner D. L. Modulation of serum testosterone and autonomic function through stimulation of the male human vomeronasal organ (VNO) with pregna-4,20-diene-3,6-dione. J Steroid Biochem Mol Biol. 1998 Apr;65(1-6):237–242. doi: 10.1016/s0960-0760(98)00025-9. [DOI] [PubMed] [Google Scholar]
  32. Monti-Bloch L., Jennings-White C., Berliner D. L. The human vomeronasal system. A review. Ann N Y Acad Sci. 1998 Nov 30;855:373–389. doi: 10.1111/j.1749-6632.1998.tb10595.x. [DOI] [PubMed] [Google Scholar]
  33. Moran D. T., Jafek B. W., Rowley J. C., 3rd The vomeronasal (Jacobson's) organ in man: ultrastructure and frequency of occurrence. J Steroid Biochem Mol Biol. 1991 Oct;39(4B):545–552. doi: 10.1016/0960-0760(91)90251-y. [DOI] [PubMed] [Google Scholar]
  34. Nakashima T., Kimmelman C. P., Snow J. B. Vomeronasal organs and nerves of Jacobson in the human fetus. Acta Otolaryngol. 1985 Mar-Apr;99(3-4):266–271. doi: 10.3109/00016488509108907. [DOI] [PubMed] [Google Scholar]
  35. Ortmann R. Uber Sinneszellen am fetalen vomeronasalen Organ des Menschen. Ein Beitrag zur Variabilität seiner Differenzierung bzw. Rudimentierung. HNO. 1989 May;37(5):191–197. [PubMed] [Google Scholar]
  36. Sandham A. Embryonic facial vertical dimension and its relationship to palatal shelf elevation. Early Hum Dev. 1985 Dec;12(3):241–245. doi: 10.1016/0378-3782(85)90145-8. [DOI] [PubMed] [Google Scholar]
  37. Sherwood R. J., McLachlan J. C., Aiton J. F., Scarborough J. The vomeronasal organ in the human embryo, studied by means of three-dimensional computer reconstruction. J Anat. 1999 Oct;195(Pt 3):413–418. doi: 10.1046/j.1469-7580.1999.19530413.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Siegel M. I., Todhunter J. S., Kimes K. R., Mooney M. P. Human fetal specimens available. Cleft Palate J. 1984 Apr;21(2):115–116. [PubMed] [Google Scholar]
  39. Smith T. D., Siegel M. I., Burrows A. M., Mooney M. P., Burdi A. R., Fabrizio P. A., Clemente F. R. Searching for the vomeronasal organ of adult humans: preliminary findings on location, structure, and size. Microsc Res Tech. 1998 Jun 15;41(6):483–491. doi: 10.1002/(SICI)1097-0029(19980615)41:6<483::AID-JEMT4>3.0.CO;2-O. [DOI] [PubMed] [Google Scholar]
  40. Smith T. D., Siegel M. I., Mooney M. P., Burdi A. R., Burrows A. M., Todhunter J. S. Prenatal growth of the human vomeronasal organ. Anat Rec. 1997 Jul;248(3):447–455. doi: 10.1002/(SICI)1097-0185(199707)248:3<447::AID-AR18>3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  41. Smith T. D., Siegel M. I., Mooney M. P., Burdi A. R., Todhunter J. S. Vomeronasal organ growth and development in normal and cleft lip and palate human fetuses. Cleft Palate Craniofac J. 1996 Sep;33(5):385–394. doi: 10.1597/1545-1569_1996_033_0385_vogadi_2.3.co_2. [DOI] [PubMed] [Google Scholar]
  42. Stensaas L. J., Lavker R. M., Monti-Bloch L., Grosser B. I., Berliner D. L. Ultrastructure of the human vomeronasal organ. J Steroid Biochem Mol Biol. 1991 Oct;39(4B):553–560. doi: 10.1016/0960-0760(91)90252-z. [DOI] [PubMed] [Google Scholar]
  43. Takami S., Getchell M. L., Chen Y., Monti-Bloch L., Berliner D. L., Stensaas L. J., Getchell T. V. Vomeronasal epithelial cells of the adult human express neuron-specific molecules. Neuroreport. 1993 Apr;4(4):375–378. doi: 10.1097/00001756-199304000-00008. [DOI] [PubMed] [Google Scholar]
  44. Vaccarezza O. L., Sepich L. N., Tramezzani J. H. The vomeronasal organ of the rat. J Anat. 1981 Mar;132(Pt 2):167–185. [PMC free article] [PubMed] [Google Scholar]
  45. Wilson D. B., Hendrickx A. G. Quantitative aspects of proliferation in the nasal epithelium of the rhesus monkey embryo. J Embryol Exp Morphol. 1977 Apr;38:217–226. [PubMed] [Google Scholar]
  46. YOUSSEF E. H. Jacobson's organ and the nasal floor cartilages in a 34mm crown-rump length embryo. J Egypt Med Assoc. 1962;45:404–413. [PubMed] [Google Scholar]
  47. Zingeser M. R. The nasopalatine ducts and associated structures in the rhesus monkey (Macaca mulatta): topography, prenatal development, function, and phylogeny. Am J Anat. 1984 Aug;170(4):581–595. doi: 10.1002/aja.1001700406. [DOI] [PubMed] [Google Scholar]
  48. Zuri I., Fishelson L., Terkel J. Morphology and cytology of the nasal cavity and vomeronasal organ in juvenile and adult blind mole rats (Spalax ehrenbergi). Anat Rec. 1998 Aug;251(4):460–471. doi: 10.1002/(SICI)1097-0185(199808)251:4<460::AID-AR5>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]

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