Vomeronasal versus olfactory epithelium: Is there a cellular basis for human vomeronasal perception?

International Review of Cytology

Volumn 248, Issue , 2006, Pages 209-259

  Witt, Martin ^a,b   Hummel, Thomas ^b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF DRESDEN MEDICAL SCHOOL   (Germany)

Author keywords

Chemoreception; Immunohistochemistry; Neuroanatomy; Olfaction; Pheromones; Vomeronasal organ

Indexed keywords

AQUAPORIN; CAVEOLIN; CELL ADHESION MOLECULE; CYTOKERATIN; EZRIN; GONADORELIN; HERMES ANTIGEN; HYALURONIC ACID; INTEGRIN; LECTIN; MARKER; PHEROMONE; VIMENTIN;

APOPTOSIS; CHEMORECEPTOR; CRANIAL NERVE; HISTOCHEMISTRY; HISTOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT; NERVE CELL; NONHUMAN; OLFACTORY BULB; OLFACTORY EPITHELIUM; OLFACTORY NERVE; OLFACTORY SYSTEM; PERCEPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SENSE ORGAN; SMELLING; TERMINAL NERVE; VERTEBRATE; VOMERONASAL ORGAN;

ANIMALS; ANTIGENS, CD44; AQUAPORINS; CAVEOLINS; HUMANS; INTEGRINS; INTERMEDIATE FILAMENTS; LECTINS; MORPHOGENESIS; OLFACTORY MUCOSA; PHEROMONES; SMELL; VOMERONASAL ORGAN;

ANIMALIA; VERTEBRATA;

EID: 32544457537     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7696(06)48004-9     Document Type: Review

References (244)

1. Abo T., and Balch C.M. A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1) J. Immunol. 127 1981 1024 1029
2. Abolmaali N.D., Kuhnau D., Knecht M., Kohler K., Hüttenbrink K.B., and Hummel T. Imaging of the human vomeronasal duct Chem. Senses 26 2001 35 39
3. Anton W. Beiträge zur Kenntnis des Jacobson'schen Organes bei Erwachsenen Zeitschr. Heilk. 16 1895 355 372
4. Asan E., and Drenckhahn D. Immunocytochemical characterization of two types of microvillar cells in rodent olfactory epithelium Histochem. Cell Biol. 123 2005 157 168
5. Astic L., Pellier-Monnin V., and Godinot F. Spatio-temporal patterns of ensheathing cell differentiation in the rat olfactory system during development Neuroscience 84 1998 295 307
6. Au E., and Roskams A.J. Olfactory ensheathing cells of the lamina propria in vivo and in vitro Glia 41 2003 224 236
7. Barondes S.H., Cooper D.N.W., Gitt M.A., and Leffler H. Galectins. Structure and function of a large family of animal lectins J. Biol. Chem. 269 1994 20807 20810
8. Beauchamp G.K., Doty R.L., Moulton D.G., and Mugford R.A. The pheromone concept in mammalian chemical communication: A critique R.L. Doty "Mammalian Olfaction, Reproductive Processes, and Behavior" 1976 Academic Press New York 143 160
9. Belluscio L., Koentges G., Axel R., and Dulac C. A map of pheromone receptor activation in the mammalian brain Cell 97 1999 209 220
10. Besli R., Saylam C., Veral A., Karl B., and Ozek C. The existence of the vomeronasal organ in human beings J. Craniofac. Surg. 15 2004 730 735
11. Bhatnagar K.P., and Meisami E.P. Vomeronasal organ in bats and primates: Extremes of structural variability and its phylogenetic implications Microsc. Res. Tech. 43 1998 465 475
12. Bhatnagar K.P., and Reid K.H. The human vomeronasal organ - I: Historical perspectives. A study of Ruysch's (1703) and Jacobson's (1811) reports on the vomeronasal organ with comparative comments and English translations Biomed. Res. 7 1996 219 229
13. Bhatnagar K.P., and Smith T.D. The human vomeronasal organ. III. Postnatal development from infancy to the ninth decade J. Anat. 199 2001 289 302
14. Bhatnagar K.P., and Smith T.D. The human vomeronasal organ. V. An interpretation of its discovery by Ruysch, Jacobson, or Kolliker, with an English translation of Kolliker (1877) Anat. Rec. 270B 2003 4 15
15. Bhatnagar K.P., Smith T.D., and Winstead W. The human vomeronasal organ: Part IV. Incidence, topography, endoscopy, and ultrastructure of the nasopalatine recess, nasopalatine fossa, and vomeronasal organ Am. J. Rhinol. 16 2002 343 350
16. Bigiani A., Mucignat-Caretta C., Montani G., and Tirindelli R. Pheromone reception in mammals Rev. Physiol. Biochem. Pharmacol. 2005 DOI: 10.1007/s10254-004-0038-0.
17. Boehm N., and Gasser B. Sensory receptor-like cells in the human foetal vomeronasal organ Neuroreport 4 1993 867 870
18. Boehm N., Roos J., and Gasser B. Luteinizing hormone-releasing hormone (LHRH)-expressing cells in the nasal septum of human fetuses Brain Res. Dev. Brain Res. 82 1994 175 180
19. Breer H. Molecular reaction cascades in olfactory signal transduction J. Steroid Biochem. Mol. Biol. 39 1991 621 625
20. Brookover C. The peripheral distribution of the nervus terminalis in an infant J. Comp. Neurol. 28 1917 349 360
21. Brown D., Katsura T., Kawashima M., Verkman A.S., and Sabolic I. Cellular distribution of the aquaporins: A family of water channel proteins Histochem. Cell Biol. 104 1995 1 9
22. Buck L. Information coding in the vertebrate olfactory system Annu. Rev. Neurosci. 19 1996 517 544
23. Buck L., and Axel R. A novel multigene family may encode odorant receptors: A molecular basis for odor recognition Cell 65 1991 175 187
24. Calof A.L., Campanero M.R., O'Rear J.J., Yurchenco P.D., and Lander A.D. Domain-specific activation of neuronal migration and neurite outgrowth-promoting activities of laminin Neuron 13 1994 117 130
25. Chuah M.I., and Zheng D.R. Olfactory marker protein is present in olfactory receptor cells of human fetuses Neuroscience 23 1987 363 370
26. Cloutier J.F., Giger R.J., Koentges G., Dulac C., Kolodkin A.L., and Ginty D.D. Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons Neuron 33 2002 877 892
27. Cloutier J.-F., Sahay A., Chang E.C., Tessier-Lavigne M., Dulac C., Kolodkin A.L., and Ginty D.D. Differential requirements for semaphorin 3F and slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections J. Neurosci. 24 2004 9087 9096
28. Comte I., Mathonnet M., Chevalier G., and Ayer Le-Lievre C. Developmental changes of keratin expression in chick embryo olfactory epithelium in relation to cellular differentiation and neurogenesis in vivo and in vitro Brain Res. Dev. Brain Res. 148 2004 1 10
29. Crandall J.E., Dibble C., Butler D., Pays L., Ahmad N., Kostek C., Puschel A.W., and Schwarting G.A. Patterning of olfactory sensory connections is mediated by extracellular matrix proteins in the nerve layer of the olfactory bulb J. Neurobiol. 45 2000 195 206
30. Cummings D.M., and Brunjes P.C. Migrating luteinizing hormone-releasing hormone (LHRH) neurons and processes are associated with a substrate that expresses S100 Brain Res. Dev. Brain Res. 88 1995 148 157
31. Cutler W.B., Preti G., Krieger A., Huggins G.R., Garcia C.R., and Lawley H.J. Human axillary secretions influence women's menstrual cycles: The role of donor extract from men Horm. Behav. 20 1986 463 473
32. Daikoku S. The olfactory origin of luteinizing hormone-releasing hormone (LHRH) neurons. A new era in reproduction physiology Arch. Histol. Cytol. 62 1999 107 117
33. Dawson M.E., Schell A.M., and Filion D.L. The electrodermal system J.T. Caccioppo L.G. Tassinary G. Berntson "Handbook of Psychophysiology" 2000 Cambridge University Press Cambridge, UK 200 223
34. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., Zufall F., and Mombaerts P. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes Nature 419 2002 70 74
35. Dorries K.M., Adkins-Regan E., and Halpern B.P. Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in domestic pigs Brain Behav. Evol. 49 1997 53 62
36. Drapkin P.T., Monard D., and Silverman A.J.P. The role of serine proteases and serine protease inhibitors in the migration of gonadotropin-releasing hormone neurons BMC Dev. Biol. 2 2002 1
37. Dulac C., and Axel R. A novel family of genes encoding putative pheromone receptors in mammals Cell 83 1995 195 206
38. Dulac C., and Torello A.T. Molecular detection of pheromone signals in mammals: From genes to behaviour Nat. Rev. Neurosci. 4 2003 551 562
39. Dursy E. Atlas zur Entwicklungsgeschichte des Kopfes des Menschen und der höheren Wirbelthiere 1869 Laupp'sche Buchhandlung Tübingen 135 139
40. Eisthen H.L. Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates Microsc. Res. Tech. 23 1992 1 21
41. Eisthen H.L. Evolution of vertebrate olfactory systems Brain Behav. Evol. 50 1997 222 233
42. Eisthen H.L., Delay R.J., Wirsig-Wiechmann C.R., and Dionne V.E. Neuromodulatory effects of gonadotropin releasing hormone on olfactory receptor neurons J. Neurosci. 20 2000 3947 3955
43. Elsaesser R., Montani G., Tirindelli R., and Paysan J. Phosphatidyl-inositide signalling proteins in a novel class of sensory cells in the mammalian olfactory epithelium Eur. J. Neurosci. 21 2005 2692 2700
44. Farbman A.I. Cell biology of olfactory epithelium T.E. Finger W. Silver D. Restrepo "The Neurobiology of Taste and Smell" 2000 Wiley-Liss New York 131 158
45. Finger T.E., Böttger B., Hansen A., Anderson K.T., Alimohammadi H., and Silver W.L. Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration Proc. Natl. Acad. Sci. USA 100 2003 8981 8986
46. Franke W.W., Schmid E., Osborn M., and Weber K. Different intermediate-sized filaments distinguished by immunofluorescence microscopy Proc. Natl. Acad. Sci. USA 75 1978 5034 5038
47. Fueshko S.M., Key S., and Wray S. GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants J. Neurosci. 18 1998 2560 2569
48. Fuller G.N., and Burger P.C. Nervus terminalis (cranial nerve zero) in the adult human Clin. Neuropathol. 9 1990 279 283
49. Gaafar H.A., Tantawy A.A., Melis A.A., Hennawy D.M., and Shehata H.M. The vomeronasal (Jacobson's) organ in adult humans: Frequency of occurrence and enzymatic study Acta Otolaryngol. (Stockh.) 118 1998 409 412
50. Gaikwad A., Biju K.C., Muthal P.L., Saha S., and Subhedar N. Role of neuropeptide Y in the regulation of gonadotropin releasing hormone system in the forebrain of Clarias batrachus (Linn.): Immunocytochemistry and high performance liquid chromatography-electrospray ionization-mass spectrometric analysis Neuroscience 133 2005 267 279
51. Gamble J.A., Karunadasa D.K., Pape J.-R., Skynner M.J., Todman M.G., Bicknell R.J., Allen J.P., and Herbison A.E. Disruption of ephrin signaling associates with disordered axophilic migration of the gonadotropin-releasing hormone neurons J. Neurosci. 25 2005 3142 3150
52. Garcia-Velasco J., and Mondragon M. The incidence of the vomeronasal organ in 1000 human subjects and its possible clinical significance J. Steroid Biochem. Mol. Biol. 1991 561 563
53. Garrosa M., Gayoso M.J., and Esteban F.J. Prenatal development of the mammalian vomeronasal organ Microsc. Res. Tech. 41 1998 456 470
54. Gerber J.C., Lundstrom J.N., Frasnelli F., Knecht M., Olsson M., and Hummel T. Cortical response to androstadienone with or without functional occlusion of the vomeronasal duct - a functional magnetic resonance imaging study Chem. Senses 30 2005 A79
55. Gheri G., Gheri Bryk S., and Balboni G.C. Identification of sugar residues in human fetal olfactory epithelium using lectin histochemistry Acta Anat. (Basel) 145 1992 167 174
56. Giacobini P., Giampietro C., Fioretto M., Maggi R., Cariboni A., Perroteau I., and Fasolo A. Hepatocyte growth factor/scatter factor facilitates migration of GN-11 immortalized LHRH neurons Endocrinology 143 2002 3306 3315
57. Gillenwater A., Xu X.C., el-Naggar A.K., Clayman G.L., and Lotan R. Expression of galectins in head and neck squamous cell carcinoma Head Neck 18 1996 422 432
58. Giorgi D., and Rouquier S. Identification of V1R-like putative pheromone receptor sequences in non-human primates. Characterization of V1R pseudogenes in marmoset, a primate species that possesses an intact vomeronasal organ Chem. Senses 27 2002 529 537
59. Giorgi D., Friedman C., Trask B.J., and Rouquier S. Characterization of nonfunctional V1R-like pheromone receptor sequences in human Genome Res. 10 2000 1979 1985
60. Goldstein I., Hughes R.C., Monsigny M., and Osawa T.N.S. What should be called a lectin? Nature 285 1980 66
61. Gower D.B., and Ruparelia B.A. Olfaction in humans with special reference to odorous 16-androstenes: Their occurrence, perception and possible social, psychological and sexual impact J. Endocrinol. 137 1993 167 187
62. Grosser B.I., Monti-Bloch L., Jennings-White C., and Berliner D.L. Behavioral and electrophysiological effects of androstadienone, a human pheromone Psychoneuroendocrinology 25 2000 289 299
63. Grus W.E., Shi P., Zhang Y.P., and Zhang J. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals Proc. Natl. Acad. Sci. USA 102 2005 5767 5772
64. Halpern M., and Martinez-Marcos A. Structure and function of the vomeronasal system: An update Prog. Neurobiol. 70 2003 245 318
65. Heilmann S., Hummel T., Margolis F.L., Kasper M., and Witt M. Immunohistochemical distribution of galectin-1, galectin-3, and olfactory marker protein in human olfactory epithelium Histochem. Cell Biol. 113 2000 241 245
66. Henion T.R., Raitcheva D., Grosholz R., Biellmann F., Skarnes W.C., Hennet T., and Schwarting G.A. β1,3-N-Acetylglucosaminyltransferase 1 glycosylation is required for axon pathfinding by olfactory sensory neurons J. Neurosci. 25 2005 1894 1903
67. Hirao M., Sato N., Kondo T., Yonemura S., Monden M., Sasaki T., Takai Y., and Tsukita S. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: Possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway J. Cell Biol. 135 1996 37 51
68. Höfer D., Shin D.W., and Drenckhahn D. Identification of cytoskeletal markers for the different microvilli and cell types of the rat vomeronasal sensory epithelium J. Neurocytol. 29 2000 147 156
69. Hofmann M.H., and Meyer D.L. Peripheral origin of olfactory nerve fibers by-passing the olfactory bulb in Xenopus laevis Brain Res. 589 1992 161 163
70. Holbrook E.H., Szumowski K.E., and Schwob J.E. An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium J. Comp. Neurol. 363 1995 129 146
71. Hudson R., and Distel H. Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ Physiol. Behav. 37 1986 123 128
72. Hummel T. Assessment of intranasal trigeminal function Int. J. Psychophysiol. 36 2000 147 155
73. Hummel T., and Kobal G. Olfactory event-related potentials S.A. Simon M.A.L. Nicolelis "Methods and Frontiers in Chemosensory Research" 2001 CRC Press Boca Raton, FL 429 464
74. Humphrey T. The development of the olfactory and the accessory olfactory formations in human embryos and fetuses J. Comp. Neurol. 73 1940 431 468
75. Inamura K., Kashiwayanagi M., and Kurihara K. Inositol-1,4,5- trisphosphate induces responses in receptor neurons in rat vomeronasal sensory slices Chem. Senses 22 1997 93 103
76. Ishimitsu K. Über die Entwicklung des Vomeronasalorgans beim Menschen Yokohama Med. Bull. 9 1958 148 156
77. Jacob S., Zelano B., Gungor A., Abbott D., Naclerio R., and McClintock M.K. Location and gross morphology of the nasopalatine duct in human adults Arch. Otolaryngol. Head Neck Surg. 126 2000 741 748
78. Jacob S., McClintock M.K., Zelano B., and Ober C. Paternally inherited HLA alleles are associated with women's choice of male odor Nat. Genet. 30 2002 175 179
79. Jacobson L. Description anatomique d'un organe observé dans les mammifères (reported by M. Cuvier; translated into English by Bhatnagar and Reid, 1996) Ann. Mus. Nat. Hist. Nat. Paris 18 1811 412 424
80. Jacobson L. Anatomisk beskrivelse over et nyt organ i huusdyrenes naese Veter. Salesk Skrift 2 1813 209 246
81. Jafek B.W. Ultrastructure of human nasal mucosa Laryngoscope 93 1983 1576 1599
82. Jafek B.W., Murrow B., Michaels R., Restrepo D., and Linschoten M. Biopsies of human olfactory epithelium Chem. Senses 27 2002 623 628
83. Jahnke V., and Merker H.J. Electron microscopy studies of the human vomeronasal organ HNO 46 1998 502 506
84. Jia C., and Halpern M. Subclasses of vomeronasal receptor neurons: Differential expression of G proteins (Gi alpha 2 and G[o alpha]) and segregated projections to the accessory olfactory bulb Brain Res. 719 1996 117 128
85. Johnson A., Josephson R., and Hawke M. Clinical and histological evidence for the presence of the vomeronasal (Jacobson's) organ in adult humans J. Otolaryngol. 14 1985 71 79
86. Johnson E.W. CaBPs and other immunohistochemical markers of the human vomeronasal system: A comparison with other mammals Microsc. Res. Tech. 41 1998 530 541
87. Johnson E.W., Eller P.M., and Jafek B.W. Protein gene product 9.5-like and calbindin-like immunoreactivity in the nasal respiratory mucosa of perinatal humans Anat. Rec. 247 1997 38 45
88. Kalinoski D., Bruch R.C., and Brand J.G. Differential interaction of lectins with chemosensory receptors Brain Res. 418 1987 34 40
89. Kallius E. Geruchsorgan (organon olfactus) G. Fischer Jena "Bardeleben's Handbuch der Anatomie des Menschen" Vol. 5 1905 116 270
90. Karlson P., and Lüscher M. Pheromones: A new term for a class of biologically active substances Nature 183 1959 55 56
91. Kasper M., and Fehrenbach H. Immunohistochemical evidence for the occurrence of similar epithelial phenotypes during lung development and radiation-induced fibrogenesis Int. J. Radiat. Biol. 76 2000 493 501
92. Keverne E.B. The vomeronasal organ Science 286 1999 716 720
93. Keverne E.B. Pheromones, vomeronasal function, and gender-specific behavior Cell 108 2002 735 738
94. Keverne E.B., and de la Riva C. Pheromones in mice: Reciprocal interaction between the nose and brain Nature 296 1982 148 150
95. Key B., and Giorgi P.P. Selective binding of soybean agglutinin to the olfactory system of Xenopus Neuroscience 18 1986 507 515
96. Kim K.H., Patel L., Tobet S.A., King J.C., Rubin B.S., and Stopa E.G. Gonadotropin-releasing hormone immunoreactivity in the adult and fetal human olfactory system Brain Res. 826 1999 220 229
97. Kimoto H., and Touhara K. Induction of c-Fos expression in mouse vomeronasal neurons by sex-specific non-volatile pheromone(s) Chem. Senses 30 2005 i146 i147
98. Kinzinger J.H., Johnson E.W., Bhatnagar K.P., Bonar C.J., Burrows A.M., Mooney M.P., Siegel M.I., and Smith T.D. Comparative study of lectin reactivity in the vomeronasal organ of human and nonhuman primates Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 284 2005 550 560
99. Kjaer I., and Fischer Hansen B. The human vomeronasal organ: Prenatal developmental stages and distribution of luteinizing hormone-releasing hormone Eur. J. Oral Sci. 104 1996 34 40
100. Knecht M., Kuhnau D., Hüttenbrink K.B., Witt M., and Hummel T. Frequency and localization of the putative vomeronasal organ in humans in relation to age and gender Laryngoscope 111 2001 448 452
101. Knecht M., Lundstrom J.N., Witt M., Hüttenbrink K.B., Heilmann S., and Hummel T. Assessment of olfactory function and androstenone odor thresholds in humans with or without functional occlusion of the vomeronasal duct Behav. Neurosci. 117 2003 1135 1141
102. Knecht M., Witt M., Abolmaali N., Huttenbrink K.B., and Hummel T. Das vomeronasale Organ des Menschen Nervenarzt 74 2003 858 862
103. Knecht M., Kittner T., Beleites T., Huttenbrink K.B., Hummel T., and Witt M. Morphological and radiologic evaluation of the human nasopalatine duct Ann. Otol. Rhinol. Laryngol. 114 2005 229 232
104. Knöll B., Zarbalis K., Wurst W., and Drescher U. A role for the EphA family in the topographic targeting of vomeronasal axons Development 128 2001 895 906
105. Kobayakawa K., Hayashi R., Morita K., Miyamichi K., Oka Y., Tsuboi A., and Sakano H. Stomatin-related olfactory protein, SRO, specifically expressed in the murine olfactory sensory neurons J. Neurosci. 22 2002 5931 5937
106. Kölliker A. "Ueber die Jacobsonschen Organe des Menschen." 1877 Wilhelm Engelmann Leipzig
107. Kouros-Mehr H., Pintchovski S., Melnyk J., Chen Y.J., Friedman C., Trask B., and Shizuya H. Identification of non-functional human VNO receptor genes provides evidence for vestigiality of the human VNO Chem. Senses 26 2001 1167 1174
108. Kreda S.M., Gynn M.C., Fenstermacher D.A., Boucher R.C., and Gabriel S.E. Expression and localization of epithelial aquaporins in the adult human lung Am. J. Respir. Cell Mol. Biol. 24 2001 224 234
109. Kreutzer E.W., and Jafek B.W. The vomeronasal organ of Jacobson in the human embryo and fetus Otolaryngol. Head. Neck Surg. 88 1980 119 123
110. Kuhrt H., Hartig W., Grimm D., Faude F., Kasper M., and Reichenbach A. Changes in CD44 and ApoE immunoreactivities due to retinal pathology of man and rat J. Hirnforsch. 38 1997 223 229
111. Kwon B., Kim M., Kim W., Pyo J., Cheon Y., Cha C., Nam S., Baik T., and Lee B. Age-related changes in microvillar cells of rat olfactory epithelium Neurosci. Lett. 378 2005 65 69
112. Lallier T.E., Whittaker C.A., and DeSimone D.W. Integrin alpha 6 expression is required for early nervous system development in Xenopus laevis Development 122 1996 2539 2554
113. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., and Zufall F. Ultrasensitive pheromone detection by mammalian vomeronasal neurons Nature 405 2000 792 796
114. Liman E.R., Corey D.P., and Dulac C. TRP2: A candidate transduction channel for mammalian pheromone sensory signaling Proc. Natl. Acad. Sci. USA 96 1999 5791 5796
115. Lipscomb B.W., Treloar H.B., Klenoff J., and Greer C.A. Cell surface carbohydrates and glomerular targeting of olfactory sensory neuron axons in the mouse J. Comp. Neurol. 467 2003 22 31
116. Lotz M.M., Andrews C.W. Jr., Korzelius C.A., Lee E.C., Steele G.D. Jr., Clarke A., and Mercurio A.M. Decreased expression of Mac-2 (carbohydrate binding protein 35) and loss of its nuclear localization are associated with the neoplastic progression of colon carcinoma Proc. Natl. Acad. Sci. USA 90 1993 3466 3470
117. Luo M., and Katz L.C. Encoding pheromonal signals in the mammalian vomeronasal system Curr. Opin. Neurobiol. 14 2004 428 434
118. Luo M., Fee M.S., and Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice Science 299 2003 1196 1201
119. Mahanthappa N.K., Cooper D.N.W., Barondes S.H., and Schwarting G.A. Rat olfactory neurons can utilize the endogenous lectin, L-14, in a novel adhesion mechanism Development 120 1994 1373 1384
120. Mangakis M. Ein Fall von Jacobson'schen Organen beim Erwachsenen Anat. Anz. 21 1902 106 109
121. Martinez-Marcos A., Jia C., Quan W., and Halpern M. Neurogenesis, migration, and apoptosis in the vomeronasal epithelium of adult mice J. Neurobiol. 63 2005 173 187
122. Matsuoka M., Yoshida-Matsuoka J., Iwasaki N., Norita M., Costanzo R.M., and Ichikawa M. Immunocytochemical study of G(i)2alpha and G(o)alpha on the epithelium surface of the rat vomeronasal organ Chem. Senses 26 2001 161 166
123. Matsuzaki T., Suzuki T., Koyama H., Tanaka S., and Takata K. Water channel protein AQP3 is present in epithelia exposed to the environment of possible water loss J. Histochem. Cytochem. 47 1999 1275 1286
124. McClintock M.K. Menstrual synchrony and suppression Nature 229 1971 244 245
125. McClintock M.K. Human pheromones: Primers, releasers, signalers, or modulators? K. Wallen J.E. Schneider "Reproduction in Context: Social and Environmental Influences on Reproductive Physiology and Behavior" 2000 MIT Press Cambridge, MA 355 420
126. McCotter R.E. The connection of the vomero-nasal nerves with the accessory olfactory bulb in the opossum and other mammals Anat. Rec. 6 1912 299 318
127. McGarry R.C., Helfand S.L., Quarles R.H., and Roder J.C. Recognition of myelin-associated glycoprotein by the monoclonal antibody HNK-1 Nature 306 1983 376 378
128. Meisami E., and Bhatnagar K.P. Structure and diversity in mammalian accessory olfactory bulb Microsc. Res. Tech. 43 1998 476 499
129. Menco B.P., Carr V.M., Ezeh P.I., Liman E.R., and Yankova M.P. Ultrastructural localization of G-proteins and the channel protein TRP2 to microvilli of rat vomeronasal receptor cells J. Comp. Neurol. 438 2001 468 489
130. Meredith M. Human vomeronasal organ function: A critical review of best and worst cases Chem. Senses 26 2001 433 445
131. Merkel F. Jacobson'sches Organ und Papilla palatina beim Menschen (Festschrift zum fünfzigjährigen Doktorjubiläum des Herrn Geheimrat A. v. Kölliker) 1891 213 232
132. Mombaerts P. Seven-transmembrane proteins as odorant and chemosensory receptors Science 286 1999 707 711
133. Mombaerts P. Genes and ligands for odorant, vomeronasal and taste receptors Nat. Rev. Neurosci. 5 2004 263 278
134. Monti-Bloch L. Effect of vomeropherin pregna-4,20-diene-3,6-dione on isolated cells from the human vomeronasal organ Chem. Senses 22 1997 752
135. Monti-Block L., and Grosser B.I. Effect of putative pheromones on the electrical activity of the human vomeronasal organ and olfactory epithelium J. Steroid Biochem. Mol. Biol. 39 1991 573 582
136. Monti-Bloch L., Jennings-White C., and Berliner D.L. The human vomeronasal system. A review Ann. NY Acad. Sci. 855 1998 373 389
137. Moran D.T., Jafek B.W., and Rowley J.C.D. The vomeronasal (Jacobson's) organ in man: Ultrastructure and frequency of occurrence J. Steroid Biochem. Mol. Biol. 39 1991 545 552
138. Mori K., von Campenhause H., and Yoshihara Y. Zonal organization of the mammalian main and accessory olfactory systems Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 1801 1812
139. Morrison E.E., and Costanzo R.M. Morphology of the human olfactory epithelium J. Comp. Neurol. 297 1990 1 13
140. Morrison E.E., and Costanzo R.M. Morphology of olfactory epithelium in humans and other vertebrates Microsc. Res. Tech. 23 1992 49 61
141. Müller F., and O'Rahilly R. Olfactory structures in staged human embryos Cells Tissues Organs 178 2004 93 116
142. Mundy N.I., and Cook S. Positive selection during the diversification of class I vomeronasal receptor-like (V1RL) genes, putative pheromone receptor genes, in human and primate evolution Mol. Biol. Evol. 20 2003 1805 1810
143. Murrell W., Feron F., Wetzig A., Cameron N., Splatt K., Bellette B., Bianco J., Perry C., Lee G., and Mackay-Sim A. Multipotent stem cells from adult olfactory mucosa Dev. Dyn. 233 2005 496 515
144. Nakashima T., Kimmelman C.P., and Snow J.B. Vomeronasal organs and nerves of Jacobson in the human fetus Acta Otolaryngol. (Stockh.) 99 1985 266 271
145. Natsch A., Gfeller H., Gygax P., Schmid J., and Acuna G. A specific bacterial aminoacylase cleaves odorant precursors secreted in the human axilla J. Biol. Chem. 278 2003 5718 5727
146. Nielsen S., King L.S., Christensen B.M., and Agre P. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat Am. J. Physiol. Cell Physiol. 273 1997 C1549 C1561
147. Noden D.M. Vertebrate craniofacial development: The relation between ontogenetic process and morphological outcome Brain Behav. Evol. 38 1991 190 225
148. Northcutt R.G. A reassessment of Goodrich's model of cranial nerve phylogeny Acta Anat. (Basel) 148 1993 71 80
149. Ober C., Weitkamp L.R., Cox N., Dytch H., Kostyu D., and Elias S. HLA and mate choice in humans Am. J. Hum. Genet. 61 1997 497 504
150. Ortmann R. The sensory cells of the fetal vomeronasal organ in the human. A contribution to the variability of their differentiation and rudimentary development HNO 37 1989 191 197
151. Pace K.E., Lebestky T., Hummel T., Arnoux P., Kwan K., and Baum L.G. Characterization of a novel Drosophila melanogaster galectin. Expression in developing immune, neural, and muscle tissues J. Biol. Chem. 277 2002 13091 13098
152. Pearson A.D. The development of the nervus terminalis in man J. Comp. Neurol. 75 1941 39 66
153. Pfister P., and Rodriguez I. Olfactory expression of a single and highly variable V1r pheromone receptor-like gene in fish species Proc. Natl. Acad. Sci. USA 102 2005 5489 5494
154. Planel H. Etude anatomique et physiologique de l'organe Jacobson Arch. Anat. Histol. Embryol. 36 1953 199 205
155. Plendl J., and Schmahl W. Dolichos biflorus agglutinin: A marker of the developing olfactory system in the NMRI-mouse strain Anat. Embryol. (Berl.) 177 1988 459 464
156. Plendl J., and Sinowatz F. Glycobiology of the olfactory system Acta Anat. (Basel) 161 1998 234 253
157. Porter J.C., and Hogg N. Integrins take partners: Cross-talk between integrins and other membrane receptors Trends Cell Biol. 8 1998 390 396
158. Porter R.H., Cernoch J.M., and Balogh R.D. Odor signatures and kin recognition Physiol. Behav. 34 1985 445 448
159. Potiquet A. Du canal de Jacobson. De la possibilité de le reconnaitre sur le vivant et de son role probable dans la pathogénie de certaines lésions de la cloison nasale Rev. Laryngol. Otol. Rhinol. 24 1891 737 753
160. Powers J.B., and Winans S.S. Vomeronasal organ: Critical role in mediating sexual behavior of the male hamster Science 187 1975 961 963
161. Preti G., Wysocki C.J., Barnhart K.T., Sondheimer S.J., and Leyden J.J. Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients Biol. Reprod. 68 2003 2107 2113
162. Puche A.C., Poirier F., Hair M., Bartlett P.F., and Key B. Role of galectin-1 in the developing mouse olfactory system Dev. Biol. 179 1996 274 287
163. Radlanski R.J., Emmerich S., and Renz H. Prenatal morphogenesis of the human incisive canal Anat. Embryol. 208 2004 265 271
164. Rawson N.E. Human olfaction T.E. Finger W. Silver D. Restrepo "The Neurobiology of Taste and Smell" 2000 Wiley-Liss New York 257 284
165. Restrepo D., Arellano J., Oliva A., Schaefer M., and Lin W. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice Horm. Behav. 46 2004 247 256
166. Rodriguez I., and Mombaerts P. Novel human vomeronasal receptor-like genes reveal species-specific families Curr. Biol. 12 2002 R409 R411
167. Rodriguez I., Feinstein P., and Mombaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system Cell 97 1999 199 208
168. Rodriguez I., Greer C.A., Mok M.Y., and Mombaerts P. A putative pheromone receptor gene expressed in human olfactory mucosa Nat. Genet. 26 2000 18 19
169. Rosenthal F. Über das von Jacobson in der Nasenhöhle entdeckte Organ Z. Physiol. 1 1824 289 300
170. Ruysch F. "Thesaurus Anatomicus Tertius," 1703 Johann Wolters Amstelaedami 49
171. Salazar I., Sanchez Quinteiro P., Lombardero M., and Cifuentes J.M. Histochemical identification of carbohydrate moieties in the accessory olfactory bulb of the mouse using a panel of lectins Chem. Senses 26 2001 645 652
172. Sam M., Vora S., Malnic B., Ma W., Novotny M.V., and Buck L.B. Neuropharmacology. Odorants may arouse instinctive behaviours Nature 412 2001 142
173. Savic I., Berglund H., Gulyas B., and Roland P. Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans Neuron 31 2001 661 668
174. Scalia F., and Winans S.S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals J. Comp. Neurol. 161 1975 31 55
175. Schaeffer J.P. "The Nose, Parasinal Sinuses, Nasolacrimal Passageways, and Olfactory Organ in Man." 1920 P. Blakiston's Son and Co. Philadelphia, PA
176. Schandar M., Laugwitz K.L., Boekhoff I., Kroner C., Gudermann T., Schultz G., and Breer H. Odorants selectively activate distinct G protein subtypes in olfactory cilia J. Biol. Chem. 273 1998 16669 16677
177. Schreiber S., Fleischer J., Breer H., and Boekhoff I. A possible role for caveolin as a signaling organizer in olfactory sensory membranes J. Biol. Chem. 275 2000 24115 24123
178. Schrier R.W., Chen Y.C., and Cadnapaphornchai M.A. From finch to fish to man: Role of aquaporins in body fluid and brain water regulation Neuroscience 129 2004 897 904
179. Schwanzel-Fukuda M. Origin and migration of luteinizing hormone-releasing hormone neurons in mammals Microsc. Res. Tech. 44 1999 2 10
180. Schwanzel-Fukuda M., and Pfaff D.W. Nervus terminalis R. Doty "Handbook of Olfaction and Gustation" 2003 Marcel Dekker, Inc. New York 1001 1026
181. Schwanzel-Fukuda M., Garcia M.S., Morrell J.I., and Pfaff D.W. Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry J. Comp. Neurol. 255 1987 231 244
182. Schwanzel-Fukuda M., Abraham S., Crossin K.L., Edelman G.M., and Pfaff D.W. Immunocytochemical demonstration of neural cell adhesion molecule (NCAM) along the migration route of luteinizing hormone-releasing hormone (LHRH) neurons in mice J. Comp. Neurol. 321 1992 1 18
183. Schwanzel-Fukuda M., Crossin K.L., Pfaff D.W., Bouloux P.M., Hardelin J.P., and Petit C. Migration of luteinizing hormone-releasing hormone (LHRH) neurons in early human embryos J. Comp. Neurol. 366 1996 547 557
184. Schwarting G., Raitcheva D., Bless E., Ackerman S., and Tobet S. Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons Eur. J. Neurosci. 19 2004 11 20
185. Schwob J.E. Neural regeneration and the peripheral olfactory system Anat. Rec. 269 2002 33 49
186. Shapiro L.S., Ee P.L., and Halpern M. Lectin histochemical identification of carbohydrate moieties in opossum chemosensory systems during development, with special emphasis on VVA-identified subdivisions in the accessory olfactory bulb J. Morphol. 224 1995 331 349
187. Sherman L., Sleeman J., Herrlich P., and Ponta H. Hyaluronate receptors: Key players in growth, differentiation, migration and tumor progression Curr. Opin. Cell Biol. 6 1994 726 733
188. Shimp K., Bhatnagar K., Bonar C., and Smith T. Ontogeny of the nasopalatine duct in primates Anat. Rec. 274A 2003 862 869
189. Smith T.D., Siegel M.I., Mooney M.P., Burdi A.R., Burrows A.M., and Todhunter J.S. Prenatal growth of the human vomeronasal organ Anat. Rec. 248 1997 447 455
190. Smith T.D., Buttery T.A., Bhatnagar K.P., Burrows A.M., Mooney M.P., and Siegel M.I. Anatomical position of the vomeronasal organ in postnatal humans Ann. Anat. 183 2001 475 479
191. Smith T.D., Bhatnagar K.P., Shimp K.L., Kinzinger J.H., Bonar C.J., Burrows A.M., Mooney M.P., and Siegel M.I. Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates Anat. Rec. 267 2002 166 176
192. Sömmering S.T. "Abbildungen der menschlichen Organe des Geruches." 1809 Varrentrapp und Wenner Frankfurt
193. Sorokin S.P., Hoyt R.F., and Shaffer M.J. Ontogeny of neuroepithelial bodies: Correlations with mitogenesis and innervation Microsc. Res. Tech. 37 1997 43 61
194. Spehr M., and Leinders-Zufall T. One neuron-multiple receptors: Increased complexity in olfactory coding? Sci. STKE 285 2005 25
195. Spielman A.I., Zeng X.N., Leyden J.J., and Preti G. Proteinaceous precursors of human axillary odor: Isolation of two novel odor-binding proteins Experientia 51 1995 40 47
196. Stensaas L.J., Lavker R.M., Monti-Bloch L., Grosser B.I., and Berliner D.L. Ultrastructure of the human vomeronasal organ J. Steroid Biochem. Mol. Biol. 39 1991 553 560
197. Stern K., and McClintock M.K. Regulation of ovulation by human pheromones Nature 392 1998 177 179
198. Storan M., Magnaldo T., Biol-N'Garagba M., Zick Y., and Key B. Expression and putative role of lactoseries carbohydrates present on NCAM in the rat primary olfactory pathway J. Comp. Neurol. 475 2004 289 302
199. Surridge A.K., Osorio D., and Mundy N.I. Evolution and selection of trichromatic vision in primates Trends Ecol. Evol. 18 2003 198 205
200. Takami S. Recent progress in the neurobiology of the vomeronasal organ Microsc. Res. Tech. 58 2002 228 250
201. Takami S., Getchell M.L., Chen Y., Monti-Bloch L., Berliner D.L., Stensaas L.J., and Getchell T.V. Vomeronasal epithelial cells of the adult human express neuron-specific molecules Neuroreport 4 1993 375 378
202. Takami S., Yukimatsu M., Matsumura G., and Nishiyama F. Vomeronasal epithelial cells of human fetuses contain immunoreactivity for G proteins, Go (alpha) and Gi (alpha 2) Chem. Senses 26 2001 517 522
203. Trinh K., and Storm D.R. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium Nat. Neurosci. 31 2003 31
204. Trotier D., Eloit C., Wassef M., Talmain G., Bensimon J.L., Doving K.B., and Ferrand J. The vomeronasal cavity in adult humans Chem. Senses 25 2000 369 380
205. Tsukita S., Oishi K., Sato N., Sagara J., and Kawai A. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons J. Cell Biol. 126 1994 391 401
206. Verney C., el Amraoui A., and Zecevic N. Comigration of tyrosine hydroxylase- and gonadotropin-releasing hormone-immunoreactive neurons in the nasal area of human embryos Brain Res. Dev. Brain Res. 97 1996 251 259
207. von Bartheld C.S. The terminal nerve and its relation with extrabulbar "olfactory" projections: Lessons from lampreys and lungfishes Microsc. Res. Tech. 65 2004 13 24
208. von Lanz T., and Wachsmuth W. J. Lang W. Wachsmuth "Praktische Anatomie" 1985 Springer-Verlag Berlin 173 Erster Band, Teil 1A
209. von Mihalkovics V. Nasenhöhle und Jacobsonsches Organ. Eine morphologische Studie Anat. Hefte 11 1899 1 107
210. Wakabayashi Y., Mori Y., Ichikawa M., Yazaki K., and Hagino-Yamagishi K. A putative pheromone receptor gene is expressed in two distinct olfactory organs in goats Chem. Senses 27 2002 207 213
211. Walz A., Rodriguez I., and Mombaerts P. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice J. Neurosci. 22 2002 4025 4035
212. Ward J.M. Leu 7 immunoreactivity in fetal olfactory epithelium and dysplastic or neoplastic olfactory lesions induced in Syrian golden hamsters by N-nitrosodiethylamine Am. J. Pathol. 123 1986 371 376
213. Wedekind C., Seebeck T., Bettens F., and Paepke A.J. MHC-dependent mate preferences in humans Proc. Biol. Sci. 260 1995 245 249
214. Weiler E. Postnatal development of the rat vomeronasal organ Chem. Senses 30 2005 i127 i128
215. Weiler E., McCulloch M.A., and Farbman A.I. Proliferation in the vomeronasal organ of the rat during postnatal development Eur. J. Neurosci. 11 1999 700 711
216. Whitlock K.E. Development of the nervus terminalis: Origin and migration Microsc. Res. Tech. 65 2004 2 12
217. Winstead W., Marshall C.T., Lu C.L., Klueber K.M., and Roisen F.J. Endoscopic biopsy of human olfactory epithelium as a source of progenitor cells Am. J. Rhinol. 19 2005 83 90
218. Witt M., and Kasper M. Immunohistochemical distribution of CD44 and some of its isoforms during human taste bud development Histochem. Cell Biol. 110 1998 95 103
219. Witt M., and Reutter K. Lectin histochemistry on mucous substances of the taste buds and adjacent epithelia of different vertebrates Histochemistry 88 1988 453 461
220. Witt M., Reutter K., Ganchrow D., and Ganchrow J.R. Fingerprinting taste buds: Intermediate filaments and their implication for taste bud formation Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 1233 1237
221. Witt M., Georgiewa B., Knecht M., and Hummel T. On the chemosensory nature of the vomeronasal epithelium in adult humans Histochem. Cell Biol. 117 2002 493 509
222. Witt M., Reutter K., and Miller I.J. Jr. Morphology of the peripheral taste system R.L. Doty "Handbook of Olfaction and Gustation" 2003 Marcel Dekker, Inc. New York 651 677
223. Won J., Mair E.A., Bolger W.E., and Conran R.M. The vomeronasal organ: An objective anatomic analysis of its prevalence Ear Nose Throat J. 79 2000 600 605
224. Woodley S.K., Cloe A.L., Waters P., and Baum M.J. Effects of vomeronasal organ removal on olfactory sex discrimination and odor preferences of female ferrets Chem. Senses 29 2004 659 669
225. Wray S. Molecular mechanisms for migration of placodally derived GnRH neurons Chem. Senses 27 2002 569 572
226. Wray S., Grant P., and Gainer H. Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode Proc. Natl. Acad. Sci. USA 86 1989 8132 8136
227. Wray S., Fueshko S.M., Kusano K., and Gainer H. GABAergic neurons in the embryonic olfactory pit/vomeronasal organ: Maintenance of functional GABAergic synapses in olfactory explants Dev. Biol. 180 1996 631 645
228. Wysocki C.J., and Preti G. Facts, fallacies, fears, and frustrations with human pheromones Anat. Rec. 281A 2004 1201 1211
229. Wysocki C., Yamazaki K., Curran M., Wysocki L., and Beauchamp G. Mice (Mus musculus) lacking a vomeronasal organ can discriminate MHC-determined odortypes Horm. Behav. 46 2004 241 246
230. Yang R.Y., Hsu D.K., and Liu F.T. Expression of galectin-3 modulates T-cell growth and apoptosis Proc. Natl. Acad. Sci. USA 93 1996 6737 6742
231. Yoshida J., Osada T., Mori Y., and Ichikawa M. Differential binding patterns of three antibodies (VOBM1, VOBM2, and VOM2) in the rat vomeronasal organ and accessory olfactory bulb Cell Tissue Res. 281 1995 243 248
232. Yoshida K., Rutishauser U., Crandall J.E., and Schwarting G.A. Polysialic acid facilitates migration of luteinizing hormone-releasing hormone neurons on vomeronasal axons J. Neurosci. 19 1999 794 801
233. Yoshida-Matsuoka J., Osada T., Mori Y., and Ichikawa M. A developmental study using three antibodies (VOBM1, VOBM2, and VOM2): Immunocytochemical and electron microscopical analysis of the luminal surface of the rat vomeronasal sensory epithelium Anat. Embryol. (Berl.) 199 1999 215 224
234. Yoshihara Y., Kawasaki M., Tamada A., Fujita H., Hayashi H., Kagamiyama H., and Mori K. OCAM: A new member of the neural cell adhesion molecule family related to zone-to-zone projection of olfactory and vomeronasal axons J. Neurosci. 17 1997 5830 5842
235. Young J.M., Kambere M., Trask B.J., and Lane R.P. Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs Genome Res. 15 2005 231 240
236. Zbar R.I., Zbar L.I., Dudley C., Trott S.A., Rohrich R.J., and Moss R.L. A classification schema for the vomeronasal organ in humans Plast. Reconstr. Surg. 105 2000 1284 1288
237. Zehntner S.P., Mackay-Sim A., and Bushell G.R. Differentiation in an olfactory cell line. Analysis via differential display Ann. NY Acad. Sci. 855 1998 235 239
238. Zeng C., Spielman A.I., Vowels B.R., Leyden J.J., Biemann K., and Preti G. A human axillary odorant is carried by apolipoprotein D Proc. Natl. Acad. Sci. USA 93 1996 6626 6630
239. Zhang J., and Webb D.M. Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates Proc. Natl. Acad. Sci. USA 100 2003 8337 8341
240. Zhang J.-X., Ni J., Ren X.-J., Sun L., Zhang Z.-B., and Wang Z.-W. Possible coding for recognition of sexes, individuals and species in anal gland volatiles of Mustela eversmanni and M. sibirica Chem. Senses 28 2003 381 388
241. Zhang X., Rodriguez I., Mombaerts P., and Firestein S. Odorant and vomeronasal receptor genes in two mouse genome assemblies Genomics 83 2004 802 811
242. Zuckerkandl E. "Normale und pathologische Anatomie der Nasenhöhle und ihrer pneumatischen Anhänge." 1893 Braumüller Wien
243. Zufall F. The TRPC2 ion channel and pheromone sensing in the accessory olfactory system Naunyn Schmiedebergs Arch Pharmacol. 371 2005 245 250
244. Zufall F., Kelliher K.R., and Leinders-Zufall T.P. Pheromone detection by mammalian vomeronasal neurons Microsc. Res. Tech. 58 2002 251 260