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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Dec 29;355(1404):1801–1812. doi: 10.1098/rstb.2000.0736

Zonal organization of the mammalian main and accessory olfactory systems.

K Mori 1, H von Campenhause 1, Y Yoshihara 1
PMCID: PMC1692907  PMID: 11205342

Abstract

Zonal organization is one of the characteristic features observed in both main and accessory olfactory systems. In the main olfactory system, most of the odorant receptors are classified into four groups according to their zonal expression patterns in the olfactory epithelium. Each group of odorant receptors is expressed by sensory neurons distributed within one of four circumscribed zones. Olfactory sensory neurons in a given zone of the epithelium project their axons to the glomeruli in a corresponding zone of the main olfactory bulb. Glomeruli in the same zone tend to represent similar odorant receptors having similar tuning specificity to odorants. Vomeronasal receptors (or pheromone receptors) are classified into two groups in the accessory olfactory system. Each group of receptors is expressed by vomeronasal sensory neurons in either the apical or basal zone of the vomeronasal epithelium. Sensory neurons in the apical zone project their axons to the rostral zone of the accessory olfactory bulb and form synaptic connections with mitral tufted cells belonging to the rostral zone. Signals originated from basal zone sensory neurons are sent to mitral tufted cells in the caudal zone of the accessory olfactory bulb. We discuss functional implications of the zonal organization in both main and accessory olfactory systems.

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Selected References

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  1. BRUCE H. M. An exteroceptive block to pregnancy in the mouse. Nature. 1959 Jul 11;184:105–105. doi: 10.1038/184105a0. [DOI] [PubMed] [Google Scholar]
  2. Bacchini A., Gaetani E., Cavaggioni A. Pheromone binding proteins of the mouse, Mus musculus. Experientia. 1992 Apr 15;48(4):419–421. doi: 10.1007/BF01923448. [DOI] [PubMed] [Google Scholar]
  3. Belluscio L., Koentges G., Axel R., Dulac C. A map of pheromone receptor activation in the mammalian brain. Cell. 1999 Apr 16;97(2):209–220. doi: 10.1016/s0092-8674(00)80731-x. [DOI] [PubMed] [Google Scholar]
  4. Ben-Arie N., Lancet D., Taylor C., Khen M., Walker N., Ledbetter D. H., Carrozzo R., Patel K., Sheer D., Lehrach H. Olfactory receptor gene cluster on human chromosome 17: possible duplication of an ancestral receptor repertoire. Hum Mol Genet. 1994 Feb;3(2):229–235. doi: 10.1093/hmg/3.2.229. [DOI] [PubMed] [Google Scholar]
  5. Bonhoeffer T., Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature. 1991 Oct 3;353(6343):429–431. doi: 10.1038/353429a0. [DOI] [PubMed] [Google Scholar]
  6. Brennan P. A., Schellinck H. M., Keverne E. B. Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience. 1999;90(4):1463–1470. doi: 10.1016/s0306-4522(98)00556-9. [DOI] [PubMed] [Google Scholar]
  7. Brennan P., Kaba H., Keverne E. B. Olfactory recognition: a simple memory system. Science. 1990 Nov 30;250(4985):1223–1226. doi: 10.1126/science.2147078. [DOI] [PubMed] [Google Scholar]
  8. Brugge J. F., Merzenich M. M. Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol. 1973 Nov;36(6):1138–1158. doi: 10.1152/jn.1973.36.6.1138. [DOI] [PubMed] [Google Scholar]
  9. Buck L. B. Information coding in the vertebrate olfactory system. Annu Rev Neurosci. 1996;19:517–544. doi: 10.1146/annurev.ne.19.030196.002505. [DOI] [PubMed] [Google Scholar]
  10. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 1991 Apr 5;65(1):175–187. doi: 10.1016/0092-8674(91)90418-x. [DOI] [PubMed] [Google Scholar]
  11. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 1994 Sep 9;78(5):823–834. doi: 10.1016/s0092-8674(94)90562-2. [DOI] [PubMed] [Google Scholar]
  12. Clyne P. J., Warr C. G., Freeman M. R., Lessing D., Kim J., Carlson J. R. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron. 1999 Feb;22(2):327–338. doi: 10.1016/s0896-6273(00)81093-4. [DOI] [PubMed] [Google Scholar]
  13. Del Cerro M. C., Izquierdo M. A., Collado P., Segovia S., Guillamón A. Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats. Physiol Behav. 1991 Jul;50(1):67–71. doi: 10.1016/0031-9384(91)90499-e. [DOI] [PubMed] [Google Scholar]
  14. Dryer L., Graziadei P. P. Mitral cell dendrites: a comparative approach. Anat Embryol (Berl) 1994 Feb;189(2):91–106. doi: 10.1007/BF00185769. [DOI] [PubMed] [Google Scholar]
  15. Dulac C., Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 1995 Oct 20;83(2):195–206. doi: 10.1016/0092-8674(95)90161-2. [DOI] [PubMed] [Google Scholar]
  16. Emery D. E., Sachs B. D. Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis. Physiol Behav. 1976 Nov;17(5):803–806. doi: 10.1016/0031-9384(76)90044-5. [DOI] [PubMed] [Google Scholar]
  17. Ezeh P. I., Davis L. M., Scott J. W. Regional distribution of rat electroolfactogram. J Neurophysiol. 1995 Jun;73(6):2207–2220. doi: 10.1152/jn.1995.73.6.2207. [DOI] [PubMed] [Google Scholar]
  18. Fujita S. C., Mori K., Imamura K., Obata K. Subclasses of olfactory receptor cells and their segregated central projections demonstrated by a monoclonal antibody. Brain Res. 1985 Feb 4;326(1):192–196. doi: 10.1016/0006-8993(85)91403-9. [DOI] [PubMed] [Google Scholar]
  19. Gao Q., Chess A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics. 1999 Aug 15;60(1):31–39. doi: 10.1006/geno.1999.5894. [DOI] [PubMed] [Google Scholar]
  20. Griff I. C., Reed R. R. The genetic basis for specific anosmia to isovaleric acid in the mouse. Cell. 1995 Nov 3;83(3):407–414. doi: 10.1016/0092-8674(95)90118-3. [DOI] [PubMed] [Google Scholar]
  21. HUBEL D. H., WIESEL T. N. Receptive fields of single neurones in the cat's striate cortex. J Physiol. 1959 Oct;148:574–591. doi: 10.1113/jphysiol.1959.sp006308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Halpern M., Jia C., Shapiro L. S. Segregated pathways in the vomeronasal system. Microsc Res Tech. 1998 Jun 15;41(6):519–529. doi: 10.1002/(SICI)1097-0029(19980615)41:6<519::AID-JEMT7>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
  23. Herrada G., Dulac C. A novel family of putative pheromone receptors in mammals with a topographically organized and sexually dimorphic distribution. Cell. 1997 Aug 22;90(4):763–773. doi: 10.1016/s0092-8674(00)80536-x. [DOI] [PubMed] [Google Scholar]
  24. Hildebrand J. G., Shepherd G. M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci. 1997;20:595–631. doi: 10.1146/annurev.neuro.20.1.595. [DOI] [PubMed] [Google Scholar]
  25. Hubel D. H., Wiesel T. N. Early exploration of the visual cortex. Neuron. 1998 Mar;20(3):401–412. doi: 10.1016/s0896-6273(00)80984-8. [DOI] [PubMed] [Google Scholar]
  26. Hubel D. H., Wiesel T. N. Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol. 1972 Dec;146(4):421–450. doi: 10.1002/cne.901460402. [DOI] [PubMed] [Google Scholar]
  27. Hubel D. H., Wiesel T. N., Stryker M. P. Anatomical demonstration of orientation columns in macaque monkey. J Comp Neurol. 1978 Feb 1;177(3):361–380. doi: 10.1002/cne.901770302. [DOI] [PubMed] [Google Scholar]
  28. Imamura K., Mataga N., Mori K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. J Neurophysiol. 1992 Dec;68(6):1986–2002. doi: 10.1152/jn.1992.68.6.1986. [DOI] [PubMed] [Google Scholar]
  29. Imamura K., Mori K., Fujita S. C., Obata K. Immunochemical identification of subgroups of vomeronasal nerve fibers and their segregated terminations in the accessory olfactory bulb. Brain Res. 1985 Mar 4;328(2):362–366. doi: 10.1016/0006-8993(85)91050-9. [DOI] [PubMed] [Google Scholar]
  30. Jemiolo B., Harvey S., Novotny M. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4576–4579. doi: 10.1073/pnas.83.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jia C., Halpern M. Segregated populations of mitral/tufted cells in the accessory olfactory bulb. Neuroreport. 1997 May 27;8(8):1887–1890. doi: 10.1097/00001756-199705260-00019. [DOI] [PubMed] [Google Scholar]
  32. Jia C., 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. 1996 May 6;719(1-2):117–128. doi: 10.1016/0006-8993(96)00110-2. [DOI] [PubMed] [Google Scholar]
  33. Kashiwadani H., Sasaki Y. F., Uchida N., Mori K. Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J Neurophysiol. 1999 Oct;82(4):1786–1792. doi: 10.1152/jn.1999.82.4.1786. [DOI] [PubMed] [Google Scholar]
  34. Katoh K., Koshimoto H., Tani A., Mori K. Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. J Neurophysiol. 1993 Nov;70(5):2161–2175. doi: 10.1152/jn.1993.70.5.2161. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Krautwurst D., Yau K. W., Reed R. R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 1998 Dec 23;95(7):917–926. doi: 10.1016/s0092-8674(00)81716-x. [DOI] [PubMed] [Google Scholar]
  37. Krieger J., Schmitt A., Löbel D., Gudermann T., Schultz G., Breer H., Boekhoff I. Selective activation of G protein subtypes in the vomeronasal organ upon stimulation with urine-derived compounds. J Biol Chem. 1999 Feb 19;274(8):4655–4662. doi: 10.1074/jbc.274.8.4655. [DOI] [PubMed] [Google Scholar]
  38. Kurahashi T., Yau K. W. Co-existence of cationic and chloride components in odorant-induced current of vertebrate olfactory receptor cells. Nature. 1993 May 6;363(6424):71–74. doi: 10.1038/363071a0. [DOI] [PubMed] [Google Scholar]
  39. Lehman M. N., Winans S. S., Powers J. B. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science. 1980 Oct 31;210(4469):557–560. doi: 10.1126/science.7423209. [DOI] [PubMed] [Google Scholar]
  40. Luskin M. B., Price J. L. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol. 1983 May 20;216(3):264–291. doi: 10.1002/cne.902160305. [DOI] [PubMed] [Google Scholar]
  41. MOUNTCASTLE V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol. 1957 Jul;20(4):408–434. doi: 10.1152/jn.1957.20.4.408. [DOI] [PubMed] [Google Scholar]
  42. Malnic B., Hirono J., Sato T., Buck L. B. Combinatorial receptor codes for odors. Cell. 1999 Mar 5;96(5):713–723. doi: 10.1016/s0092-8674(00)80581-4. [DOI] [PubMed] [Google Scholar]
  43. Marchlewska-Koj A. Pregnancy block elicited by male urinary peptides in mice. J Reprod Fertil. 1981 Jan;61(1):221–224. doi: 10.1530/jrf.0.0610221. [DOI] [PubMed] [Google Scholar]
  44. Matsunami H., Buck L. B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell. 1997 Aug 22;90(4):775–784. doi: 10.1016/s0092-8674(00)80537-1. [DOI] [PubMed] [Google Scholar]
  45. Miyawaki A., Homma H., Tamura H., Matsui M., Mikoshiba K. Zonal distribution of sulfotransferase for phenol in olfactory sustentacular cells. EMBO J. 1996 May 1;15(9):2050–2055. [PMC free article] [PubMed] [Google Scholar]
  46. Mombaerts P., Wang F., Dulac C., Chao S. K., Nemes A., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell. 1996 Nov 15;87(4):675–686. doi: 10.1016/s0092-8674(00)81387-2. [DOI] [PubMed] [Google Scholar]
  47. Mori K., Fujita S. C., Imamura K., Obata K. Immunohistochemical study of subclasses of olfactory nerve fibers and their projections to the olfactory bulb in the rabbit. J Comp Neurol. 1985 Dec 8;242(2):214–229. doi: 10.1002/cne.902420205. [DOI] [PubMed] [Google Scholar]
  48. Mori K., Imamura K., Fujita S. C., Obata K. Projections of two subclasses of vomeronasal nerve fibers to the accessory olfactory bulb in the rabbit. Neuroscience. 1987 Jan;20(1):259–278. doi: 10.1016/0306-4522(87)90018-2. [DOI] [PubMed] [Google Scholar]
  49. Mori K., Mataga N., Imamura K. Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. J Neurophysiol. 1992 Mar;67(3):786–789. doi: 10.1152/jn.1992.67.3.786. [DOI] [PubMed] [Google Scholar]
  50. Mori K. Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog Neurobiol. 1987;29(3):275–320. doi: 10.1016/0301-0082(87)90024-4. [DOI] [PubMed] [Google Scholar]
  51. Mori K., Nagao H., Yoshihara Y. The olfactory bulb: coding and processing of odor molecule information. Science. 1999 Oct 22;286(5440):711–715. doi: 10.1126/science.286.5440.711. [DOI] [PubMed] [Google Scholar]
  52. Mori K., Yoshihara Y. Molecular recognition and olfactory processing in the mammalian olfactory system. Prog Neurobiol. 1995 Apr;45(6):585–619. doi: 10.1016/0301-0082(94)00058-p. [DOI] [PubMed] [Google Scholar]
  53. Mucignat-Caretta C., Caretta A., Cavaggioni A. Acceleration of puberty onset in female mice by male urinary proteins. J Physiol. 1995 Jul 15;486(Pt 2):517–522. doi: 10.1113/jphysiol.1995.sp020830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Nagao H., Yoshihara Y., Mitsui S., Fujisawa H., Mori K. Two mirror-image sensory maps with domain organization in the mouse main olfactory bulb. Neuroreport. 2000 Sep 11;11(13):3023–3027. doi: 10.1097/00001756-200009110-00039. [DOI] [PubMed] [Google Scholar]
  55. Novotny M., Harvey S., Jemiolo B., Alberts J. Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2059–2061. doi: 10.1073/pnas.82.7.2059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Price J. L. An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol. 1973 Jul 1;150(1):87–108. doi: 10.1002/cne.901500105. [DOI] [PubMed] [Google Scholar]
  57. Qasba P., Reed R. R. Tissue and zonal-specific expression of an olfactory receptor transgene. J Neurosci. 1998 Jan 1;18(1):227–236. doi: 10.1523/JNEUROSCI.18-01-00227.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Reed R. R. Signaling pathways in odorant detection. Neuron. 1992 Feb;8(2):205–209. doi: 10.1016/0896-6273(92)90287-n. [DOI] [PubMed] [Google Scholar]
  59. Ressler K. J., Sullivan S. L., Buck L. B. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell. 1993 May 7;73(3):597–609. doi: 10.1016/0092-8674(93)90145-g. [DOI] [PubMed] [Google Scholar]
  60. Ressler K. J., Sullivan S. L., Buck L. B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 1994 Dec 30;79(7):1245–1255. doi: 10.1016/0092-8674(94)90015-9. [DOI] [PubMed] [Google Scholar]
  61. Rodriguez I., Feinstein P., Mombaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell. 1999 Apr 16;97(2):199–208. doi: 10.1016/s0092-8674(00)80730-8. [DOI] [PubMed] [Google Scholar]
  62. Royet J. P., Souchier C., Jourdan F., Ploye H. Morphometric study of the glomerular population in the mouse olfactory bulb: numerical density and size distribution along the rostrocaudal axis. J Comp Neurol. 1988 Apr 22;270(4):559–568. doi: 10.1002/cne.902700409. [DOI] [PubMed] [Google Scholar]
  63. Rubin B. D., Katz L. C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron. 1999 Jul;23(3):499–511. doi: 10.1016/s0896-6273(00)80803-x. [DOI] [PubMed] [Google Scholar]
  64. Ryba N. J., Tirindelli R. A new multigene family of putative pheromone receptors. Neuron. 1997 Aug;19(2):371–379. doi: 10.1016/s0896-6273(00)80946-0. [DOI] [PubMed] [Google Scholar]
  65. Saito H., Mimmack M. L., Keverne E. B., Kishimoto J., Emson P. C. Isolation of mouse vomeronasal receptor genes and their co-localization with specific G-protein messenger RNAs. Brain Res Mol Brain Res. 1998 Oct 1;60(2):215–227. doi: 10.1016/s0169-328x(98)00183-1. [DOI] [PubMed] [Google Scholar]
  66. Sato T., Hirono J., Tonoike M., Takebayashi M. Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. J Neurophysiol. 1994 Dec;72(6):2980–2989. doi: 10.1152/jn.1994.72.6.2980. [DOI] [PubMed] [Google Scholar]
  67. Saucier D., Astic L. Analysis of the topographical organization of olfactory epithelium projections in the rat. Brain Res Bull. 1986 Apr;16(4):455–462. doi: 10.1016/0361-9230(86)90173-5. [DOI] [PubMed] [Google Scholar]
  68. Scalia F., Winans S. S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol. 1975 May 1;161(1):31–55. doi: 10.1002/cne.901610105. [DOI] [PubMed] [Google Scholar]
  69. Schoenfeld T. A., Clancy A. N., Forbes W. B., Macrides F. The spatial organization of the peripheral olfactory system of the hamster. Part I: Receptor neuron projections to the main olfactory bulb. Brain Res Bull. 1994;34(3):183–210. doi: 10.1016/0361-9230(94)90059-0. [DOI] [PubMed] [Google Scholar]
  70. Schwarting G. A., Crandall J. E. Subsets of olfactory and vomeronasal sensory epithelial cells and axons revealed by monoclonal antibodies to carbohydrate antigens. Brain Res. 1991 May 3;547(2):239–248. doi: 10.1016/0006-8993(91)90967-z. [DOI] [PubMed] [Google Scholar]
  71. Schwob J. E., Gottlieb D. I. Purification and characterization of an antigen that is spatially segregated in the primary olfactory projection. J Neurosci. 1988 Sep;8(9):3470–3480. doi: 10.1523/JNEUROSCI.08-09-03470.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Schwob J. E., Gottlieb D. I. The primary olfactory projection has two chemically distinct zones. J Neurosci. 1986 Nov;6(11):3393–3404. doi: 10.1523/JNEUROSCI.06-11-03393.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Sorensen P. W. Biological responsiveness to pheromones provides fundamental and unique insight into olfactory function. Chem Senses. 1996 Apr;21(2):245–256. doi: 10.1093/chemse/21.2.245. [DOI] [PubMed] [Google Scholar]
  74. Strotmann J., Wanner I., Helfrich T., Beck A., Breer H. Rostro-caudal patterning of receptor-expressing olfactory neurones in the rat nasal cavity. Cell Tissue Res. 1994 Oct;278(1):11–20. doi: 10.1007/BF00305773. [DOI] [PubMed] [Google Scholar]
  75. Strotmann J., Wanner I., Krieger J., Raming K., Breer H. Expression of odorant receptors in spatially restricted subsets of chemosensory neurones. Neuroreport. 1992 Dec;3(12):1053–1056. doi: 10.1097/00001756-199212000-00005. [DOI] [PubMed] [Google Scholar]
  76. Sugai T., Sugitani M., Onoda N. Subdivisions of the guinea-pig accessory olfactory bulb revealed by the combined method with immunohistochemistry, electrophysiological, and optical recordings. Neuroscience. 1997 Aug;79(3):871–885. doi: 10.1016/s0306-4522(96)00690-2. [DOI] [PubMed] [Google Scholar]
  77. Sullivan S. L., Adamson M. C., Ressler K. J., Kozak C. A., Buck L. B. The chromosomal distribution of mouse odorant receptor genes. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):884–888. doi: 10.1073/pnas.93.2.884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Sullivan S. L., Ressler K. J., Buck L. B. Spatial patterning and information coding in the olfactory system. Curr Opin Genet Dev. 1995 Aug;5(4):516–523. doi: 10.1016/0959-437x(95)90057-n. [DOI] [PubMed] [Google Scholar]
  79. Takami S., Graziadei P. P. Morphological complexity of the glomerulus in the rat accessory olfactory bulb--a Golgi study. Brain Res. 1990 Mar 5;510(2):339–342. doi: 10.1016/0006-8993(90)91387-v. [DOI] [PubMed] [Google Scholar]
  80. Touhara K., Sengoku S., Inaki K., Tsuboi A., Hirono J., Sato T., Sakano H., Haga T. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4040–4045. doi: 10.1073/pnas.96.7.4040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Tsuboi A., Yoshihara S., Yamazaki N., Kasai H., Asai-Tsuboi H., Komatsu M., Serizawa S., Ishii T., Matsuda Y., Nagawa F. Olfactory neurons expressing closely linked and homologous odorant receptor genes tend to project their axons to neighboring glomeruli on the olfactory bulb. J Neurosci. 1999 Oct 1;19(19):8409–8418. doi: 10.1523/JNEUROSCI.19-19-08409.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Vassar R., Chao S. K., Sitcheran R., Nuñez J. M., Vosshall L. B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell. 1994 Dec 16;79(6):981–991. doi: 10.1016/0092-8674(94)90029-9. [DOI] [PubMed] [Google Scholar]
  83. Vassar R., Ngai J., Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 1993 Jul 30;74(2):309–318. doi: 10.1016/0092-8674(93)90422-m. [DOI] [PubMed] [Google Scholar]
  84. Vosshall L. B., Amrein H., Morozov P. S., Rzhetsky A., Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 1999 Mar 5;96(5):725–736. doi: 10.1016/s0092-8674(00)80582-6. [DOI] [PubMed] [Google Scholar]
  85. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 1998 Apr 3;93(1):47–60. doi: 10.1016/s0092-8674(00)81145-9. [DOI] [PubMed] [Google Scholar]
  86. Weth F., Nadler W., Korsching S. Nested expression domains for odorant receptors in zebrafish olfactory epithelium. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13321–13326. doi: 10.1073/pnas.93.23.13321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Woolsey T. A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970 Jan 20;17(2):205–242. doi: 10.1016/0006-8993(70)90079-x. [DOI] [PubMed] [Google Scholar]
  88. Yokoi M., Mori K., Nakanishi S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3371–3375. doi: 10.1073/pnas.92.8.3371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Yoshihara Y., Katoh K., Mori K. Odor stimulation causes disappearance of R4B12 epitope on axonal surface molecule of olfactory sensory neurons. Neuroscience. 1993 Mar;53(1):101–110. doi: 10.1016/0306-4522(93)90288-q. [DOI] [PubMed] [Google Scholar]
  90. Yoshihara Y., Kawasaki M., Tamada A., Fujita H., Hayashi H., Kagamiyama H., 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. 1997 Aug 1;17(15):5830–5842. doi: 10.1523/JNEUROSCI.17-15-05830.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Yoshihara Y., Mori K. Basic principles and molecular mechanisms of olfactory axon pathfinding. Cell Tissue Res. 1997 Nov;290(2):457–463. doi: 10.1007/s004410050953. [DOI] [PubMed] [Google Scholar]
  92. Zhao H., Ivic L., Otaki J. M., Hashimoto M., Mikoshiba K., Firestein S. Functional expression of a mammalian odorant receptor. Science. 1998 Jan 9;279(5348):237–242. doi: 10.1126/science.279.5348.237. [DOI] [PubMed] [Google Scholar]
  93. de Olmos J., Hardy H., Heimer L. The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J Comp Neurol. 1978 Sep 15;181(2):213–244. doi: 10.1002/cne.901810202. [DOI] [PubMed] [Google Scholar]
  94. von Campenhausen H., Yoshihara Y., Mori K. OCAM reveals segregated mitral/tufted cell pathways in developing accessory olfactory bulb. Neuroreport. 1997 Jul 28;8(11):2607–2612. doi: 10.1097/00001756-199707280-00037. [DOI] [PubMed] [Google Scholar]

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