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Structure and diversity in mammalian accessory olfactory bulb

1998; Wiley; Volume: 43; Issue: 6 Linguagem: Inglês

10.1002/(sici)1097-0029(19981215)43

1097-0029

Esmail Meisami, Kunwar P. Bhatnagar,

Neurobiology and Insect Physiology Research

Microscopy Research and TechniqueVolume 43, Issue 6 p. 476-499 Topical PaperFree Access Structure and diversity in mammalian accessory olfactory bulb Esmail Meisami, Esmail Meisami Department of Molecular and Integrative Physiology and the Neuroscience Program, University of Illinois, Urbana, Illinois 61801Search for more papers by this authorKunwar P. Bhatnagar, Kunwar P. Bhatnagar Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky 40292Search for more papers by this author Esmail Meisami, Esmail Meisami Department of Molecular and Integrative Physiology and the Neuroscience Program, University of Illinois, Urbana, Illinois 61801Search for more papers by this authorKunwar P. Bhatnagar, Kunwar P. Bhatnagar Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky 40292Search for more papers by this author First published: 29 December 1998 https://doi.org/10.1002/(SICI)1097-0029(19981215)43:6 3.0.CO;2-VCitations: 149AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract The accessory olfactory bulb (AOB) is the first neural integrative center for the olfactory-like vomeronasal sensory system. In this article, we first briefly present an overview of vomeronasal system organization and review the history of the discovery of mammalian AOB. Next, we briefly review the evolution of the vomeronasal system in vertebrates, in particular the reptiles. Following these introductory aspects, the structure of the rodent AOB, as typical of the well-developed mammalian AOB, is presented, detailing laminar organization and cell types as well as aspects of the homology with the main olfactory bulb. Then, the evolutionary origin and diversity of the AOB in mammalian orders and species is discussed, describing structural, phylogenetic, and species-specific variation in the AOB location, shape, and size and morphologic differentiation and development. The AOB is believed to be absent in fishes but present in terrestrial tetrapods including amphibians; among the reptiles AOB is absent in crocodiles, present in turtles, snakes, and some lizards where it may be as large or larger than the main bulb. The AOB is absent in bird and in the aquatic mammals (whales, porpoises, manatees). Among other mammals, AOB is present in the monotremes and marsupials, edentates, and in the majority of the placental mammals like carnivores, herbivores, as well as rodents and lagomorphs. Most bat species do not have an AOB and among those where one is found, it shows marked variation in size and morphologic development. Among insectivores and primates, AOB shows marked variation in occurrence, size, and morphologic development. It is small in shrews and moles, large in hedgehogs and prosimians; AOB continues to persist in New World monkeys but is not found in the adults of the higher primates such as the Old World monkeys, apes, and humans. In many species where AOB is absent in the adult, it often develops in the embryo and fetus but regresses in later stages of development. Finally, new areas in vomeronasal system research such as the diversity of receptor molecules and the regional variation in receptor neuron type as well as in the output neurons of the AOB and their projection pathways are briefly discussed. In view of the pronounced diversity of size, morphologic differentiation, and phylogenetic development, the need to explore new functions for the vomeronasal system in areas other than sexual and reproductive behaviors is emphasized. Microsc. Res. Tech. 43:476–499, 1998. © 1998 Wiley-Liss, Inc. References Allison AC. 1953a. The morphology of the olfactory system in the vertebrates. Biol Rev 281: 195– 244. Allison AC. 1953b. The structure of the olfactory bulb and its relationship to the olfactory pathways in the rabbit and the rat. J Comp Neurol 98: 309– 355. Bailey K. 1978. Flehman in the ring tailed lemur, Lemur catta. Behaviour 65: 309– 319. Baker H. 1986. Species differences in the distribution of substance-P and tyrosine hydroxylase immunoreactivity in the olfactory bulbs. J Comp Neurol 252: 206– 226. Baker H, Towle AC, Margolis FL. 1988. Differential afferent regulation of dopaminergic and GABAergic neurons in the mouse main olfactory bulb. Brain Res 450: 69– 80. Balogh C. 1860. Das Jacobsonsche Organ de Schafes. S. B. Akad. Wiss. Wien, III, 42: 449– 476. Barber PC, Field PM. 1975. Autoradiographic demonstration of afferent connections of the accessory olfactory bulb in the mouse. Brain Res 85: 201– 203. Barber PC, Raisman G. 1974. An autoradiographic investigation of the projection of the vomeronasal organ to the accessory olfactory bulb in the mouse. Brain Res 81: 21– 30. Baron G, Frahm HD, Bhatnagar KP, Stephan H. 1983. Comparison of brain structure volumes in Insectivora and Primates. III. Main olfactory bulb (MOB). J Hirnforsch 24: 551– 568. Baron G, Stephan H, Fràhm, HD. 1996. Comparative neurobiology in Chiròptera. Vols. 1, 2, and 3. Berlin: Burkhauser Verlag. Bertmar G. 1981. Evolution of vomeronasal organs in vertebrates. Evolution 35: 359– 366. Bhatnagar KP. 1980. The chiropteran vomeronasal organ: its relevance to phylogeny of bats. In: DE Wilson, AL Gardner, editors. Proc. Fifth International Bat Research Conference. Lubbock, TX: Texas Tech Press, p 289– 315. Bhatnagar KP. 1988. Anatomy. In: AM Greehall, U Schmidt, editors. Natural history of vampire bats. Boca Raton, FL: CRC Press, Boca Raton, p 41– 70. Bhatnagar KP, Kallen FC. 1974. Morphology of the nasal cavities and associated structures in Artibeus jamaicensis and Myotis lucifugus. Am J Anat 139: 167– 190. Bhatnagar KP, Reid KH. 1996. 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: 219– 229. Bhatnagar KP, Wible JR. 1994. Observations on the vomeronasal organ of the colugo Cynocephalus (Mammalia, Dermoptera). Acta Anat (Basel) 151: 43– 48. Bhatnagar KP, Kennedy RC, Baron G, Greenberg RA. 1987. Number of mitral cells and bulb volume in the aging human olfactory bulb: a quantitative morphological study. Anat Rec 218: 73– 87. Bonfanti L, Peretto P, Merighi A, Fasolo A. 1997. Newly-generated cells from the rostral migratory stream in the accessory olfactory bulb of the adult rat. Neuroscience 81: 489– 502. Bossy J. 1980. Development of olfactory and related structures in staged human embryo. Anat Embryol (Berlin) 161: 225– 236. Brennan PA, Keverne EB. 1997. Neural mechanisms of mammalian olfactory learning. Prog Neurobiol 51: 457– 481. Burkholder JF. 1918. The anatomy of the brain. 2nd edition. Chicago: Engelhard and Co. Burton PR. 1990. Vomeronasal and olfactory nerves of adult and larval bullfrogs: II. Axon terminations and synaptic contacts in the accessory olfactory bulb. J Comp Neurol 292: 624– 637. y Cajal SR. 1901. Textura del lobulo olfativo accessorio. Trab, del Lab de Invest. Biol., Tome 1. (Republished in Rev. Microsc., 1: 141– 150, 1902); English translation published as: Structure of the accessory olfactory lobule. In: SRy Cajal. Studies on the cerebral cortex (limbic structures). Chicago: The Year Book Publishers, 1955,<//PUBYR> p 127– 134. y Cajal SR. 1911. Histolgie du systeme nerveus de l'hommes et des vertebre. Tome 2. Madrid: Institut Ramoy y Cajal [Maloine, Paris]. Cooper JC, Bhatnagar KP. 1976. Comparative anatomy of the vomeronasal organ complex in bats. J Anat (London) 122: 571– 601. Crosby EC, Humphrey T. 1939a. Studies of the vertebrate telencephalon. I. The nuclear configuration of the olfactory and accessory olfactory formation and of the nucleus olfactorius anterior of certain reptiles, birds and mammals. J Comp Neurol 71: 121– 213. Crosby EC, Humphrey T. 1939b. A comparison of the olfactory and accessory olfactory bulb in certain representative vertebrates. Pap Mich Acad Sci Arts Lett 24: 95– 104. Crosby EC, Humphrey T, Lauer EW. 1962. Correlative anatomy of the nervous system. "Olfactory bulb, accessory olfactory bulb and its associated structures. New York: MacMillan," 414– 418. de Olmos J, Hardy H, Heimer L. 1978. The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J Comp Neurol 181: 213– 244. Dulac C, Axel R. 1995. A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195– 206. Eisthen HL. 1992. Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates. Microsc Res Tech 23: 1– 21. Eisthen HL. 1997. Evolution of vertebrate olfactory systems. Brain Behav Evol 50: 222– 233. Elof FC. 1951. On the organ of Jacobson and the nasal floor cartilage in the chondrocranium of Galago senegalensis. Proc Zool Soc Lond 121: 651– 655. Fox CA. 1940. Certain basal telencephalic centers in the cat. J Comp Neurol 72: 1– 62. Frahm HD. 1981. Volumetric comparison of the accessory olfactory bulb in bats. Acta Anat 109: 173– 183. Frahm HD, Bhatnagar KP. 1980. Comparative morphology of the accessory olfactory bulb in bats. J Anat (Lond) 130: 349– 365. Frahm HD, Stephan H, Baron G. 1984. Comparison of accessory olfactory bulb volumes in the common tree shrew (Tupaia glis). Acta Anat 119: 129– 135. Frets GP. 1914. Beritrage zur vergleichenden Anatomie und Embryologie der Nase der Primaten. Morph Jahrb 48: 239– 279. Fuller TA, Price JL. 1988. Putative glutamatergic and/or aspartatergic cells in the main and accessory olfactory bulbs of the rat. J Comp Neurol 276: 209– 218. Ganser S. 1882. Vergleichend-anatomische Studien uber das Gehirn des Maulworfs. Morph Jahrb 7: 591– 725. Gouda M, Matsutani S, Senba E, Tohyama M. 1990. Peptidergic granule cell populations in the rat main and accessory olfactory bulb. Brain Res 512: 339– 342. Guillamon A, Segovia S. 1997. Sex differences in the vomeronasal system. Brain Res Bull 44: 377– 382. Gurdijian ES. 1925. Olfactory centers in the albino rat with special reference to the stria medullaris and anterior commissure. J Comp Neurol 38: 127– 163. Halpern M. 1987. The organization and function of the vomeronasal system. Ann Rev Neurosci 10: 325– 362. Harrison D. 1987. Preliminary thoughts on the incidence and function of the mammalian vomeronasal organ. Acta Otolaryngol (Stockh) 103: 489– 495. Herrick CL. 1892. The cerebrum and olfactories of the opossum, Deidelphys virginica. J Comp Neurol 2: 1– 23. Herrick CJ. 1924. The nucleus olfactorius anterior of the opossum. J Comp Neurol 37: 317– 359. Holtzman DA, Halpern M. 1990. Embryonic and neonatal development of the vomeronasal and olfactory systems in garter snakes (Thamnophis spp.). J Morphol 203: 123– 140. Huffman HJH. 1963. The olfactory bulb, accessory olfactory bulb and hemispheres of some animals. J Comp Neurol 120: 317– 368. Humphrey T. 1940. The development of the olfactory and the accessory olfactory formation in human embryos and fetuses. J Comp Neurol 73: 431– 468. Humphrey T, Crosby EC. 1938. The human olfactory bulb. Univ Mich Med Bull 4: 61– 62. Iwahori N, Nakamura K, Mameya C. 1989. A Golgi study on the accessory olfactory bulb in the snake, Elaphe quadrivirgata. Neurosci Res 7: 55– 70. Jansen HT, Iwamoto GA, Jackson GL. 1998. Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res Bull 45: 27– 39. Jia C, Halpern M. 1996. Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and Go alpha) and segregated projections to the accessory olfactory bulb. Brain Res 719: 117– 128. Jia C, Halpern M. 1997. Segregated populations of mitral/tufted cells in the accessory olfactory bulb. NeuroReport 8: 1887– 1890. Johnson TN. 1957. The olfactory centers and connections in the cerebral hemispheres of the mole (Scalopus aquaticus machrinus). J Comp Neurol 107: 379– 425. Johnston RE. 1983. Mechanisms of individual discrimination in hamsters. In: D Muller-Schwarz, RM Silverstein, editors. Chemical signals in vertebrates, III. New York: Plenum Press, p 245– 258. Johnston RE. 1985. Olfactory and vomeronasal mechanisms of communication. In: DW Pfaff, editor. Taste, olfaction and the central nervous system. New York: Rockefeller University Press, p 322– 346. Jordan K. 1972. The vomeronasal organ of Jacobson in primates. Folia Morphol 31: 417– 432. Jordan K, Sernicki A. 1967. The cartilage of the nose, vomeronasal organ and palate in Nycticebus tardigradus (L). Folia Morphol 36: 167– 178. Kjaer I, Fischer-Hansen B. 1996. The human vomeronasal organ: prenatal developmental stages and distribution of luteinizing hormone-releasing hormone. Eur J Oral Sci 104: 34– 40. Kölliker, A. 1896. Hanbuch der Gewebelehre des Menschen. Leipzig: W. Englelmann Kratskin IL. 1995. Functional anatomy, central connections and neurochemistry of the mammalian olfactory bulb. In: RL Doty, editor. Handbook of olfaction and gustation. New York: Marcel Dekker, p 103– 126. Kreiner G. 1933. Bulbus olfactorius der Weissen Ratte. Z Anat Enw Gesch 102: 232– 245. Kreutzer EW, Jafek BW. 1980. The vomeronasal organ of Jacobson in the human embryo and fetus. Otolaryngol Head Neck Surg 88: 119– 123. Le Gros Clark WE. 1924. On the brain of the tree-shrew (Tupaia minor). Proc Zool Soc Lond 2: 1053– 1074. Le Gros Clark WE. 1931. The brain of Microcebus murinus. Proc Zool Soc Lond 30: 463– 486. Lauer EW. 1945. The nuclear pattern and fiber connections of certain basal telencephalic centers in the macaque. J Comp Neurol 82: 215– 254. Lohman AHM. 1963. The anterior olfactory lobe of the guinea pig. A descriptive anatomic study Acta Anat (Basel) 53: (Suppl.): 1– 109. Lohman AHM, Lammers HJ. 1964. On the structure and fiber connections of the olfactory centers in mammals. Prog Brain Res 23: 65– 68. Loo SK. 1973. A comparative study of four non-human primates. Folia Morphol 20: 410– 422. Loo SK, Kanagasuntheram R. 1972. The vomeronasal organ in the tree shrew and slow loris. J Anat 112: 165– 172. Mackay-Sim A, Duvall D, Graves BM. 1985. The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ. Brain Behav Evol 27: 186– 194. Macchi G. 1951. The ontogenetic development of the olfactory telencephalon in man. J Comp Neurol 95: 245– 305. Macrides R, Davis BJ. 1983. The olfactory bulb. In: PC Emson, editor. Chemical neuroanatomy. New York, Raven Press, p 391– 426. Mann G. 1961. Bulbus olfactorius accessorius in Chiroptera. J Comp Neurol 116: 135– 144. Mann G. 1963. The rhinencephalon of Chiroptera. Invest Zool Chile 9: 1– 93. McCotter RE. 1912. The connection of the vomeronasal organ with the accessory olfactory bulb in the opossum and mammals. Anat Rec 6: 299– 331. McLean JH, Shipley MT. 1992. Neuroanatomical substrates of olfaction. In: MJ Serby, KL Chobor, editors. Science of olfaction. New York: Springer, p 126– 171. Meisami E. 1979. The developing rat olfactory bulb: Prospects of a new model system for developmental neurobiology. In: E Meisami, MAB Brazier, editors. Neural growth and differentiation. IBRO Monograph Series, Vol. 5. New York: Raven Press, p 183– 206. Meisami E. 1986. Central and peripheral influences on postnatal growth and development of the olfactory bulb in the rat. In: W Breipohl, editor. Ontogeny of olfaction. Principles of olfactory maturation in vertebrates. Berlin: Springer Verlag, p 157– 176. Meisami E. 1988a. The uses of olfaction and its neural development in the neonate. In: C Jones, editor. Fetal and neonatal development. New York: Perinatology Press, p 195– 203. Meisami E. 1988b. Olfactory development in the human. In: E Meisami, PS Timiras, editors. Handbook of human growth and developmental biology. Vol. I, part B, sensory, motor and integrative development. Boca Raton, FL: CRC Press, p 33– 62. Meisami E. 1989. A proposed relationship between increases in the number of olfactory receptor neurons, convergence ratio and sensitivity in the developing rat. Dev Brain Res 46: 9– 19. Meisami E. 1991. Chemoreception. In: C Ladd Prosser, editor. Neural and integrative animal physiology: Vol. 2, comparative animal physiology. 4th ed. New York: Wiley-Liss, p 335– 434. Meisami E. 1991a. Convergence in the vomeronasal and main olfactory system of neonatal and mature mammals and its relation to sensitivity. Soc Neurosci Abstr 17: 635. Meisami E, Sendera TJ. 1993. Morphometry of rat olfactory bulbs stained with cytochrome oxidase reveals that the entire population of glomeruli forms early in the neonatal period. Dev Brain Res 71: 253– 257. Meisami E, Mikhail L, Baim D, Bhatnagar KP. 1998. Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann NY Acad Sci 855: 708– 715. Mendoza AS, Kuderlings I, Kuhn HJ, Kuhna, W. 1994. The vomeronasal organ of the New World monkey saguinus fuscicollis. A light and transmission electron microscopic study Ann Anat 176: 217– 222. Miodonski R. 1968. Bulbus olfactorius of the dog (Canis familiaris). Acta Biol Cracow 11: 65– 75. Monti-Bloch L, Jennings-White C, Dolberg DS, Berliner DL. 1994. The human vomeronasal system. Psychoneuroendocrinology 19: 673– 686. Moran DT, Monti-Bloch L, Steraus J, Berliner DL. 1995. Structure and function of the human vomeronasal organ. In: RL Doty, editor. Handbook of olfaction and gustation. New York: Marcel Dekker, p 793– 820. Mori K, Imamura K, Fujita SC, Obata K. 1987. Projections of two subclasses of vomeronasal nerve fibers to the accessory olfactory bulb in the rabbit. Neuroscience, 20: 259– 278. Negus V. 1958. Comparative anatomy and physiology of the nose and the paranasal sinuses. The organ of Jacobson. London: Churchill Livingstone, p 103– 129. Parsons TS. 1970. The nose and Jacobson's organ. In: BC Gans, editor. Biology of the reptilia, Vol. 2. Morphology. London: Academica Press, p 99– 192. Pospisilova E, Malinsky J. 1985a. The main and the accessory olfactory bulb in the hedgehog (a light microscopic study). Acta Univ Palacki Olomuc Fac Med 108: 93– 107. Pospisilova E, Malinsky J. 1985b. The accessory olfactory bulb of the hedgehog. Folia Morphol (Prah) 33: 34– 37. Raven PH, Johnson GB. 1996. Biology. DuBuque, IA: W. M. Brown, Rasmussen LE, Munger BL. 1996. The sensorineural specialization of the trunk tip (finger) of the Asian elephant, elephas maximus. Anat Rec 246: 127– 134. Roos J, Roos M, Schaeffer C, Aron C. 1988. Sexual differences in the development of the accessory olfactory bulbs in the rat. J Comp Neurol 270: 121– 131. Rosselli-Austin L, Hamilton KH, Williams J. 1987. Early postnatal development of the rat accessory olfactory bulb. Brain Res 433: 304– 308. Salazar I, Cifuentes JM, SanchesQuiterro P, Garcia Caballero T. 1994. Structural and morphometric and immunohistological study of the accessory olfactory bulb in the dog. Anat Rec 240: 277– 285. Scalia F, Winans SS. 1975. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161: 31– 55. Scalia F, Gallousis G, Roca S. 1991. Differential projections of the main and accessory olfactory bulb in the frog. J Comp Neurol 305: 443– 461. Schilling A. 1970. L'organe de Jacobson du lemurien malgache Microcebus murinus (Miller 1977). Mem Mus Hist Nat (Ser. A) 61: 203– 280. Smith CG. 1935. The changes in volume of the olfactory and accessory olfactory bulbs of the albino rat during postnatal life. J Comp Neurol 61: 477– 508. Smith TD, Siegel MI, Mooney MP, Burdi AR, Burrows AM, Todhunter JS. 1997. Prenatal growth of the human vomeronasal organ. Anat Rec 248: 447– 455. Smithson KG, Weiss ML, Hatton GI. 1992. Supraoptic nucleus afferents from the accessory olfactory bulb: evidence from anterograde and retrograde tract tracing in the rat. Brain Res Bull 29: 209– 220. Stephan H. 1965. Der Bulbus olfactorius accessorius bei Insektivoren und Primaten. Acta Anat 62: 215– 253. Stephan H, Baron G, Frahm HD. 1982. Comparison of brain structure volumes in Insectivora and Primates. II. Accessory olfactory bulb (AOB). J Hirnforschung 23: 575– 591. Stephan H, Baron G, Frahm HD. 1991. Insectivora: with a stereotaxic atlas of the hedgehog brain. Comparative brain research in mammals, Vol. 1 Berlin: Springer Verlag. Switzer RC, Johnson JI, Kirsch JAW. 1980. Phylogeny through brain traits. Relation of lateral olfactory tract fibers to the accessory olfactory formation as a palimpsest of mammalian descent. Brain Behav Evol 17: 339– 363. Takagi SF. 1986. Studies in the olfactory system of Old World monkeys. Prog Neurobiol 27: 195– 250. Takagi SF. 1989. Human olfaction. Tokyo: University of Tokyo Press, p 391– 408 Takami S, Graziadei PP. 1990. Morphological complexity of the glomerulus in the rat accessory olfactory bulb: a Golgi study. Brain Res 510: 339– 342. Takami S, Graziadei PP. 1991. Light microscopic Golgi study of mitral/tufted cells in the accessory olfactory bulb of the adult rat. J Comp Neurol 311: 65– 83. Takami S, Graziadei PP. 1992. The morphology of GABA-immunoreactive neurons in the accessory olfactory bulb of rats. Brain Res 588: 317– 323. Takami S, Getchel ML, Chen Y, Monti-Bloch L, Berliner D, Stensaas LJ, Getchel TV. 1993. Vomeronasal epithelial cells of the adult human express neuron-specific molecules. NeuroReport 4: 375– 378. Taniguchi K, Matsuskai Y, Ogawa K, Saito TR. 1992. Fine structure of the vomeronasal organ in the common marmoset (Callithrix jacchus). Folia Primatol 59: 169– 176. Tillet Y, Thibault J, Dubois MP. 1987. Immunocytochemical demonstration of the presence of catecholamine and serotonin neurons in the sheep olfactory bulb. Neuroscience 20: 1011– 1022. Tucker D. 1971. Nonolfactory responses from the nasal cavity: Jacobson's organ and the trigeminal system. In: LM Beidler, editor. Handbook of sensory physiology, vol. IV. Chemical senses, part 1. Olfaction. Berlin: Springer Verlag, p 151– 181. van Gehuchten A, Martin I. 1891. Le bulbe olfactif chez quelques mamiferes. Cellule 7: 203– 237. von Gudden B. 1871. Archiv Psych Nervenkr 11: 693– 723. Wahle P, Sanides-Kohlrausch C, Meyer G, Lubke J. 1990. Substance P- and opioid-immunoreactive structures in olfactory centers of the cat: adult pattern and postnatal development. J Comp Neurol 302: 349– 369. Wible JR, Bhatnagar KP. 1996. Chiropteran vomeronasal complex and the interfamilial relations of bats. J Mamm Evol 3: 285– 314. Wilson DB, Hendrickx AG. 1977. Quantitative aspects of proliferation in the nasal epithelium of the rhesus monkey embryo. J Exp Morphol 38: 217– 226. DE Wilson, DM Reeder, eds. 1993. Mammal species of the world: a taxonomic atlas and geographic reference. Washington, DC: Smith-sonian Institution Press Winkler C, Potter A. 1912. An anatomical guide to experimental research on the rabbit brain. W. Verslyus, Amsterdam. Winkler C, Potter A. 1914. An anatomical guide to experimental research on the cat brain. Amsterdam: W. Verslyus Wollard HH. 1925. The anatomy of Tarsius spectrum. Proc Zool Soc Lond Part 3: 1071– 1184. Wysocki CJ. 1979. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci Behav Rev 3: 301– 341. Wysocki CJ, Meredith M. 1987. The vomeronasal system. In: TE Finger, WL Silver, editors. Neurobiology of taste and olfaction. New York: Wiley, p 125– 150. Young MW. 1936. The nuclear pattern and fiber connections of the non-cortical centers of the rabbit (Lepus cuniculus). J Comp Neurol 65: 295– 401. Zingeser MR. 1984. The nasopalatine ducts and associated structures in the rhesus monkey Macaca mulatta: topography, prenatal development, function and phylogeny. Am J Anat 170: 581– 595. Citing Literature Volume43, Issue615 December 1998Pages 476-499 ReferencesRelatedInformation