Brief Report
Folia Primatol 1992;59:169-176
K. Taniguchia Y. Matsusakia K. Ogawaa T.R. Saitob
Fine Structure of the Vomeronasal Organ in the Common Marmoset
Department of Veterinary Anatomy, Faculty of Agriculture, Iwate University, Morioka, Japan; Department of Laboratory Animal Science, Nippon Veterinary and Animal Science University, Musashino, Japan
(Callithrix ja cchus)
Introduction The occurrence and structure of the vome ronasal organ have been well documented for various vertebrate species [1-10] following the full description of this organ by Jacobson [11]. For primates, however, there have been only a few detailed reports on the structure of this organ [12, 13]. Hunter et al. [14] studied this organ histologically in 3 simian species (owl monkey, Aotus trivirgatus; spider mon key, Ateles geoffroyi; saddle-backed tamarin, Saguinus fuscicollis) and in 1 prosimian spe cies (angwantibo, Arctocebus calabarensis). Johnson et al. [ 15] observed the presence of a part or all of this organ in 70% of adult humans and reported histological findings.
Received: April 9, 1992 Accepted: November 14. 1992
Finally, Loo and Kanagasuntheram [16] de scribed the fine structure of the organ in 1 prosimian species (slow loris, Nycticebus coucang). There have been no previous reports on the fine structure of the organ in simian spe cies. Haplorhine primates are vision-domi nated animals, and all show reductions in the complex anatomical structures subserving ol faction [10], This has led to the absence of the vomeronasal organ in Old World simians [17], On the other hand, there is increasing evidence of the important role played by olfaction in mammalian social and reproduc tive behaviours [18]. In this context, Abbott [19] proposed that this organ might play an important role in certain primate species such
Kazuyuki Taniguchi, PhD Department of Veterinary Anatomy Faculty of Agriculture Iwate University, 3-18-8, Ueda Morioka, Iwate 020 (Japan)
© 1992 S. Karger AG, Basel 0015-5713/92/ 0593-016952.75/0
Downloaded by: Duke Medical Center Library 152.3.102.254 - 1/11/2019 12:38:05 AM
Key Words Common marmoset Jacobson’s organ Nasopalatine duct Olfactory receptors Sensory epithelium Simian primates Vomeronasal organ
Materials and Methods Ten adult common marmosets (Callithrix jacchus) of both sexes were studied. The animals ranged from 250 to 400 g in body weight. For light microscopy, 5 animals of both sexes were sacrificed under ether anaes thesia by cardiac perfusion with physiological saline fol lowed by 10% formalin. The frontal portion of the upper jaw was removed from each animal so as to include the palate and the nasal fossa as far as the cribri form plate. These portions were then decalcified in a mixture of 10% formic acid and 10% formalin for 1-2 months and embedded in celloidin or paraffin by rou tine procedures. Celloidin sections were cut coronally at 30 pm and stained with hematoxylin and eosin to con firm the topography of the vomeronasal organ in the nasal fossa. In addition, paraffin sections were cut seri ally at 7 pm in a coronal plane and processed for stain ing with periodic acid-Schiff and hematoxylin, Alcian blue and hematoxylin or hematoxylin and eosin for his tological observations of the vomeronasal organ. For electron microscopy, 5 animals of both sexes were anaesthetized as for light microscopy and sacri ficed by cardiac perfusion with physiological saline fol lowed by a fixative consisting of 2% paraformaldehyde and 2.5% glutaraldehyde in 0.08 M cacodylatc buffer (pH 7.3). The vomeronasal organ was removed from each animal, immersed in the same fixative for an additional 2 h , postfixed in 1% osmium tetroxide in the same buffer for 1 h and embedded in epoxy resin by routine procedures. Ultrathin sections were cut on a Porter-Blum MT-II ultramicrotome, double-stained with uranyl acetate and lead citrate and examined with a Hitachi H-800 electron microscope. Semithin sec tions were cut at 2 pm, stained with Mallory’s azure II-methylene blue and used for light microscope obser vations.
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Observations Topography and Histological Structure o f the Vomeronasal Organ The vomeronasal organs of the common marmoset are paired tubular structures situ ated at the base of the nasal septum. Each organ is about 4-5 mm in length and sur rounded almost completely by the paraseptal cartilage. It communicates anteriorly with the nasopalatine duct and hence with both oral and nasal cavities, while it ends posteriorly as a blind pouch. The lumen of this organ is slen der and elliptical in coronal section, and it is uniformly lined with sensory epithelium (fig. 1) along almost its entire length. The sensory epithelium consists of senso ry, supporting and basal cells. It is about 4565 pm in height and is covered with micro villi on its free surface. The elliptical nuclei of the supporting cells are arranged in the upper third of the epithelium, while round nuclei of the sensory cells occupy its lower two thirds. The small basal cells are scattered over the basement membrane. By contrast, Jacobson’s glands attached to this organ are situated in the submucosa and penetrate the sensory epi thelium with their ducts to open into the lumen of the organ. These glands consist of tubuloalveolar acini, and intense staining with periodic acid-Schiff indicated the pres ence of neutral mucosubstances, whereas neg ative results with Alcian blue suggested the absence of acid mucins. Fine Structure o f the Vomeronasal Organ Vomeronasal sensory cells were bipolar neurons with a small protrusion at the distal end of the dendrite (fig. 2), whose free surface is densely covered with microvilli. These mi crovilli are slender cylindrical processes con taining several microfilaments running longi tudinally to extend into the cytoplasm. On rare occasions, a structure similar to an olfac-
Taniguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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as the common marmoset, which has pre viously been reported to possess a vomero nasal organ [20], Conflicting findings have been presented with respect to the presence of a functioning vomeronasal organ in simian primates [21]. In the present study, the fine structure of the organ was therefore examined in the common mar moset in order to permit assessment of its func tional significance in the simian primates from a viewpoint of comparative morphology.
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Fig. 1. Vomeronasal sensory epithelium of the common marmoset. The arrow indicates the opening of a duct of Jacobson’s glands. B = Basal cell; Se = sensory cell; Sp = supporting cell. Mallory’s azure II-methylene blue. X 1.000. Fig. 2. Free surface of the vomeronasal sensory epithelium. Arrowheads indicate ciliary precursor bodies. C = Centriole; Mv = microvilli; N f = neurofilaments; Se = sensory cell; Sp = supporting cell; V = vesicle. X 13,600. Fig. 3. Structure similar to an olfactory vesicle on the distal end of a sensory cell (Se). Arrowheads indicate ciliary percursor bodies. Ci = Cilium; Sp = supporting cell. X 13,600. Fig. 4. Perinuclear cytoplasm of a sensory cell. N = Nucleus; N f = neurofilaments; rER = rough endoplasmic reticulum. X 6,800.
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endoplasmic reticulum, often surrounding the axons of sensory cells. Acini of Jacobson’s glands consist of aci nar cells with a high electron density (fig. 7). The nucleus is oval and situated in the basal part of the cell. The cytoplasm contains a con spicuously well-developed Golgi apparatus, mitochondria, lipid droplets and many secre tory granules. These granules are round, about 600-1,000 nm in diameter, low to moderate in electron density and are located in the upper part of the cell.
Discussion The vomeronasal organ communicates with the external world in different ways in different mammalian species. It communi cates directly with the nasal cavity by a small pore on its rostral end in the rabbit [1, 6], guinea pig [1], hamster [5], rat [6, 22], mouse [6, 23] and some bat species [24], while it joins the nasopalatine duct and communi cates with both oral and nasal cavities in the horse [7], cattle [7, 25], sheep [3], dog [1, 8], cat [ 1] and some bat species [24], It communi cates directly with the oral cavity by a duct in the camel [2], In primates, it joins the naso palatine duct and is connected to both oral and nasal cavities in prosimian [12, 14, 16] and New World simian [13,14] species. In the common marmoset, a New World simian, it also joins the nasopalatine duct as in prosim ian and other New World simian species reported previously. The differences in com munication of the vomeronasal organ with the external world may depend on whether the vomeronasal organ detects odoriferous molecules in the nasal cavity or in the oral cavity [18]. The Old World simians, however, are usually said to lack the vomeronasal organ completely because of a major reduction of the olfactory organs. Certainly, they appar-
Taniguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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tory vesicle was observed on the distal end of the dendrite (fig. 3). This structure possessed several cilia with basal bodies. The dendrite is somewhat constricted be low the free surface, where it is connected with the supporting cell by the junctional complex, and contains many pinocytotic vesi cles, several centrioles and ciliary precursor bodies, and occasional smooth endoplasmic reticulum and spirally arranged neurofila ments in its superficial part (fig. 2). Below this area, numerous mitochondria are densely ag gregated and then abruptly replaced by neuro tubules. These neurotubules run parallel in large numbers proximally to reach the supra nuclear cytoplasm. There, Golgi apparatus, rough endoplasmic reticulum, lysosomes and mitochondria are sometimes well developed, although sometimes spirally arranged neuro filaments are well developed instead (fig. 4). The nucleus of the sensory cell is round, with a well-developed nucleolus, and possesses de posits of heterochromatin material at its pe riphery. The cytoplasm of the sensory cell decreases proximal to the nucleus to take the form of an axon, which leaves the sensory epi thelium to join the vomeronasal nerve. Supporting cells are also covered with mi crovilli. These microvilli are a little longer and thicker than those of the sensory cells, small in number, and coated with glycocalyx. The cytoplasm of supporting cells is relatively high in electron density, rich in free ribo somes and mitochondria, and possesses a Golgi apparatus, rough endoplasmic reticu lum and dense bodies in its perinuclear part. The nucleus is elliptical with heterochromatin materials in its periphery (fig. 5). Basal cells of the sensory epithelium are small with scanty cytoplasm and mostly occu pied by a nucleus with an irregular contour (fig. 6). Their cytoplasm is relatively high in electron density and contains a small number of mitochondria, free ribosomes and rough
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Fig. 5. Perinuclear cytoplasm of supporting cells. N = Nucleus; Se = dendrite of a sensory cell; Sp = supporting cell. X 6,800. Fig. 6. Basal cell (B) of the vomeronasal sensory epithelium. N = Nucleus. X 6,800. Fig. 7. Acinus of Jacobson’s glands. A = Acinar cell; G = Golgi apparatus; L = lumen of an acinus; LD = lipid droplet; N = nucleus; SG = secretory granules. X 4,000.
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lumen and lacks any evidence that the organ may be functional. In the present study of the common marmoset, the lumen of this organ was found to be entirely lined with sensory epithelium as in the owl monkey and saddlebacked tamarin. The sensory epithelium may line the entire lumen to compensate for the reduction in size of both the nasal cavity and the vomeronasal organ during phylogeny [16, 17], This may indicate that the organ is func tional in these simian species. The fine structure of the epithelium of the vomeronasal sensory organ has been well doc umented for various mammalian species, in cluding prosimian primates [3, 5-8, 16, 23, 25]. In the present study of the common mar moset, the findings on the fine structure of the sensory epithelium agree well with those pre viously reported for the other mammalian species. Although the present findings cannot be compared with other simian primates be cause of a lack of information, they may at least suggest that the organ is functional in the common marmoset. In prosimian primates, microvilli on the free surface of the sensory cells are reported to be very numerous and greatly elongated, and they are interpreted as the result of elabora tion of the sensory cells in compensation for an overall phylogenetic reduction in size of the vomeronasal organ [16], In the present study, although microvilli of the sensory cells were not so well developed as in prosimian primates, the lumen of the organ was entirely lined with the sensory epithelium, resulting in an increase in the number of sensory cells in the organ. This may also be interpreted as a compensatory elaboration of the organ to off set phylogenetic reduction in its size. In the present study, spirally arranged neu rofilaments were occasionally observed in the dendrite and/or supranuclear cytoplasm of the sensory cell. Although the neurofilaments are generally considered to play a part as the
Tanlguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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ently lack the accessory olfactory bulb. Nev ertheless, Johnson et al. [ 15] recently reported the presence of the vomeronasal organ in humans, although it is rather rudimentary and lacks a sensory epithelium. This may sug gest that the vomeronasal organ is present at least in some Old World simians other than humans. In humans, however, it does not communicate with the nasopalatine duct as in the prosimian and New World simian species but communicates directly with the nasal cav ity. Such a communication may be caused by the simplification of the turbinate system and the disappearance of the nasopalatine duct during evolution of the Old World simians including humans [16, 17]. Therefore, the vomeronasal organ in the Old World simians, if present, may be nonfunctional as a reflec tion of the decrease in reliance on olfactory function. In many mammalian species, the lateral wall of the lumen of the vomeronasal organ is lined with ciliated and pseudostratified respi ratory epithelium, while the medial wall is lined with sensory epithelium consisting of sensory, supporting and basal cells [1,3, 5-8, 10], In the primates, however, the kind of epi thelium lining the lumen varies between spe cies. In prosimian species, such as the angwantibo and the slow loris [ 14, 16], the lateral and medial walls of the lumen are lined with respiratory and sensory epithelium, respec tively, as in many other mammalian species. By contrast, the lumen is entirely lined with sensory epithelium in simian species such as the owl monkey and saddle-backed tamarin [14], In another simian species, the spider monkey [14], however, the epithelium lining the lumen is similar to that lining the nasopal atine duct, thinner and less closely packed than in the sensory epithelium, and seems to be a kind of respiratory epithelium. In hu mans [15], the epithelium is ciliated, pseudo stratified and columnar on all aspects of the
influence on the odoriferous molecules them selves and/or on the mechanism of olfactory perception [18, 28]. Because Jacobson’s and Bowman’s glands are attached to the vome ronasal organ and olfactory epithelium, re spectively, and because these two types of glands differ in the nature of their secretion and morphology of their secretory granules, the respective olfactory receptors are sug gested to play different roles in olfactory per ception [18, 28], In the present study, the glands agreed well in histological and ultrastructural details with those reported pre viously [3, 5, 6, 16, 28] and displayed active granule formation, which may be regarded as further evidence that the vomeronasal organ is functionally active. In summary, all of the histological and ultrastructural findings on the vomeronasal organ in the present sutdy strongly suggest that the organ is actively functional in at least one simian species, the common marmoset.
Acknowledgment The authors wish to express their thanks to Dr. Yoshikuni Tanioka, Central Institute for Experimental Animals, for generously providing the common mar mosets.
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cytoskeleton in the maintenance of the form of a neuron, spirally arranged neurofilaments have never been previously reported, at least in the vomeronasal sensory cell. Since these neurofilaments were only occasionally en countered in the sensory cell, they may appear in relation to ageing of the cell. The signifi cance of their presence in the sensory cell requires further investigation. In addition, a structure similar to an olfac tory vesicle of the olfactory epithelium was observed on the distal end of the sensory cell in the present study. Such modifications of the distal cytoplasm of sensory cells are re ported as cilia in the dog [8] and rabbit [26], as microprocesses in the sheep [3] and horse [7], and as bleb-like cytoplasmic protrusion in cat tle [7], These structures are rarely encoun tered, and their functional significance is still unknown. The structure observed in the present study, however, may be formed on the distal end of sensory cells as a result of modifi cations during development, because both the olfactory epithelium and vomeronasal organ differentiate from the olfactory placode into individual organs [18], and because microvilli of the vomeronasal sensory cell are accompa nied by centrioles and ciliary precursor bod ies, and are hence intermediate in structure between cilia and ordinary microvilli [5, 27], Jacobson’s glands are attached to the vom eronasal organ and secrete neutral mucosubstances [3, 28]. These glands are reported to consist mainly of acinar cells containing many secretory granules and well-developed rough endoplasmic reticulum [3, 5, 6, 16, 28]. The functional significance of the glands must be considered with respect to the mechanism of olfactory perception. In general, odoriferous molecules are at first dissolved in the secre tion of the glands on the surface of the olfac tory receptors before being perceived as olfac tory stimuli. Therefore, the nature of the secretion of the glands may exert some
1 Negus V: The organ of Jacobson. J Anat 1956;90:515-519. 2 Arnautovic I, Abdalla O. Fahmy MFA: Anatomical study of the vom eronasal organ and the nasopalatine duct of the one-humped camel. Acta Anat 1970;77:144-154. 3 Kratzing JE: The structure of the vomeronasal organ in the sheep. J Anat 1970;108:247-260. 4 Kratzing JE: The fine structure of the olfactory and vomeronasal or gans of a lizard (Tiliqtta scincoides scincoides). Cell Tissue Res 1975; 156:239-252. 5 Taniguchi K, Mochizuki K: Mor phological studies on the vomero nasal organ in the golden hamster. Jpn J Vet Sci 1982;44:419-426. 6 Taniguchi K, Mochizuki K: Com parative morphological studies on the vomeronasal organ in rats, mice, and rabbits. Jpn J Vet Sci 1983;45: 67-76. 7 Taniguchi K, Mikami S: Fine struc ture of the epithelia of the vomero nasal organ of horse and cattle: A comparative study. Cell Tissue Res 1985;240:41-48. ’ 8 Adams DR. Wiekamp MD: The ca nine vomeronasal organ. J Anat 1984;138:771-790. 9 Wang RT. Halpcrn M: Light and electron microscopic observations on the normal structure of the vom eronasal organ of garter snakes. J Morphol 1980;164:47-67. 10 Harrison D: Preliminary thoughts on the incidence, structure and func tion of the mammalian vomeronasal organ. Acta Otolaryngol (Stockh) 1987;103:489-495.
11 Jacobson L: Fait à l’Institut, sur un mémoire de M. Jacobson, intitulé: description anatomique d’un organe observé dans les mammifères. Rap port par M. Cuvier. Ann Mus Hist Nat Paris 1811;18:412-424. 12 Eloff FC: On the organ of Jacobson and the nasal floor cartilage in the chondrocranium of Galago senegalensis. Proc Zool Soc Lond 1951 ; 121 : 651-655. 13 Jordan J: The vomeronasal organ (of Jacobson) in primates. Folia Morphol 1972;31:418-432. 14 Hunter AJ. Fleming D, Dixson AF: The structure of the vomeronasal or gan and nasopalatine ducts in Aolus trivirgalus and some other primate species. J Anat 1984; 138:217-226. 15 Johnson A, Josephson R, Hawke M: Clinical and histological evidence for the presence of the vomeronasal (Jacobson’s) organ in adult humans. J Otolaryngol 1985;14:71-79. 16 Loo SK, Kanagasuntheram R: The vomeronasal organ in tree shrew and slow loris. J Anat 1972; 112: 165-172. 17 Loo SK: A comparative study of the nasal fossa of four nonhuman pri mates. Folia Primatol 1973;20:410— 422. 18 Halpern M: The organization and function of the vomeronasal system. Annu Rev Neurosci 1987; 10:325— 362. 19 Abbott DH: Behavioral and physio logical suppression of fertility in subordinate marmoset monkeys. Am J Primatol 1984:6:169-136.
20 Beattie J: The anatomy of the com mon marmoset (Hapale jacchus Kuhl). Proc Zool Soc Lond 1927;2: 593-716. 21 Wysocki CJ: Ncurobehavioural evi dence for the involvement of the vomeronasal system in mammalian reproduction. Neurosci Biobehav Rev 1978;3:301-341. 22 Breipohl W, Bhatnagar KP, Men doza A: Fine structure of the recep tor-free epithelium in the vomero nasal organ of the rat. Cell Tissue Res 1979;200:383-395. 23 Naguro T, Breipohl W: The vome ronasal epithelia of NMRI mouse: A scanning electron-microscopic study. Cell Tissue Res 1982,227: 519-534. 24 Cooper JG, Bhatnagar KP: Compar ative anatomy of the vomeronasal organ complex in bats. J Anat 1976; 122:571-601. 25 Adams DR: The bovine vomero nasal organ. Arch Histol Jpn 1986: 49:211-225. 26 Luckhaus G: Licht- und clektronenmikroskopische Befunde an der Lamina epithelialis dcs Vomeronasalorgans vom Kaninchen. Anat Anz 1969;124:477-489. 27 Kolnberger 1. Altner H: Ciliary structure precursor bodies as stable constituents in the sensory cells of the vomeronasal organ of reptiles and mammals. Z Zellforsch 1971; 118:254-262. 28 Mendoza AS: The mouse vomero nasal glands: A light and electron microscopical study. Chcm Senses 1986:11:541-555.
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References
Folia Primatol 1992;59:169-176
K. Taniguchia Y. Matsusakia K. Ogawaa T.R. Saitob
Fine Structure of the Vomeronasal Organ in the Common Marmoset
Department of Veterinary Anatomy, Faculty of Agriculture, Iwate University, Morioka, Japan; Department of Laboratory Animal Science, Nippon Veterinary and Animal Science University, Musashino, Japan
(Callithrix ja cchus)
Introduction The occurrence and structure of the vome ronasal organ have been well documented for various vertebrate species [1-10] following the full description of this organ by Jacobson [11]. For primates, however, there have been only a few detailed reports on the structure of this organ [12, 13]. Hunter et al. [14] studied this organ histologically in 3 simian species (owl monkey, Aotus trivirgatus; spider mon key, Ateles geoffroyi; saddle-backed tamarin, Saguinus fuscicollis) and in 1 prosimian spe cies (angwantibo, Arctocebus calabarensis). Johnson et al. [ 15] observed the presence of a part or all of this organ in 70% of adult humans and reported histological findings.
Received: April 9, 1992 Accepted: November 14. 1992
Finally, Loo and Kanagasuntheram [16] de scribed the fine structure of the organ in 1 prosimian species (slow loris, Nycticebus coucang). There have been no previous reports on the fine structure of the organ in simian spe cies. Haplorhine primates are vision-domi nated animals, and all show reductions in the complex anatomical structures subserving ol faction [10], This has led to the absence of the vomeronasal organ in Old World simians [17], On the other hand, there is increasing evidence of the important role played by olfaction in mammalian social and reproduc tive behaviours [18]. In this context, Abbott [19] proposed that this organ might play an important role in certain primate species such
Kazuyuki Taniguchi, PhD Department of Veterinary Anatomy Faculty of Agriculture Iwate University, 3-18-8, Ueda Morioka, Iwate 020 (Japan)
© 1992 S. Karger AG, Basel 0015-5713/92/ 0593-016952.75/0
Downloaded by: Duke Medical Center Library 152.3.102.254 - 1/11/2019 12:38:05 AM
Key Words Common marmoset Jacobson’s organ Nasopalatine duct Olfactory receptors Sensory epithelium Simian primates Vomeronasal organ
Materials and Methods Ten adult common marmosets (Callithrix jacchus) of both sexes were studied. The animals ranged from 250 to 400 g in body weight. For light microscopy, 5 animals of both sexes were sacrificed under ether anaes thesia by cardiac perfusion with physiological saline fol lowed by 10% formalin. The frontal portion of the upper jaw was removed from each animal so as to include the palate and the nasal fossa as far as the cribri form plate. These portions were then decalcified in a mixture of 10% formic acid and 10% formalin for 1-2 months and embedded in celloidin or paraffin by rou tine procedures. Celloidin sections were cut coronally at 30 pm and stained with hematoxylin and eosin to con firm the topography of the vomeronasal organ in the nasal fossa. In addition, paraffin sections were cut seri ally at 7 pm in a coronal plane and processed for stain ing with periodic acid-Schiff and hematoxylin, Alcian blue and hematoxylin or hematoxylin and eosin for his tological observations of the vomeronasal organ. For electron microscopy, 5 animals of both sexes were anaesthetized as for light microscopy and sacri ficed by cardiac perfusion with physiological saline fol lowed by a fixative consisting of 2% paraformaldehyde and 2.5% glutaraldehyde in 0.08 M cacodylatc buffer (pH 7.3). The vomeronasal organ was removed from each animal, immersed in the same fixative for an additional 2 h , postfixed in 1% osmium tetroxide in the same buffer for 1 h and embedded in epoxy resin by routine procedures. Ultrathin sections were cut on a Porter-Blum MT-II ultramicrotome, double-stained with uranyl acetate and lead citrate and examined with a Hitachi H-800 electron microscope. Semithin sec tions were cut at 2 pm, stained with Mallory’s azure II-methylene blue and used for light microscope obser vations.
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Observations Topography and Histological Structure o f the Vomeronasal Organ The vomeronasal organs of the common marmoset are paired tubular structures situ ated at the base of the nasal septum. Each organ is about 4-5 mm in length and sur rounded almost completely by the paraseptal cartilage. It communicates anteriorly with the nasopalatine duct and hence with both oral and nasal cavities, while it ends posteriorly as a blind pouch. The lumen of this organ is slen der and elliptical in coronal section, and it is uniformly lined with sensory epithelium (fig. 1) along almost its entire length. The sensory epithelium consists of senso ry, supporting and basal cells. It is about 4565 pm in height and is covered with micro villi on its free surface. The elliptical nuclei of the supporting cells are arranged in the upper third of the epithelium, while round nuclei of the sensory cells occupy its lower two thirds. The small basal cells are scattered over the basement membrane. By contrast, Jacobson’s glands attached to this organ are situated in the submucosa and penetrate the sensory epi thelium with their ducts to open into the lumen of the organ. These glands consist of tubuloalveolar acini, and intense staining with periodic acid-Schiff indicated the pres ence of neutral mucosubstances, whereas neg ative results with Alcian blue suggested the absence of acid mucins. Fine Structure o f the Vomeronasal Organ Vomeronasal sensory cells were bipolar neurons with a small protrusion at the distal end of the dendrite (fig. 2), whose free surface is densely covered with microvilli. These mi crovilli are slender cylindrical processes con taining several microfilaments running longi tudinally to extend into the cytoplasm. On rare occasions, a structure similar to an olfac-
Taniguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
Downloaded by: Duke Medical Center Library 152.3.102.254 - 1/11/2019 12:38:05 AM
as the common marmoset, which has pre viously been reported to possess a vomero nasal organ [20], Conflicting findings have been presented with respect to the presence of a functioning vomeronasal organ in simian primates [21]. In the present study, the fine structure of the organ was therefore examined in the common mar moset in order to permit assessment of its func tional significance in the simian primates from a viewpoint of comparative morphology.
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Fig. 1. Vomeronasal sensory epithelium of the common marmoset. The arrow indicates the opening of a duct of Jacobson’s glands. B = Basal cell; Se = sensory cell; Sp = supporting cell. Mallory’s azure II-methylene blue. X 1.000. Fig. 2. Free surface of the vomeronasal sensory epithelium. Arrowheads indicate ciliary precursor bodies. C = Centriole; Mv = microvilli; N f = neurofilaments; Se = sensory cell; Sp = supporting cell; V = vesicle. X 13,600. Fig. 3. Structure similar to an olfactory vesicle on the distal end of a sensory cell (Se). Arrowheads indicate ciliary percursor bodies. Ci = Cilium; Sp = supporting cell. X 13,600. Fig. 4. Perinuclear cytoplasm of a sensory cell. N = Nucleus; N f = neurofilaments; rER = rough endoplasmic reticulum. X 6,800.
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endoplasmic reticulum, often surrounding the axons of sensory cells. Acini of Jacobson’s glands consist of aci nar cells with a high electron density (fig. 7). The nucleus is oval and situated in the basal part of the cell. The cytoplasm contains a con spicuously well-developed Golgi apparatus, mitochondria, lipid droplets and many secre tory granules. These granules are round, about 600-1,000 nm in diameter, low to moderate in electron density and are located in the upper part of the cell.
Discussion The vomeronasal organ communicates with the external world in different ways in different mammalian species. It communi cates directly with the nasal cavity by a small pore on its rostral end in the rabbit [1, 6], guinea pig [1], hamster [5], rat [6, 22], mouse [6, 23] and some bat species [24], while it joins the nasopalatine duct and communi cates with both oral and nasal cavities in the horse [7], cattle [7, 25], sheep [3], dog [1, 8], cat [ 1] and some bat species [24], It communi cates directly with the oral cavity by a duct in the camel [2], In primates, it joins the naso palatine duct and is connected to both oral and nasal cavities in prosimian [12, 14, 16] and New World simian [13,14] species. In the common marmoset, a New World simian, it also joins the nasopalatine duct as in prosim ian and other New World simian species reported previously. The differences in com munication of the vomeronasal organ with the external world may depend on whether the vomeronasal organ detects odoriferous molecules in the nasal cavity or in the oral cavity [18]. The Old World simians, however, are usually said to lack the vomeronasal organ completely because of a major reduction of the olfactory organs. Certainly, they appar-
Taniguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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tory vesicle was observed on the distal end of the dendrite (fig. 3). This structure possessed several cilia with basal bodies. The dendrite is somewhat constricted be low the free surface, where it is connected with the supporting cell by the junctional complex, and contains many pinocytotic vesi cles, several centrioles and ciliary precursor bodies, and occasional smooth endoplasmic reticulum and spirally arranged neurofila ments in its superficial part (fig. 2). Below this area, numerous mitochondria are densely ag gregated and then abruptly replaced by neuro tubules. These neurotubules run parallel in large numbers proximally to reach the supra nuclear cytoplasm. There, Golgi apparatus, rough endoplasmic reticulum, lysosomes and mitochondria are sometimes well developed, although sometimes spirally arranged neuro filaments are well developed instead (fig. 4). The nucleus of the sensory cell is round, with a well-developed nucleolus, and possesses de posits of heterochromatin material at its pe riphery. The cytoplasm of the sensory cell decreases proximal to the nucleus to take the form of an axon, which leaves the sensory epi thelium to join the vomeronasal nerve. Supporting cells are also covered with mi crovilli. These microvilli are a little longer and thicker than those of the sensory cells, small in number, and coated with glycocalyx. The cytoplasm of supporting cells is relatively high in electron density, rich in free ribo somes and mitochondria, and possesses a Golgi apparatus, rough endoplasmic reticu lum and dense bodies in its perinuclear part. The nucleus is elliptical with heterochromatin materials in its periphery (fig. 5). Basal cells of the sensory epithelium are small with scanty cytoplasm and mostly occu pied by a nucleus with an irregular contour (fig. 6). Their cytoplasm is relatively high in electron density and contains a small number of mitochondria, free ribosomes and rough
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Fig. 5. Perinuclear cytoplasm of supporting cells. N = Nucleus; Se = dendrite of a sensory cell; Sp = supporting cell. X 6,800. Fig. 6. Basal cell (B) of the vomeronasal sensory epithelium. N = Nucleus. X 6,800. Fig. 7. Acinus of Jacobson’s glands. A = Acinar cell; G = Golgi apparatus; L = lumen of an acinus; LD = lipid droplet; N = nucleus; SG = secretory granules. X 4,000.
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lumen and lacks any evidence that the organ may be functional. In the present study of the common marmoset, the lumen of this organ was found to be entirely lined with sensory epithelium as in the owl monkey and saddlebacked tamarin. The sensory epithelium may line the entire lumen to compensate for the reduction in size of both the nasal cavity and the vomeronasal organ during phylogeny [16, 17], This may indicate that the organ is func tional in these simian species. The fine structure of the epithelium of the vomeronasal sensory organ has been well doc umented for various mammalian species, in cluding prosimian primates [3, 5-8, 16, 23, 25]. In the present study of the common mar moset, the findings on the fine structure of the sensory epithelium agree well with those pre viously reported for the other mammalian species. Although the present findings cannot be compared with other simian primates be cause of a lack of information, they may at least suggest that the organ is functional in the common marmoset. In prosimian primates, microvilli on the free surface of the sensory cells are reported to be very numerous and greatly elongated, and they are interpreted as the result of elabora tion of the sensory cells in compensation for an overall phylogenetic reduction in size of the vomeronasal organ [16], In the present study, although microvilli of the sensory cells were not so well developed as in prosimian primates, the lumen of the organ was entirely lined with the sensory epithelium, resulting in an increase in the number of sensory cells in the organ. This may also be interpreted as a compensatory elaboration of the organ to off set phylogenetic reduction in its size. In the present study, spirally arranged neu rofilaments were occasionally observed in the dendrite and/or supranuclear cytoplasm of the sensory cell. Although the neurofilaments are generally considered to play a part as the
Tanlguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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ently lack the accessory olfactory bulb. Nev ertheless, Johnson et al. [ 15] recently reported the presence of the vomeronasal organ in humans, although it is rather rudimentary and lacks a sensory epithelium. This may sug gest that the vomeronasal organ is present at least in some Old World simians other than humans. In humans, however, it does not communicate with the nasopalatine duct as in the prosimian and New World simian species but communicates directly with the nasal cav ity. Such a communication may be caused by the simplification of the turbinate system and the disappearance of the nasopalatine duct during evolution of the Old World simians including humans [16, 17]. Therefore, the vomeronasal organ in the Old World simians, if present, may be nonfunctional as a reflec tion of the decrease in reliance on olfactory function. In many mammalian species, the lateral wall of the lumen of the vomeronasal organ is lined with ciliated and pseudostratified respi ratory epithelium, while the medial wall is lined with sensory epithelium consisting of sensory, supporting and basal cells [1,3, 5-8, 10], In the primates, however, the kind of epi thelium lining the lumen varies between spe cies. In prosimian species, such as the angwantibo and the slow loris [ 14, 16], the lateral and medial walls of the lumen are lined with respiratory and sensory epithelium, respec tively, as in many other mammalian species. By contrast, the lumen is entirely lined with sensory epithelium in simian species such as the owl monkey and saddle-backed tamarin [14], In another simian species, the spider monkey [14], however, the epithelium lining the lumen is similar to that lining the nasopal atine duct, thinner and less closely packed than in the sensory epithelium, and seems to be a kind of respiratory epithelium. In hu mans [15], the epithelium is ciliated, pseudo stratified and columnar on all aspects of the
influence on the odoriferous molecules them selves and/or on the mechanism of olfactory perception [18, 28]. Because Jacobson’s and Bowman’s glands are attached to the vome ronasal organ and olfactory epithelium, re spectively, and because these two types of glands differ in the nature of their secretion and morphology of their secretory granules, the respective olfactory receptors are sug gested to play different roles in olfactory per ception [18, 28], In the present study, the glands agreed well in histological and ultrastructural details with those reported pre viously [3, 5, 6, 16, 28] and displayed active granule formation, which may be regarded as further evidence that the vomeronasal organ is functionally active. In summary, all of the histological and ultrastructural findings on the vomeronasal organ in the present sutdy strongly suggest that the organ is actively functional in at least one simian species, the common marmoset.
Acknowledgment The authors wish to express their thanks to Dr. Yoshikuni Tanioka, Central Institute for Experimental Animals, for generously providing the common mar mosets.
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cytoskeleton in the maintenance of the form of a neuron, spirally arranged neurofilaments have never been previously reported, at least in the vomeronasal sensory cell. Since these neurofilaments were only occasionally en countered in the sensory cell, they may appear in relation to ageing of the cell. The signifi cance of their presence in the sensory cell requires further investigation. In addition, a structure similar to an olfac tory vesicle of the olfactory epithelium was observed on the distal end of the sensory cell in the present study. Such modifications of the distal cytoplasm of sensory cells are re ported as cilia in the dog [8] and rabbit [26], as microprocesses in the sheep [3] and horse [7], and as bleb-like cytoplasmic protrusion in cat tle [7], These structures are rarely encoun tered, and their functional significance is still unknown. The structure observed in the present study, however, may be formed on the distal end of sensory cells as a result of modifi cations during development, because both the olfactory epithelium and vomeronasal organ differentiate from the olfactory placode into individual organs [18], and because microvilli of the vomeronasal sensory cell are accompa nied by centrioles and ciliary precursor bod ies, and are hence intermediate in structure between cilia and ordinary microvilli [5, 27], Jacobson’s glands are attached to the vom eronasal organ and secrete neutral mucosubstances [3, 28]. These glands are reported to consist mainly of acinar cells containing many secretory granules and well-developed rough endoplasmic reticulum [3, 5, 6, 16, 28]. The functional significance of the glands must be considered with respect to the mechanism of olfactory perception. In general, odoriferous molecules are at first dissolved in the secre tion of the glands on the surface of the olfac tory receptors before being perceived as olfac tory stimuli. Therefore, the nature of the secretion of the glands may exert some
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Taniguchi/Matsusaki/Ogawa/Saito
Vomeronasal Organ of the Common Marmoset
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References
