Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius)

Summary The olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) has been studied with a conventional histochemical and a novel immunological staining technique. In both species, the sensory epithelium is arranged in folds separated by non-sensory epithelial tissue. In the nine-spined stickleback, intrinsic folds consisting of non-sensory cells are found in the apical part of the sensory epithelium where they divide the surface of the sensory epithelium into small islets. These non-sensory cells are non-ciliated, flattened and piled on top of each other; they contain numerous electron-translucent vesicles. The intrinsic folds are absent from the sensory epithelium of the three-spined stickleback. In both species, axons of receptor cells form a layer of fibers in the sensory epithelium immediately above the basal cells. In the three-spined stickleback, thick branches of the olfactory nerve are frequently found in this layer. These branches are only occasionally observed in the sensory epithelium of the nine-spined stickleback. Thus, the three-spined stickleback and the nine-spined stickleback show considerable differences in the organization of the sensory regions of the olfactory epithelium.     

Developmental expression of the calcium‐activated chloride channels TMEM16A and TMEM16B in the mouse olfactory epithelium

Calcium‐activated chloride channels are involved in several physiological processes including olfactory perception. TMEM16A and TMEM16B, members of the transmembrane protein 16 family (TMEM16), are responsible for calcium‐activated chloride currents in several cells. Both are present in the olfactory epithelium of adult mice, but little is known about their expression during embryonic development. Using immunohistochemistry we studied their expression in the mouse olfactory epithelium at various stages of prenatal development from embryonic day (E) 12.5 to E18.5 as well as in postnatal mice. At E12.5, TMEM16A immunoreactivity was present at the apical surface of the entire olfactory epithelium, but from E16.5 became restricted to a region near the transition zone with the respiratory epithelium, where localized at the apical part of supporting cells and in their microvilli. In contrast, TMEM16B immunoreactivity was present at E14.5 at the apical surface of the entire olfactory epithelium, increased in subsequent days, and localized to the cilia of mature olfactory sensory neurons. These data suggest different functional roles for TMEM16A and TMEM16B in the developing as well as in the postnatal olfactory epithelium. The presence of TMEM16A at the apical part and in microvilli of supporting cells is consistent with a role in the regulation of the chloride ionic composition of the mucus covering the apical surface of the olfactory epithelium, whereas the localization of TMEM16B to the cilia of mature olfactory sensory neurons is consistent with a role in olfactory signal transduction. © 2013 Wiley Periodicals, Inc. Develop Neurobiol 74: 657–675, 2014     

Photoreceptors of Bryozoan Larvae (Cheilostomata, Cellularioidea)

The ultrastructure of potential photoreceptors in larvae of Tricellaria occidentalis and four species of Bugula is described and compared with previously reported photoreceptors in larvae of Bugula neritina and Scrupocellaria bertholetti. A single sensory cell forms the functional unit of each photoreceptor. This cell is distinguished by a concentration of pigment vesicles in its apical part, a direct connection with the nervous system, and a large number of cilia that form the photoreceptoral organelle. These cilia have axonemes morphologically identical to those of motile cilia. The membranes of sensory cilia are unbeaded and qualitatively less osmophilic than those of the motile cilia of adjacent accessory and coronal cells. Three photoreceptor types are designated based on topological complexity: Type I, in which the sensory cell is flush with adjacent coronal cells and the photoreceptoral organelle is unprotected; Type II, in which the apical surface of the sensory cell is invaginated, forming a lumen containing the photoreceptoral organelle; and Type III, in which the sensory cell is at the base of an epidermal invagination and the photoreceptoral organelle is protected in a lumen formed by the sensory cell and accessory cells. There is a greater range of morphological variation among photoreceptors in larvae of Bugula spp. than between those of two species of the related genera Scrupocellaria and Tricellaria.     

Cartilaginous torus epithelium of the vomeronasal organ of swine and sheep]

The vomeronasal organ consists of receptor cells of microvillous type, supporting and basal cells. According to their ultrastructural organization the microvillar cells are analogous to those in the main olfactory organ in the pig and have all signs of the receptor cell: microvilli at the top and centrioles in cytoplasm, as well as the central process getting off the cell body. Both in the pig and in the sheep the supporting cells contain in their apical region a number of basal bodies with cilia, getting them off. In the receptor zones of epithelium albuminous glands predominate, in the respiratory zones--mucous ones. A great amount of liquid mucus, excreted on the surface of the epithelium by numerous glands and supporting cells, apparently, facilitates adsorption and desorption of odorous molecules from the receptor cells after their stimulation. The cilia of the supporting cells probably from the stream of the vomeronasal mucus. The cartilagenous torus epithelium of the vomeronasal organ of the pig and sheep has in general a similar structural organization. This demonstrates general for Vertebrata receptor mechanisms of odorous substances, evidently connected with perception of feramones or contact olfaction.     

Fine structure of the vomeronasal organ in the grass lizard, Takydromus tachydromoides

The squamates are composed of many taxa, among which there is morphological variation in the vomeronasal organ (VNO). To elucidate the evolution of chemoreception in squamate reptiles, morphological data from the VNO from a variety of squamate species is required. In this study, the morphology of the VNO of the grass lizard Takydromus tachydromoides was examined using light and electron microscopy. The VNO consists of a pair of dome-shaped structures, which communicate with the oral cavity. There are no associated glandular structures. Microvilli are present on the apical surfaces of receptor cells in its sensory epithelium, as well as on supporting cells, and there are centrioles and ciliary precursor bodies on the dendrites. In addition to ciliated cells and basal cells in the non-sensory epithelium, there is a novel type of non-ciliated cell in T. tachydromoides. They have constricted apical cytoplasm and microvilli instead of cilia, and are sparsely distributed in the epithelium. Based on these results, the variation in the morphology of the VNO in scincomorpha, a representative squamate taxon, is discussed.     

OLFACTORY CILIA IN THE FROG

Olfactory epithelium from the frog was examined in the living state by light microscopy and in the fixed state by electron microscopy. Particular attention was paid to the layer of cilia and mucus which covers the surface of the epithelium. The olfactory cilia differed from typical cilia in that they (a) arose from bipolar neurons and had centrioles near their basal bodies, (b) were up to 200 microns in length, of which the greater part was a distal segment containing an atypical array of ciliary fibers, (c) were often immotile, (d) had their distal segments arranged in parallel rows near the surface of the mucus, and (e) had many vesicles along their shafts and had splits in the array of fibers in their distal segments. These specializations make the olfactory cilia similar to cilia found on other sensory cells and support the theory that they are the locus where electrical excitation in the olfactory organ is initiated by contact with odorous substances.     

The ultrastructural organization of olfactory epithelium of two species of gadoid fish

The untrastructural organization of the olfactory epithelium of the cod Gadus morhua (L.) and the haddock Melanogrammus aeglefinus (L.) was studied using both transmission and scanning electron microscopy. The olfactory rosette was found to exhibit regional differences; the faces of the olfactory lamella were composed of sensory epithelium, the edges were non-sensory. The cellular organization of the olfactory epithelium was determined and consisted of bi-polar sensory neurones, supporting cells, mucous cells and basal cells. The ultrastructure of the sensory cells was consistent, having an elongate cell, the free surface of which terminated in an olfactory vesicle from which arose either four olfactory cilia or numerous microvilli. Ciliary aggregations have been found in the two species of gadoid fish studied; it is suggested that these structures aid in the separation and in the circulation of fluid between the lamellae. The surface structure of the supporting cells was found to be of two types: either ciliated or ridged; the former presenting distinct ciliated tufts, the latter showing definite, but unorganized, ridges over the epithelium surface.     

Electron microscope observations on chemo- and mechano-receptor cells of fishes

Summary This paper reports on the fine structure of chemo and mechano-receptor cells found in three species of fishes (Corydoras paleatus, Cnesterodon decemmaculatus, Fitzroyia lineata).Taste cells were studied in the food-finding barbels of adult species belonging to the Genus Corydoras. They are characterized by the presence of a great amount of vesicular material concentrated at the level of the apical and medial region. Most of these cells terminate at the barbel surface by means of a cylindrical or tapered extremity devoid of sensory hairs. It was possible to observe, in some cases, the existence of short and ill defined microvilli. The basal pole of each sensory cell contacts with several sensory nerve fibers. These fibers contain mitochondria and a few vesicles.The fine structure of the olfactory neurons was studied in full-developed embryos of Cnesterodon and Fitzroyia. The olfactory sensory hairs consist of long cilia which project into the lumen of the olfactory pit. Cilia arise from the olfactory knob which is merely an apical swelling of the dendrite. The dendrite of the olfactory neuron shows profiles of small tubules, aligned parallel to its length. Near the basement membrane of the epithelium groups of axons are seen encased in the surface of the sustentacular cells.The mechano-receptor cells studied were: 1.) The sensory cells existing in the neuromasts of the lateral line system of Cnesterodon and Fitzroyia, and 2.) the receptor cells of the ampullar crests of the same species.Neuromast receptor-cells have well developed sensory hairs which consist of cilia and microvilli. It is highly probable that each receptor cell, like those of the vestibular epithelium, bears only one cilium asymmetrically located in relation to the units of the sensory process. One of the most striking characteristics of this type of cell is the existence of a high amount of vesicular material accumulated in the cytoplasm of the basal region; it is at this level that the nerve fibers take contact with the receptor cell membrane.Three main types of neuroepithelial junction are described in the neuromasts (nerve fiber deeply recessed in the cytoplasm, calyx type and knob-like ending). In these junctions the vesicular material is almost exclusively concentrated in the cytoplasm of the receptor cell, while only few vesicles are seen within the neuroplasm of the sensory fibers.The receptor cells occuring in the ampullar crests of Cnesterodon and Fitzroyia show many structural characteristics similar to those present in neuromasts' receptor cells. Like these, they bear sensory hairs consisting of several microvilli and only one cilium which is always asymmetrically located within the group of hairs. The basal region of the cell is filled with a large amount of small vesicles. Nerve endings also show vesicles but they are less in number than inside the cytoplasm of the receptor cell.Comments are made on the apparent significance of the sensory hairs. These structures are considered (in chemo-receptor cells) as devices serving to enlarge the active surface of the cell and increasing by this way the effectiveness of the whole receptive system. In mechano-receptor cells cilia and microvilli may act as levers of different mechanical characteristics which convey stimuli to the receptor-cell cytoplasm.In this paper three main types of neuroepithelial junctions connecting receptor cells with the central nervous system are described.     

Scanning electron microscopy of the channel catfish olfactory lamellae

The olfactory lamellae of the channel catfish (Ictalurus punctatus) are composed of sensory and indifferent (non-sensory) epithelia organized into two distinct regions on both surfaces of each lamella. The smaller sensory region located adjacent to the midline raphe has fewer cilia per unit surface area than the indifferent epithelium and contains the olfactory neurons whose ciliated dendritic terminals occur at the epithelial surface. The indifferent epithelium, comprising the greater surface area of the olfactory lamella, is covered with a dense mat of non-sensory cilia. Fractured carbon dioxide critical point dried lamellar tissue revealed the underlying cellular structure. The lamellae are composed of two layers of epithelium enclosing a thin stromal layer. Olfactory receptors were observed in the fractured tissue only within the sensory epithelium.     

Ultrastructural studies on the epithelia of the olfactory organ of cyprinodonts (teleostei,cyprinodontoidea)

Summary The epithelia of the olfactory organ of two cyprinodontoid fish species were studied both by transmission and scanning electron microscopy. The relatively flat floor of the organ is covered by sensory and nonsensory epithelia. The latter is distributed in the form of bands or ridges separating distinct areas of sensory epithelium. Differences between the olfactory organs of the two species investigated related only to the topography and quantitative distribution of the epithelia. Their ultrastructural features are very similar. The nonsensory stratified squamous epithelium contains numerous goblet cells and surface cells provided with microridges. A hypothetical function of the microridges is discussed. The sensory epithelium consists mainly of basal, supporting, and two types of sensory cells, i.e., ciliated and microvillous receptor cells. The cilia exhibit a predominant 9+0 microtubule pattern. Both epithelia are covered by a mucus layer in which all surface structures seem to be embedded. The possible nature, origin, and movement mechanisms of the mucus are discussed.This work was supported by the Deutsche ForschungsgemeinschaftDedicated to Prof. Dr. med. W. Bargmann on the occasion of his 70th birthday     

Das Epithel der Tuba uterina des Neugeborenen Elektronenmikroskopische Befunde

Summary An electron microscopical study of the epithelium of the uterine tube was carried out in the newborn. Among the epithelial cells at least two morphologically well defined types can be distinguished: ciliated and non-ciliated cells.The ultrastructure of the cilia and related structures corresponds to what has been described by other authors in ciliated cells of various organs and of different species. Near the basal bodies of the cilia there is a concentration of vesicular mitochondria, which is thought to be evidence of a high metabolic activity in this region of the cell. Large opaque granules in the supranuclear zone of the ciliated cells are, it is suggested, paraplasmatic inclusions, perhaps supporting material for the ciliokinetic processes. There was no evidence of a secretory function of the ciliated cells.Among the non-ciliated cells, which in general show a straight lined luminal border with few microvilli, there are some cells containing dense granules, which are distributed throughout the cytoplasm and concentrated in the luminar side of the cell. The apical parts of these cells are protruding and sometimes digitated or branched; they contain accumulated granular materials and are separated from the rest of the cell after the formation of an intracellular plasmalemma. A similar detachment was found in an other cell type, but here the protruded apical parts of the cells are edematous and do not contain any visible secretory materials. It is uncertain if the detached cytoplasmic substances form a part of a specific secretory product; there are no secretory granules within the cytoplasm. On the contrary, the detachment of cytoplasmic parts may only accompany the excessive proliferation of cells which takes place during this period of growth.     

Histology and ultrastructure of the olfactory organ of the freshwater pulmonate Helisoma trivolvis

Summary The olfactory organ of Helisoma trivolvis is located on the surface of the body at the base of the cephalic tentacles. An evagination of skin, the olfactory plica, at the base of the tentacle extends over the olfactory organ dorsally. The epithelium of the olfactory organs contains unspecialized epithelial cells, ciliated epithelial cells, basal cells, mucous secretory cells, and sensory dendrites. The surface of the epithelium has a complex brush border of thick plasmatic processes, which branch to form several terminal microvillar twigs. Long slender cytoplasmic processes form a dense spongy layer among the plasmatic processes beneath the level of the terminal twigs. Bipolar primary sensory neurons clustered beneath the epithelium of the olfactory organ send dendrites through the epithelium to the free surface. Some sensory endings have a few short cilia, but most bear only microvilli. Cilia of sensory endings and epithelial cells extend beyond the brush border of the epithelium. Small axons arise from the perikarya of the sensory neurons and enter a branch of the olfactory nerve. HRP tracing indicates that the axons pass to the cerebral ganglion without interruption. Histochemical tests indicate that the sensory neurons are neither aminergic nor cholinergic.     

Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: The significance of structure–function relationships based on phylogeny and ecology

This study investigated the relationship between olfactory morphology, habitat occupancy, and lifestyle in 21 elasmobranch species in a phylogenetic context. Four measures of olfactory capability, that is, the number of olfactory lamellae, the surface area of the olfactory epithelium, the mass of the olfactory bulb, and the mass of the olfactory rosette were compared between individual species and groups, comprised of species with similar habitat and/or lifestyle. Statistical analyses using generalized least squares phylogenetic regression revealed that bentho‐pelagic sharks and rays possess significantly more olfactory lamellae and larger sensory epithelial surface areas than benthic species. There was no significant correlation between either olfactory bulb or rosette mass and habitat type. There was also no significant difference between the number of lamellae or the size of the sensory surface area in groups comprised of species with similar diets, that is, groups preying predominantly on crustaceans, cephalopods, echinoderms, polychaetes, molluscs, or teleosts. However, some groups had significantly larger olfactory bulb or rosette masses than others. There was little evidence to support a correlation between phylogeny and morphology, indicating that differences in olfactory capabilities are the result of functional rather than phylogenetic adaptations. All olfactory epithelia exhibited microvilli and cilia, with microvilli in both nonsensory and sensory areas, and cilia only in sensory areas. Cilia over the sensory epithelia originated from supporting cells. In contrast to teleosts, which possess ciliated and microvillous olfactory receptor types, no ciliated olfactory receptor cells were observed. This is the first comprehensive study comparing olfactory morphology to several aspects of elasmobranch ecology in a phylogenetic context. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Postnatal development of the vomeronasal epithelium in the rat: an ultrastructural study

Three basic types of cells are distinguished in the rat vomeronasal epithelium at birth: bipolar neurons, supporting cells, and basal cells. Neurons at this time include both immature and differentiated cells. By the end of the first postnatal week, all neurons show morphological signs of maturity in their cytoplasm, including abundant granular and smooth endoplasmic reticulum, neurotubules, dense lamellar bodies, apical centrioles, and tufts of microvilli. During the third week microvilli are more frequently encountered and appear to be longer and more branched. Supporting cells appear well-developed by the second day after birth. During the first ten days of life, supporting cells lose their centrioles and all of the complex associated with ciliary generation in the apical zone. Basal cells appear to be more numerous in newborns than in older animals. Protrusions projecting into the lumen are frequently observed in the epithelium of newborn animals, both on the dendrites of neurons and on supporting cells. After the third week, such protrusions are only observed in the transitional zone between the sensory and the non-sensory epithelia of the vomeronasal tubes. In this transitional zone, a fourth cell type showing apical protrusions with microvilli differentiates. Cytoplasm in this type resembles that of neighboring ciliated cells but has no cilia or centrioles. These transitional cells are considered to be cells in an intermediate state of differentiation, between that of the differentiated neurons and supporting cells of the sensory epithelium and that of the predominate ciliated cells of the non-sensory epithelium. The results suggest that by the end of the third week the vomeronasal epithelium is morphologically mature.     

The Nervous System of the Male Dinophilus gyrociliatus (Annelida: Polychaeta). I. Number, Types and Distribution Pattern of Sensory Cells

The entire nervous system of the smallest annelid hitherto known, the dwarf male of the highly dimorphic species Dinophilus gyrociliatus , has been reconstructed by means of TEM investigations of serial ultrathin sections. Altogether there are 68 neurons, 40 of which have a sensory function. The structure and distribution of them is described. The receptor endings of the 20 sensory cells of each side are located either in two groups — the anterior receptor group and the posterior receptor group — or are singly positioned in the integument. Structural differences of the apical portion of the dendrites enables four types of receptors to be distinguished: three types with emergent cilia and one type with non-emergent cilia. Neurons with emergent cilia can be monociliated collar cells as well as mono- or multiciliated cells without collar. Special vesicle-in-vesicle structures, are located close to the basal portion of the cilia in some of these cells. The non-emergent cilia border closely to a neighbouring epidermal cell and contain a prominent intraciliary vesicle. The function of receptors is discussed with regard to a comparison with receptors in other polychaete species, structural specializations and their distribution pattern on the animal's surface.     

A SEM study of the olfactory lamellae of the catfish Heteropneustes fossilis (Bl.)

The olfactory lamellae of the catfish H. fossilis (Bl.) was studied in the scanning electron microscope. The olfactory lamellae are composed of sensory and non-sensory epithelium. The sensory epithelium contains large numbers of ciliated receptor cells, whereas the non-sensory raphe epithelium is covered with a dense mat of non-sensory cilia. It is not known whether the olfactory cilia possess receptor sites.     

"Light" epithelial cells of swine and bovine oviducts

The ultrastructure of oviduct epithelium of clinically healthy cows and 15 sows was investigated using scanning and transmission electron microscopy. In all parts of the oviduct, ciliated and non-ciliated epithelial cells are present, but their number varies in both the investigated animals in different regions of the oviduct, depending on the phase of the estrous cycle. In addition to ciliated cells with numerous cilia on their luminal surface, so-called pale ciliary cells were found in all parts of the oviduct of cows and sows. The cytoplasm of these cells is electron-lucent, their luminal surface carries few cilia and short microvilli. The apical cytoplasm contains species specific secretory granules, which means that these cells have features characteristic of both secretory and ciliated cells. It is suggested that the pale ciliated and non-ciliated secretory cells are functional stages of the same tubar epithelium cell, and that the transformation between these two cell types is regulated by functional requirements of the organ in different phases of the estrous cycle.     

Fine structure of the Malpighian tubules in the housefly, Musca domestica

The epithelium of the Malpighian tubules in the housefly is comprised of four distinct cellular types. Type I cells are characterized by the presence of intimate associations between infoldings of basal plasma membrane and mitochondria. On the luminal surface, cytoplasm is extended into microvilli which contain mitochondria. Membrane-bound vacuoles in the cytoplasm seem to progressively accumulate granular material. Type II cells have dilated canaliculi. Microvilli lack mitochondria. The Type III cell has not been reported previously in Malpighian tubules. It has very well-developed granular endoplasmic reticulum which contains intracisternal bundles of tubules. Cytoplasm contains numerous electron dense bodies. Type IV cells occur in the common duct region of the Malpighian tubules. Mitochondria do not extend into the microvilli.     

Surface ultrastructure of the olfactory rosette of an air-breathing catfish,Heteropneustes fossilis (Bloch)

The surface architecture of the olfactory rosette ofHeteropneustes fossilis (Bloch) has been studied by scanning electron microscopy. The olfactory rosette is an oval structure composed of a number of lamellae arranged pinnately on a median raphe. The raphe is invested with epithelial cells and pits which represent goblet cell openings. On the basis of cellular characteristics and their distribution the lateral surface of each olfactory lamella is identified as sensory, ciliated non-sensory and non-ciliated non-sensory epithelium. The sensory epithelium is provided with receptor and supporting cells. The ciliated non-sensory epithelium is covered with dense cilia obscuring the presence of other cell types. The non-ciliated non-sensory epithelium is with many polygonal areas containing cells.     

The postbranchial digestive tract of the ascidian, Polyandrocarpa misakiensis (Tunicata: Ascidiacea). 1. Oesophagus

The organization of the oesophagus in the budding styelid ascidian, Polyandrocarpa misakiensis, is described. The oesophagus consists of external and internal epithelium, and there are loose connective tissue, blood sinuses, and a muscular layer between them. The internal epithelium is simple columnar, except for the bottom of three folds. The external epithelium is simple squamous. The internal epithelium contains four cell types, i.e., ciliated mucous cells, band cells, endocrine cells, and undifferentiated cells. The ciliated mucous cells have apical cilia and microvilli, and two types of mucous vesicle. The band cells also have apical cilia and electron-dense granules in the apical cytoplasm. The endocrine cells are bottle-shaped, and have electron-dense granules both above and below the nucleus. The undifferentiated cells form pseudostratified epithelium at the bottom of each fold, and they have nuclei with prominent nucleoli. One type of coelomic cell, which has retractile cytoplasm, often migrates in the internal epithelium. Near the stomach, there are many darkly stained round cells clustered around the posterior end of the oesophagus. These two types of coelomic cells may be involved in the defense mechanism against the invasion of foreign organisms. The basic organization of the oesophagus of P. misakiensis is similar to those of other ascidians. However, the presence of three folds is a characteristic of a solitary species, rather than of a colonial species. Although ascidians are chordate invertebrates, the organization of their oesophagus is not very complex, which might reflect their life style.