Are there efferent synapses in fish taste buds?

In fish, nerve fibers of taste buds are organized within the bud's nerve fiber plexus. It is located between the sensory epithelium consisting of light and dark elongated cells and the basal cells. It comprises the basal parts and processes of light and dark cells that intermingle with nerve fibers, which are the dendritic endings of the taste sensory neurons belonging to the cranial nerves VII, IX or X. Most of the synapses at the plexus are afferent; they have synaptic vesicles on the light (or dark) cells side, which is presynaptic. In contrast, the presumed efferent synapses may be rich in synaptic vesicles on the nerve fibers (presynaptic) side, whereas the cells (postsynaptic) side may contain a subsynaptic cistern; a flat compartment of the smooth endoplasmic reticulum. This structure is regarded as a prerequisite of a typical efferent synapse, as occurring in cochlear and vestibular hair cells. In fish taste buds, efferent synapses are rare and were found only in a few species that belong to different taxa. The significance of efferent synapses in fish taste buds is not well understood, because efferent connections between the gustatory nuclei of the medulla with taste buds are not yet proved.     

Gustatory neurons derived from epibranchial placodes are attracted to, and trophically supported by, taste bud-bearing endoderm in vitro

Taste buds are multicellular receptor organs innervated by the VIIth, IXth, and Xth cranial nerves. In most vertebrates, taste buds differentiate after nerve fibers have reached the lingual epithelium, suggesting that nerves induce taste buds. However, under experimental conditions, taste buds of amphibians develop independently of innervation. Thus, rather than being induced by nerves, the developing taste periphery likely regulates ingrowing nerve fibers. To test this idea, we devised a culture approach using axolotl embryos. Gustatory neurons were generated from cultured epibranchial placodes, and when cultured alone, axon outgrowth was random over 4 days, a time period coincident with axon growth to the periphery in vivo. In contrast, cocultures of placodal neurons with oropharyngeal endoderm (OPE), the normal taste bud-containing target for these neurons, resulted in neurite growth toward the target tissue. Unexpectedly, placodal neurons also grew toward flank ectoderm (FE), which these neurons do not encounter in vivo. To compare further the impact of OPE and FE explants on gustatory neurons, cocultures were extended and examined at 6, 8, and 10 days, when, in vivo, placodal fibers have innervated the epithelium but prior to taste bud formation, when taste buds have differentiated and are innervated, and when the mouth has opened and larvae have begun to feed, respectively. The behavior of placodal axons with respect to target type did not differ between OPE and FE cocultures at 6 days. However, by 8 days, differences in axonal outgrowth were observed with respect to target type, and these differences were enhanced by 10 days in vitro. Most clearly, exuberant placodal fibers grew in 10-day OPE cocultures, and numerous neurites had invaded OPE explants by this time, whereas gustatory neurites were sparse in FE cocultures, and rarely approached and almost never contacted FE explants. Thus, embryonic endoderm destined to give rise to taste buds specifically attracts its innervation early in development, as placodal neurons send out axons. Later, when gustatory axons synapse with differentiated taste buds in vivo, the OPE provides trophic support for cultured gustatory neurons.     

Expression patterns of HNK-1 carbohydrate and serotonin in sea urchin, amphioxus, and lamprey, with reference to the possible evolutionary origin of the neural crest

We examined deuterostome invertebrates, the sea urchin and amphioxus, and an extant primitive vertebrate, the lamprey, for the presence of structures expressing the HNK-1 carbohydrate and serotonin. In sea urchin embryos and larvae, HNK-1 positive cells were localized in the ciliary bands and in their precursor ectoderm. Serotonergic cells were exclusively observed in the apical organs. In juvenile amphioxus, primary sensory neurons in the dorsal nerve cords were HNK-1 immunoreactive. The juvenile amphioxus nerve cords contained anti-serotonin immunoreactive nerve fibers that seem to be the Rohde axons extending from amphioxus interneurons, the Rohde cells. In lamprey embryos, migrating neural crest cells and primary sensory neurons, including Rohon-Beard cells, expressed the HNK-1 carbohydrate. Lamprey larvae (ammocoetes) contained cell aggregates expressing both the HNK-1 carbohydrate and serotonin in the pronephros and in the regions adjacent to the gut epithelium. Some of these cell aggregates were present in the anti-serotonin positive visceral motor nerve net. Motor neurons and Müller fibers were serotonergic in ammocoetes. Comparison of the expression patterns of HNK-1 carbohydrate among sea urchins, amphioxus and lampreys seem to suggest the possible evolutionary origin of the neural crest, that is, ciliary bands in dipleurula-type ancestors evolved into primary sensory neurons in chordate ancestors, as inferred from Garstang's auricularia hypothesis, and the neural crest originated from the primary sensory neurons.     

Building sensory receptors on the tongue

Neurotrophins, neurotrophin receptors and sensory neurons are required for the development of lingual sense organs. For example, neurotrophin 3 sustains lingual somatosensory neurons. In the traditional view, sensory axons will terminate where neurotrophin expression is most pronounced. Yet, lingual somatosensory axons characteristically terminate in each filiform papilla and in each somatosensory prominence within a cluster of cells expressing the p75 neurotrophin receptor (p75NTR), rather than terminating among the adjacent cells that secrete neurotrophin 3. The p75NTR on special specialized clusters of epithelial cells may promote axonal arborization in vivo since its over-expression by fibroblasts enhances neurite outgrowth from overlying somatosensory neurons in vitro. Two classical observations have implicated gustatory neurons in the development and maintenance of mammalian taste buds—the early arrival times of embryonic innervation and the loss of taste buds after their denervation in adults. In the modern era more than a dozen experimental studies have used early denervation or neurotrophin gene mutations to evaluate mammalian gustatory organ development. Necessary for taste organ development, brain-derived neurotrophic factor sustains developing gustatory neurons. The cardinal conclusion is readily summarized: taste buds in the palate and tongue are induced by innervation. Taste buds are unstable: the death and birth of taste receptor cells relentlessly remodels synaptic connections. As receptor cells turn over, the sensory code for taste quality is probably stabilized by selective synapse formation between each type of gustatory axon and its matching taste receptor cell. We anticipate important new discoveries of molecular interactions among the epithelium, the underlying mesenchyme and gustatory innervation that build the gustatory papillae, their specialized epithelial cells, and the resulting taste buds.     

Phagocytic Cells in the Taste Buds of Rat Circumvallate Papillae after Denervation

Phagocytic cells in the taste buds of rat circumvallate papillaeafter the sectioning of bilateral glossopharyngeal nerves wereexamined by electron microscopy and immunohistochemistry. Electronmicrographs taken 1 day after denervation revealed that flat-shapedcells were present just beneath the taste buds and that theircellular processes extended toward the debris from the degeneratingtaste buds. At 2–6 days after denervation, long and thinprocesses of the flat cells surrounded the debris and appearedto have taken them up into the cytoplasm as small vesicles.Evidence for phagocytosis by the flat cells was seen up to 9days after denervation and again at 24 and 40 days, in correlationto the degeneration and regeneration of the taste buds. Pre-embeddingimmunohistochemistry using anti-vimentin antibody showed thatflat cells strongly reacted with vimentin. Light microscopicimmunohistochemistry using anti-macrophage antibodies (ED1,ED2) showed that throughout the post-operative days macrophageswere not present underneath or within the taste buds. Most ofthe ED2-immunoreactive resident macrophages were located inthe deep layer of connective tissue, and a few were found inthe nerve bundle. ED1-immunoreactive cells were seen in theduct cells of von Ebner's glands and a few were in the trenchwall of circumvallate papillae; however, they were also immunoreactivefor anti-OX62 antibody, which recognizes dendritic cells. Theresults indicate that the phagocytic cells of the taste budsare fibroblasts, not macrophages. Moreover, resident macrophagesparticipate in phagocytosis of degenerated nerves together withSchwann cells. Chem. Senses. 21: 467–476, 1996.     

Epidermal receptor development and sensory pathways in vitally stained amphioxus (Branchiostoma floridae)

Chloromethyl (CM) DiI was applied to the exterior of living embryos, larvae, and metamorphic juveniles of amphioxus. This fluorescent dye is taken up preferentially (but not highly selectively) by epidermal receptors and often stains sensory axons to their full extent. Type I primary receptors in the epidermis first become morphologically detectable along the rostrocaudal axis of the 2.5 day larva when their epidermal perikarya extend unbranched axons to the nerve cord. These axons run posteriorly or anteriorly within the nerve cord, depending on whether their perikarya are located, respectively, rostral or caudal to the most posterior pharyngeal slit. In later larvae, axons of type I receptors are organized into a dorsal and a subdorsal sensory tract on either side of the nerve cord. In the epidermis of metamorphic juveniles, CM-DiI also stains type II receptors (which are axonless, secondary receptors) and ventral pit cells (which may not be receptors). It is probable, but not yet conclusively demonstrated, that peripheral neurites from Retzius bipolar cells (primary intramedullary sensory neurones) synapse with type II secondary epidermal receptors or ramify freely among the other epidermal cells. The discussion considers homologies among epidermal sensory receptors in chordates.     

Prion infection of oral and nasal mucosa

Centrifugal spread of the prion agent to peripheral tissues is postulated to occur by axonal transport along nerve fibers. This study investigated the distribution of the pathological isoform of the protein (PrP(Sc)) in the tongues and nasal cavities of hamsters following intracerebral inoculation of the HY strain of the transmissible mink encephalopathy (TME) agent. We report that PrP(Sc) deposition was found in the lamina propria, taste buds, and stratified squamous epithelium of fungiform papillae in the tongue, as well as in skeletal muscle cells. Using laser scanning confocal microscopy, PrP(Sc) was localized to nerve fibers in each of these structures in the tongue, neuroepithelial taste cells of the taste bud, and, possibly, epithelial cells. This PrP(Sc) distribution was consistent with a spread of HY TME agent along both somatosensory and gustatory cranial nerves to the tongue and suggests subsequent synaptic spread to taste cells and epithelial cells via peripheral synapses. In the nasal cavity, PrP(Sc) accumulation was found in the olfactory and vomeronasal epithelium, where its location was consistent with a distribution in cell bodies and apical dendrites of the sensory neurons. Prion spread to these sites is consistent with transport via the olfactory nerve fibers that descend from the olfactory bulb. Our data suggest that epithelial cells, neuroepithelial taste cells, or olfactory sensory neurons at chemosensory mucosal surfaces, which undergo normal turnover, infected with the prion agent could be shed and play a role in the horizontal transmission of animal prion diseases.     

Expression of amiloride-sensitive epithelial sodium channels in mouse taste cells after chorda tympani nerve crush

Our previous electrophysiological study demonstrated that amiloride-sensitive (AS) and -insensitive (AI) components of NaCl responses recovered differentially after the mouse chorda tympani (CT) was crushed. AI responses reappeared earlier (at 3 weeks after the nerve crush) than did AS ones (at 4 weeks). This and other results suggested that two salt-responsive systems were differentially and independently reformed after nerve crush. To investigate the molecular mechanisms of formation of the salt responsive systems, we examined expression patterns of three subunits (alpha, beta and gamma) of the amiloride-sensitive epithelial Na(+) channel (ENaC) in mouse taste cells after CT nerve crush by using in situ hybridization (ISH) analysis. The results showed that all three ENaC subunits, as well as alpha-gustducin, a marker of differentiated taste cells, were expressed in a subset of taste bud cells from an early stage (1-2 weeks) after nerve crush, although these taste buds were smaller and fewer in number than for control mice. At 3 weeks, the mean number of each ENaC subunit and alpha-gustducin mRNA-positive cells per taste bud reached the control level. Also, the size of taste buds became similar to those of the control mice at this time. Our previous electrophysiological study demonstrated that at 2 weeks no significant response of the nerve to chemical stimuli was observed. Thus ENaC subunits appear to be expressed prior to the reappearance of AI and AS neural responses after CT nerve crush. These results support the view that differentiation of taste cells into AS or AI cells is initiated prior to synapse formation.     

Expression of Mash1 in basal cells of rat circumvallate taste buds is dependent upon gustatory innervation

Mash1, a mammalian homologue of the Drosophila achaete-scute proneural gene complex, plays an essential role in differentiation of subsets of peripheral neurons. In this study, using RT-PCR and in situ RT-PCR, we investigated if Mash1 gene expression occurs in rat taste buds. Further, we examined dynamics of Mash1 expression in the process of degeneration and regeneration in denervated rat taste buds. In rat tongue epithelium, Mash1 gene expression is confined to circumvallate, foliate, and fungiform papilla epithelia that include taste buds. In taste buds, Mash1-expressing cells are round cells in the basal compartment. In contrast, the mature taste bud cells do not express the Mash1 gene. Denervation and regeneration experiments show that the expression of Mash1 requires gustatory innervation. We conclude that Mash1 is expressed in cells of the taste bud lineage, and that the expression of Mash1 in rat taste buds is dependent upon gustatory innervation.     

Development of anterior gustatory epithelia in the palate and tongue requires epidermal growth factor receptor.

We characterized the gustatory phenotypes of neonatal mice having null mutations for epidermal growth factor receptor (egfr(-/-)), brain-derived neurotrophic factor (bdnf(-/-)), or both. We counted the number and diameter of fungiform taste buds, the prevalence of poorly differentiated or missing taste cells, and the incidence of ectopic filiform-like spines, each as a function of postnatal age and anterior/posterior location. Egfr(-/-) mice and bdnf(-/-) mice had similar reductions in the total number of taste buds on the anterior portions of the tongue and palate. Nonetheless, there were significant differences in their gustatory phenotypes. EGFR deficiency selectively impaired the development of anterior gustatory epithelia in the mouth. Only bdnf(-/-) mice had numerous taste buds missing from the foliate, vallate, and posterior fungiform papillae. Only egfr(-/-) fungiform taste papillae had robust gustatory innervation, markedly reduced cytokeratin 8 expression in taste cells, and a high incidence of a filiform-like spine. Egfr/bdnf double-null mutant mice had a higher frequency of failed fungiform taste bud differentiation. In bdnf(-/-) mice taste cell development failed because of sparse gustatory innervation. In contrast, in young egfr(-/-) mice the abundance of axons innervating fungiform papillae and the normal numbers of geniculate ganglion neurons implicate gustatory epithelial defects rather than neural defects.     

Rat gustatory neurons in the geniculate ganglion express glutamate receptor subunits

Taste receptor cells are innervated by primary gustatory neurons that relay sensory information to the central nervous system. The transmitter(s) at synapses between taste receptor cells and primary afferent fibers is (are) not yet known. By analogy with other sensory organs, glutamate might a transmitter in taste buds. We examined the presence of AMPA and NMDA receptor subunits in rat gustatory primary neurons in the ganglion that innervates the anterior tongue (geniculate ganglion). AMPA and NMDA type subunits were immunohistochemically detected with antibodies against GluR1, GluR2, GluR2/3, GluR4 and NR1 subunits. Gustatory neurons were specifically identified by retrograde tracing with fluorogold from injections made into the anterior portion of the tongue. Most gustatory neurons in the geniculate ganglion were strongly immunoreactive for GluR2/3 (68%), GluR4 (78%) or NR1 (71%). GluR1 was seen in few cells (16%). We further examined if glutamate receptors were present in the peripheral terminals of primary gustatory neurons in taste buds. Many axonal varicosities in fungiform and vallate taste buds were immunoreactive for GluR2/3 but not for NR1. We conclude that gustatory neurons express glutamate receptors and that glutamate receptors of the AMPA type are likely targeted to synapses within taste buds.     

Immunohistochemical investigation of the nitrergic system in the taste organ of the frog,Rana esculenta

We have studied by immunocytochemistry, the taste discs of the frog, Rana esculenta, with the aim of providing morphological and neurochemical data on the nitrergic system and of assessing the eventual presence of intrinsic neurons associated with the gustatory organs. In taste discs, antibodies against neuronal nitric oxide synthase (nNOS) revealed a positive immunoreaction in the taste receptor cell bodies and processes. The basal cells were also stained. All the fungiform papillae contained intragemmal nerve fibers showing nNOS immunoreactivity; these fiber were mainly located in the basal plexus. Immunoreactive nerve fibers were also visible at the periphery of the papilla-contacting ciliate cells, which form a ring around the taste disc. In conclusion, the findings obtained in this study suggest that the occurrence of nNOS-immunoreactivity in basal cells, taste cells and nerves might reflect a role for nitric oxide in taste mechanisms of Amphibia. The results may also sustain the physiological implication of NO as a molecule involved in the local target function of maintaining the taste bud mucosal integrity and in regulating the blood flow to the epithelium.     

Choline acetyltransferase immunoreactivity of putative intrinsic primary afferent neurons in the rat ileum

The colocalisation of choline acetyltransferase (ChAT) with markers of putative intrinsic primary afferent neurons was determined in whole-mount preparations of the myenteric and submucosal plexuses of the rat ileum. In the myenteric plexus, prepared for the simultaneous localisation of ChAT and nitric oxide synthase (NOS), all nerve cells were immunoreactive (IR) for ChAT or NOS, but seldom for both; only 1.6 +/- 1.8% of ChAT-IR neurons displayed NOS-IR and, conversely, 2.8 +/- 3.3% of NOS-IR neurons were ChAT-IR. In preparations double labelled for NOS-IR and the general nerve cell marker, neuron-specific enolase, 24% of all nerve cells were immunoreactive for NOS, indicating that about 75% of all nerve cells have ChAT-IR. All putative intrinsic primary afferent neurons in the myenteric plexus, identified by immunoreactivity for the neurokinin 1 (NK1) receptor and the neurokinin 3 (NK3) receptor, were ChAT-IR. Conversely, of the ChAT-IR nerve cells, about 45% were putative intrinsic primary afferent neurons (this represents 34% of all nerve cells). The cell bodies of putative intrinsic primary afferent neurons had Dogiel type II morphology and were also immunoreactive for calbindin. All, or nearly all, nerve cells in the submucosal plexus were immunoreactive for ChAT. About 46% of all submucosal nerve cells were immunoreactive for both neuropeptide Y (NPY) and calbindin; 91.8 +/- 10.5% of NPY/calbindin cells were also ChAT-IR and 99.1 +/- 0.7% were NK3 receptor-IR. Of the nerve cells with immunoreactivity for ChAT, 44.3 +/- 3.8% were NPY-IR, indicating that about 55% of submucosal nerve cells had ChAT but not NPY-IR. Only small proportions of the ChAT-IR, non-NPY, nerve cells had NK3 receptor or calbindin-IR. It is concluded that about 45% of submucosal nerve cells are ChAT/calbindin/NPY/VIP/NK3 receptor-IR and are likely to be secretomotor neurons. Most of the remaining submucosal nerve cells are immunoreactive for ChAT, but their functions were not deduced. They may include the cell bodies of intrinsic primary afferent neurons.     

Genetic tracing of the neural pathway for bitter taste in t2r5-WGA transgenic mice

To visualize the neural pathways originating from bitter taste receptor cells (TRCs), we generated transgenic mice expressing the transneuronal tracer wheat germ agglutinin (WGA) under the control of the mouse T2R5 gene promoter/enhancer (t2r5-WGA mice). WGA mRNA was specifically expressed in bitter TRCs. The WGA protein was detected in bitter TRCs and nerve processes in taste buds, but not in sweet, umami, or sour TRCs. The WGA protein was transferred to a subset of sensory neurons in the geniculate and nodose/petrosal ganglia. These results suggest that bitter TRCs, which are devoid of synaptic structures, are innervated by gustatory neurons and that bitter sensory information is directly transmitted to specific gustatory neurons. The t2r5-WGA mice provide a useful tool for identifying gustatory relay neurons in the peripheral sensory ganglia responsible for aversive sensations.     

Early dietary sodium restriction disrupts the peripheral anatomical development of the gustatory system

Dietary sodium restriction has profound effects on the development of peripheral taste function and central taste system anatomy. This study examined whether early dietary sodium restriction also affects innervation of taste buds. The number of geniculate ganglion cells that innervate single fungiform taste buds were quantified for the midregion of the tongue in two groups of rats: those fed either a low-sodium diet and those fed a sodium replete diet (control rats) from early prenatal development through adulthood. The same mean number of ganglion cells in developmentally sodium-restricted and control adult rats innervated taste buds on the midregion of the tongue. However, the characteristic relationship of the larger the taste bud, the more neurons that innervate it did not develop in sodium-restricted rats. The failure to form such a relationship in experimental rats was likely due to a substantially smaller mean taste bud volume than controls and probably not to changes in innervation. Further experiments demonstrated that the altered association between number of innervating neurons and taste bud size in restricted rats was reversible. Feeding developmentally sodium-restricted rats a sodium replete diet at adulthood resulted in an increase in taste bud size. Accordingly, the high correlation between taste bud volume and innervation was established in sodium-replete rats. Findings from the current study reveal that early dietary manipulations influence neuron-target interactions; however, the effects of dietary sodium restriction on peripheral gustatory anatomy can be completely restored, even in adult animals.     

Prospective protochordate homologs of vertebrate midbrain and MHB, with some thoughts on MHB origins

The MHB (midbrain-hindbrain boundary) is a key organizing center in the vertebrate brain characterized by highly conserved patterns of gene expression. The evidence for an MHB homolog in protochordates is equivocal, the "neck" region immediately caudal to the sensory vesicle in ascidian larvae being the best accepted candidate. It is argued here that similarities in expression patterns between the MHB and the ascidian neck region are more likely due to the latter being the principal source of neurons in the adult brain, and hence where all the genes involved in patterning the latter will necessarily be expressed. The contrast with amphioxus is exemplified by pax2/5/8, expressed in the neck region in ascidian larvae, but more caudally, along much of the nerve cord in amphioxus. The zone of expression in each case corresponds with that part of the nerve cord ultimately responsible for innervating the adult body, which suggests the spatially restricted MHB-like expression pattern in ascidians is secondarily reduced from a condition more like that in amphioxus. Patterns resembling those of the vertebrate MHB are nevertheless found elsewhere among metazoans. This suggests that, irrespective of its modern function, the MHB marks the site of an organizing center of considerable antiquity. Any explanation for how such a center became incorporated into the chordate brain must take account of the dorsoventral inversion chordates have experienced relative to other metazoans. Especially relevant here is a concept developed by Claus Nielsen, in which the brain is derived from a neural center located behind the ancestral mouth. While this is somewhat counterintuitive, it accords well with emerging molecular data.     

Sensory pathways in amphioxus larvae I. Constituent fibres of the rostral and anterodorsal nerves, their targets and evolutionary significance

Serial and interval electron micrograph series were used to examine the rostral and anterodorsal nerves of 12.5‐day‐old amphioxus larvae and trace selected fibres to their targets in the nerve cord. The nerves contain a variety of fibre types, including axons from at least two types of epithelial sensory cells and neurites derived from dorsal (Retzius) bipolar cells located within the cord. The rostral epithelial cells form basal synapses with a population of peripheral neurites that probably derive from the dorsal bipolar cells, though other sources are possible. Varicosities containing dense‐core vesicles occur at the tip of the rostrum, indicating the presence of efferent innervation at this site. Within the cord, some peripherally derived rostral afferents terminate at the level of the anterior cerebral vesicle, others synapse directly with both motoneurones and the notochord, but those in the largest bundle target the dendrites of the large paired neurones (LPNs) located in the primary motor centre. LPN dendrites also receive synapses from sensory fibres arriving via the anterodorsal nerves, from the anterior‐most of the dorsal bipolar cells, referred to here as tectal cells, and from a single fibre derived from the frontal eye. This convergence of multiple inputs accords with other evidence that the LPNs are key intermediaries in the sensorimotor pathway that activates the larval escape response. The rostral nerves are much larger at metamorphosis, but the ventral tracts that derive from them are still comparatively small. This is because the majority of rostral fibres are diverted into a late‐developing dorsal tract that travels within the cord to the front end of the dorsolateral neuropile, where most of its fibres disperse and form synapses. The positioning of the dorsal and ventral tracts strongly suggests homology with vertebrate olfactory and terminal nerves, respectively. This, and the question of whether the amphioxus central nervous system has anything comparable to the olfactory bulb, a telencephalic structure, is discussed.     

Chemosensory cells in the oral epithelium of Raja clavata (Chondrichthyes)

Examination by scanning and transmission electron microscopy (SEM and TEM) has found no actual taste buds in the mouth of Raja clavata. Prominences of the epithelium on the roof and floor of the mouth, and on the oral valves, contain large numbers of innervated bipolar cells, not associated in the form of taste buds, with a cytology intimating that they have a chemosensory function. The apices of these sensory cells, each bearing a group of microvilli, protrude between the superficial epithelial cells. Neurite profiles are associated with the sensory cells; synaptic specializations are marked by a cluster of vesicles with inconspicuous dense cores and some densities on the cell membrane. Shrunken, electron-dense, cell profiles are interpreted as apoptotic. Shrunken sensory cell profiles are commoner than similar epithelial cells, especially in young individuals, indicating a relatively rapid turnover of sensory cells. The epithelium contains a variety of granulocytic leucocytes, some of which contain large phagosomes.