Structure and Innervation of the Inner Ear Sensory Organs in an Otophysine Fish,the Upside–down Catfish (Synodontis nigriventrisDavid)

All the sensory epithelia of the inner ear in the upside–down catfish (Synodontis nigriventrisDavid) were examined by light microscopy. The morphology of the membranous labyrinth and the orientation of the hair cells is similar to what has been found in other otophysine fishes. The sensory cells are of variable size both inter– and intraepithelially; particularly the macula sacculi is equipped with heterogeneous receptors. Regional differences in the hair cell density are presented for all the otolith organs plus the papilla neglecta. Nerve stainings reveal regional differentiation. The central areas are innervated by stout and stubbly nerve endings intermingled with a few thin nerve fibres while the peripheral parts are reached exclusively by thin axons. In the anterior region of the macula sacculi are found unique cup–shaped axon terminations which surround the basal parts of a single or a few sensory cells. The number and diameter range of the myelinated nerve fibres as well as the hair cell/axon ratio are presented. Electron microscopy demonstrates the presence of unmyelinated axons in all inner ear nerve ramuli.     

A Qualitative and Quantitative Study of a Sensory Epithelium in the Inner Ear of a Fish (Colisa labiosa; Anabantidae)

The macula lagenae of the anabantide fish Colisa labiosa was studied with light and transmission electron microscopy. (1) The sensory area is naturally divided in a central area (A) surrounded by a peripheral part (B). (2) Generally the central hair cells are separated by supporting cells, while the peripheral hair cells are found in groups. The cells of a group are not separated by supporting cells. (3) Tubuli-like structures, hexagonal in cross section, are found in all cells. In peripheral hair cells the longitudinally oriented tubuli-like structures are aggregated in thick bundles. (4) Variation in shape, electron density, stereocilia arrangement and size of mitochondria was found in different hair cells. (5) The central hair cells contain large accumulations of presynaptic bodies (10–44). Contrarily, the peripheral hair cells contain only a few pre-synaptic bodies (1–3). (6) The central hair cells are innervated by thick afferent (6–15 μm) and fine presumed efferent (less than 1 μm nerve fibres, while the peripheral hair cells are innervated by thin (1–6 μm) afferent nerve fibres only.     

Hair Cell Polarization in the Flatfish Inner Ear

The hair cell polarization of the various sensory epithelia in the inner ear was examined in two species of flatfish, the Plaice (Pleuronectes platessa) and the Dab (Limanda limanda). The hair cells in the macula utriculi are polarized in the pattern usually seen for this macula in vertebrates. In the macula sacculi and macula lagenae the hair cell polarization is different from that hitherto described from bony fishes and other vertebrates. The polarization seen in these maculae in the flatfish explains their ability to sense movements in all directions, which is necessary if these sensory areas are the most important inner ear organs in the regulation of postural orientation.     

The ultrastructure and innervation of the ear of the gar, Lepisosteus osseus

The endorgans of the inner ear of the gar were examined using transmission and scanning electron microscopy as well as nerve staining. The ultrastructure of the sensory hair cells and supporting cells of the gar ear are similar to cells in other bony fishes, whereas there are significant differences between the gar and other bony fishes in the orientations patterns of the sensory hair cells on the saccular and lagenar sensory epithelia. The saccular sensory epithelium has two regions, a main region and a secondary region ventral to the main region. The ciliary bundles on the main region are divided into two groups, one oriented dorsally and the other ventrally. Furthermore, as a result of curvature of the saccular sensory epithelium, the dorsal and ventral ciliary bundles on the rostral portion of the epithelium are rotated ninety degrees and are thus oriented on the animal's rostro-caudal axis. Hair cells on the secondary region are generally oriented ventrally. The lagenar epithelium has three groups of sensory hair cells. The groups on the rostral and caudal ends of the macula are oriented dorsally, whereas the middle group is oriented ventrally. Hair cell orientations on the utricular epithelium and macula neglecta are similar to those in other bony fishes. Nerve fiber diameters can be divided into three size classes, 1-8 microns, 9-13 microns, and 14 microns or more, with the smallest size class containing the majority of fibers. The distribution of the various classes of fiber diameters is not the same in nerve branches to each of the end organs. Similarly, the ratio of hair cells to axons differs in each end organ. The highest hair cell to axon ratio is in the utricle (23:1) and the smallest is in the macula neglecta (7:1). The number of sensory hair cells far exceed the number of eighth nerve axons in all sensory epithelia.     

Comparative light and electron microscopic study of the auditory organs of two species of fishes (pisces): Hyphessobrycon simulans (Ostariophysi) and Poecilia reticulata (Acanthopterygii).

Hyphessobrycon simulans has a Weberian apparatus for transmission of sound energy to the auditory organ, whereas Poecilia reticulata does not. The fine structure of the auditory organs is identical in the two species. The better hearing - expressed by large bandwidth and high sensitivity - typical of the Ostariophysi - seems to be based exclusively on the presence of the Weberian apparatus. The sensory epithelium of the saccule and the lagena is made up of hair (sensory) cells and supporting cells. The vertically orientated macula sacculi is divided into a dorsal and a ventral cell area with oppositely arranged hair-cell kinocilia. The sagitta takes up the center of the saccule and shows only three small sites with connections to the otolithic membrane. Remarkably, the dorsal sensory cells are connected to the ventral part of the otolith, but the ventral cells are connected to the dorsal part. The macula of the lagena also comprises a dorsal and a ventral cell area with oppositely arranged hair cells. The sensory cells in all maculae are of type II. They exhibit a striking apical cell protrusion, the cuticular villus. It is partially fused with the kinocilium in the contact zones and joined to the otolithic membrane. The cuticular villus probably stabilizes the long kinocilia.     

Structure and Innervation of Inner Ear Sensory Epithelia in the European Eel (Anguilla anguilla L.)

Hair cell orientations of all inner ear sensory epithelia in glass eel, yellow eel and silver eel are presented. The patterns of hair cell orientation do not change with age. All sensory epithelia increase in area during growth of the eel. Examination of the hair cell population in macula utriculi show constant hair cell densities and increased hair cell population during development. Further, regional differences in hair cell densities and hair cell types are observed. The hair cells/axons ratio increases 3-fold from glass eel to silver eel stadium. Nerve stainings in silver eel reveal complex innervation patterns with large stubby fibres confined to restricted regions. Histograms of nerve fiber diameters show marked differences from glass eel to silver eel. Growth of sensory epithelia is discussed.     

On the Structure of the Avian Maculae

The maculae of the labyrinths of several avian species were examined. The striola of the macula utriculi and lagenae is tri-zonal, consisting of two zones of hair cells type I (HC I) located on each side of a middle zone of hair cells type II (HC II). An exception is the mute swan, in which the macula utriculi has a striola consisting of one broad zone of HC I. The macula sacculi is, in its central part, mainly consisting of HC I, and the striola does not have a tri-zonal structure. The hair cells in the macula utriculi are polarized with their kinociliar end oriented towards the striola, while in the macula sacculi and lagenae they are oriented away from this dividing line. A varying number, from 1 to 12, of HC I are enclosed within the same nerve chalice. The macula sacculi seems to contain chalices with slightly more HC I than the two other maculae do.     

The Number and Distribution of Calyceal Hair Cells in the Inner Ear Utricular Macula of Some Reptiles

The utricular macula in the inner ear was examined in two turtle, two lacertilian, two snake and one crocodilian species. The orientation of hair cells was found to be similar to the general pattern for this macula described previously from fish to mammals. The calyceal hair cells, characterized by their embracing afferent nerve endings, are distributed in a single belt running parallel with the anterior and lateral borders of the macula in the examined reptiles.
The number of hair cells in a large number of calyces was counted for some of the examined reptile species, and the total number of hair cells calculated in two specimens of a turtle, crocodile and snake utricular macula. In the turtle and snake maculae, the calyceal hair cells form about 10% of the total hair cell number, while the crocodiles, which were very young, only had 2% calyceal hair cells. The total number of hair cells was found to be much higher in the crocodiles than in the other reptiles examined. The presented data, as well as data from the literature of the avian and mammalian inner ear, indicate that the number of this very sensitive hair cell type in the utricular macula is independent of locomotion type.     

Dark hair cells in the inner ear of the rainbow trout. A study of the influence of different fixation methods

The occurrence of dark staining cells in different tissues has been suggested to be artefactual and caused during the fixation process. In inner ear sensory epithelia, dark hair cells (DHC) have been suggested to be apoptotic cells. We have examined whether dark cells represent dying cells or whether they are the results of fixation artefacts. The effects of buffer osmolarity and different fixation methods on the incidence of dark hair cells in the inner ear macula sacculi of the rainbow trout (Oncorhynchus mykiss) were investigated by light and electron microscopy. Glutaraldehyde in phosphate buffer with osmolarities of 0, 135, 225, 425, and 560 mosmol were used for fixation by immersion. For comparison, fixation by vascular perfusion as well as the effects of mechanical injury and delayed fixation were studied. DHC were found in all examined saccular maculae except for the delayed fixation protocol where almost all the sensory cells were lost. The number of DHC accounted for 2.5–12.9‰ of the sensory cells. Neither the buffer osmolarity nor the fixation method had significant effects on the frequencies of DHC. Mitotic cell division events were seen exclusively in the apical cell strata of the sensory epithelium. The DHC are suggested to be associated with apoptosis rather than fixation artefacts.     

Quantitative analyses of sex and size differences in the macula neglecta and ramus neglectus in the inner ear of the skate,Raja ocellata

Summary In Raja ocellata the macula neglecta is located in the posterior canal duct of the inner ear at the junction with the sacculus. The maximum length and width of a freeze-dried macula from a male skate of 61 cm width is 1035 m and 315 m respectively. Ultrastructural studies show that the hair cells of the macula are of two types. Orientation of hair cells is towards the periphery with a reverse direction of polarization in 5.0 to 6.5% of the cells. The axons of the associated nerve, the ramus neglectus, are myelinated, and include both efferent and afferent fibres.Electron-microscopic studies and quantitative analyses reveal significant sex differences in the macula neglecta and ramus neglectus. Hair cell and axon numbers, and total axon areas increase linearly with skate size, and are significantly different in males and females for any given representative size of skate, the females having the larger counts. Since the macula neglecta functions as a vibration detector of far-field localizations, the gender difference may be involved in the location of prey, or in mate detection. It is unknown whether such differences occur in any other vertebrate species.     

Scanning electron microscopic observations on the inner ear of the skate,Raja ocellata

The inner ear of the skate, Raja ocellata, was examined by scanning electron microscopy. The otolithic membranes have a gelatinous component and an endogenous class of otoconia. Cupulae are reticulate in form. The morphology and polarization of sensory cell hair bundles are described for the various regions of the labyrinth, and are compared with published observations on other species. In the otolithic maculae, the more centrally located receptor cells generally have longer sterecolia than the peripheral cells. The hair bundles of the lacinia are similar to those of the central portion of the sacculus and differed from those of the rest of the utricular macula. Hair bundles in the peripheral regions of all maculae and cristae are similar. The polarization pattern of the utriculus is similar to that of teleosts, while that of the lagena is less clearly dichotomized. The receptor cells of most of the sacculus are oriented in a bivertical direction, with cells in the anterior portion, and a few in the posterior region, being aligned longitudinally. The significance of morphology and polarization with respect to the functions of the otolithic organs is discussed. The relationship of cell processes of the ampullary receptors to the cupula is briefly considered.     

Structure of sensilla trichodea of female Aedes aegypti with comments on innervation of antennal sensilla

On each antenna of female Aedes aegypti four types of sensilla trichodea are distinguishable: long and short, pointed-tipped ones and blunt-tipped types I and II. All types are innervated by two neurones, except the short, pointed-tipped trichodea with which only one neurone is associated. Both pointed-tipped types have unbranched dendrites and relatively thicker hair walls perforated by fewer pores than the blunt-tipped types. The long, pointed-tipped trichodea are 50–60 μm in length and the short ones 20 μm. In both blunt-tipped types the dendrites divide and the hair walls are perforated by numerous pores. Blunt-tipped type I trichodea are 20–40 μm in length and taper somewhat whereas the type II hairs are 11–13 μm in length, do not taper appreciably, and have exceedingly thin walls. All types of sensilla trichodea are olfactory receptors and the blunt-tipped type I are known to respond to repellents.An investigation of the possibility of axon fusion in the flagellar nerve gave negative results.Each flagellar nerve is composed of an estimated 2058 neurones. A majority of these, namely 93%, are involved in the recognition and discrimination of olfactory cues. Approximately 65% of the neurones respond to repellents, 5% to mechanical stimuli, and 2% to heat transferred by convection.     

STRUCTURE OF THE MACULA UTRICULI WITH SPECIAL REFERENCE TO DIRECTIONAL INTERPLAY OF SENSORY RESPONSES AS REVEALED BY MORPHOLOGICAL POLARIZATION

The anatomy of the labyrinth and the structure of the macula utriculi of the teleost fish (burbot) Lota vulgaris was studied by dissection, phase contrast, and electron microscopy. The innervating nerve fibers end at the bottom of the sensory cells where two types of nerve endings are found, granulated and non-granulated. The ultrastructure and organization of the sensory hair bundles are described, and the finding that the receptor cells are morphologically polarized by the presence of an asymmetrically located kinocilium in the sensory hair bundle is discussed in terms of directional sensitivity. The pattern of orientation of the hair cells in the macula utriculi was determined, revealing a complicated morphological polarization of the sensory epithelium. The findings suggest that the interplay of sensory responses is intimately related to the directional sensitivity of the receptor cells as revealed by their morphological polarization. The problem of efferent innervation is discussed, and it is concluded that the positional information signaled by the nerve fibers innervating the vestibular organs comprises an intricate pattern of interacting afferent and efferent impulses     

Nerve-muscle networks in the accessory gland tubules of a male insect: Structural and physiological properties

The accessory gland tubules of the cockroach Leucophaea maderae, (F.) are innervated by the phallic nerves which arise from the terminal ganglion. Tubule preparations stained with methylene blue showed that a fine network of nerve fibres covers the entire surface of the tubule with putative nerve cells at various points. Muscle fibres of the tubules were arranged in an irregular lattice and appeared as flattened elipses approx 8–10 μm across and 1.5 μm in thickness. These muscles were monomyofibrillar with a poorly developed T-tubule system and a diffuse Z band. Innervation of the muscles showed abundant evidence of neurosecretomotor-type terminals. Clear evidence was also obtained for a multiterminal-type innervation. Accessory gland tubules had a basic wave-like pattern of motion in vitro which showed a wide variation in the time-course of each swing (1–50 s). A twisting and curling motion of the tubules was also recorded. Spontaneous junctional potentials were observed in accessory gland preparations isolated from the terminal ganglion. The duration for junction potential ranged between 30–140 ms. Action potentials recorded from muscles had a slower rise time and a longer duration (230–530 ms).     

Development of otolith receptors in Japanese quail

This study examined the morphological development of the otolith vestibular receptors in quail. Here, we describe epithelial growth, hair cell density, stereocilia polarization, and afferent nerve innervation during development. The otolith maculae epithelial areas increased exponentially throughout embryonic development reaching asymptotic values near posthatch day P7. Increases in hair cell density were dependent upon macular location; striolar hair cells developed first followed by hair cells in extrastriola regions. Stereocilia polarization was initiated early, with defining reversal zones forming at E8. Less than half of all immature hair cells observed had nonpolarized internal kinocilia with the remaining exhibiting planar polarity. Immunohistochemistry and neural tracing techniques were employed to examine the shape and location of the striolar regions. Initial innervation of the maculae was by small fibers with terminal growth cones at E6, followed by collateral branches with apparent bouton terminals at E8. Calyceal terminal formation began at E10; however, no mature calyces were observed until E12, when all fibers appeared to be dimorphs. Calyx afferents innervating only Type I hair cells did not develop until E14. Finally, the topographic organization of afferent macular innervation in the adult quail utricle was quantified. Calyx and dimorph afferents were primarily confined to the striolar regions, while bouton fibers were located in the extrastriola and Type II band. Calyx fibers were the least complex, followed by dimorph units. Bouton fibers had large innervation fields, with arborous branches and many terminal boutons. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70: 436–455, 2010     

Tactile-Evoked Response of Sensory Fibers in Buccal and Submandibular Regions of the Rat

Evoked neural responses to tactile stimulation were recorded electro-physiologically from the mechanoreceptive afferent fibers innervating the buccal and submandibular regions of Wistar rats anesthetized with sodium thiopental. Miniature probes 200 μm in diameter were used, and data analysis was performed on the mechanosensitivity of responses to tactile stimulation in the areas innervated by the mental, mylohyoid, auriculotemporal, and cervical nerves. Mechanosensitivity of each area showed a characteristic distribution of slowly adapting (SA), rapidly adapting (RA), C-fiber (CF), and hair follicle (HF) units in individual receptive fields. The density of the SA units was high in the areas innervated by the mylohyoid and auriculotemporal nerves. The CF units were concentrated in the small dome in the area of the mylohyoid nerve and the auriculotemporal nerve, as shown by a significant response to the dynamic features of stimulation. Estimation of the current needed for tactile acuity suggests an important role of the SA fibers in the areas innervated by the auriculotemporal, mylohyoid, and cervical nerves.     

The lateral line receptor array of cyprinids from different habitats

The lateral line system of teleost fishes consists of an array of superficial and canal neuromasts (CN). Number and distribution of neuromasts and the morphology of the lateral line canals vary across species. We investigated the morphology of the lateral line system in four diurnal European cyprinids, the limnophilic bitterling (Rhodeus sericeus), the indifferent gudgeon (Gobio gobio), and ide (Leuciscus idus), and the rheophilic minnow (Phoxinus phoxinus). All fish had lateral line canals on head and trunk. The total number of both, CN and superficial neuromasts (SN), was comparable in minnow and ide but was greater than in gudgeon and bitterling. The ratio of SNs to CNs for the head was comparable in minnow and bitterling but was greater in gudgeon and ide. The SN‐to‐CN ratio for the trunk was greatest in bitterling. Polarization of hair cells in CNs was in the direction of the canal. Polarization of hair cells in SNs depended on body area. In cephalic SNs, hair cell polarization was dorso‐ventral or rostro‐caudal. In trunk SNs, it was rostro‐caudal on lateral line scales and dorso‐ventral on other trunk scales. On the caudal fin, hair cell polarization was rostro‐caudal. The data show that, in the four species studied here, number, distribution, and orientation of CNs and SNs cannot be unequivocally related to habitat. J. Morphol. 275:357–370, 2014. © 2013 Wiley Periodicals, Inc.