On the Polarization and Innervation of the Pars Inferior Sensory Epithelia of the Herring Labyrinth

The macula sacculi and the macula lagenae of the herring, Clupea harengus L., were examined by light microscopy, the macula lagenae is large compared to what is normal among non-ostariophysan fishes, the morphological polarization of the hair cells in the inferior maculae shows a pattern which is similar to that usually seen in teleost fishes. The fibres in the nerves supplying the macula sacculi and the macula lagenae were counted and their diameters measured. The ramulus saccularis is divided in two separate ramuli innervating populations of hair cells with different morphological polarization. The saccular rostral nerve trunk contains 1800–2300 fibres, with 1300–1800 fibres in the caudal nerve trunk. The lagenar nerve is composed of 2100–4000 fibres. The fibre diameters are 1–14 μm in all ramuli. Silver staining of the nerve axoplasm reveals a unique differentiation of the maculae, which can be divided into a central area surrounded by a peripheral part. The hair cells in the central area are innervated by thick nerve fibres (5–14 μm diameter) as well as a few thin nerve fibres (about 1 μm diameter), while the receptor cells in the peripheral area are exclusively innervated by thin fibres having diameters of 2 μm or less.     

SOME OBSERVATIONS ON THE FINE STRUCTURE OF THE LATERAL LINE ORGAN OF THE JAPANESE SEA EEL LYNCOZYMBA NYSTROMI

The fine structure of the lateral line organ of the Japanese sea eel Lyncozymba nystromi has been studied with the electron microscope. The sensory epithelium of the lateral line organ consists of a cluster of two major types of cells, the sensory hair cells and the supporting cells. The sensory cell is a slender element with a flat upper surface provided with sensory hairs, Two different types of synapses are distinguished on the basal surface of the receptor cell. The first type is an ending without vesicles and the second type is an ending with many vesicles. These are presumed to correspond to the afferent and the efferent innervations of the lateral line organ. The fine structure of the supporting cells and the morphological relationship between the supporting cells and the receptor cells were observed. The possible functions of the supporting cells are as follows: (a) mechanical and metabolic support for the receptor cell; (b) isolation of the individual receptor cell; (c) mucous secretion and probably cupula formation; (d) glial function for the intraepithelial nerve fibers. Both myelinated and unmyelinated fibers were found in the lateral line nerve. The mode of penetration of these fibers into the epithelium was observed.     

A study on the fine structure of the saccular macula of the gold fish

Summary The fine structure of the saccular macula of the gold fish has been studied by means of the electron microscope.The sensory epithelium of the macula consists of sensory cells and supporting cells. The surface of the sensory cell is studded with a group of sensory hairs consisting of one kino-cilium and 50–60 stereocilia. In the dorsal half of the macula, the kino-cilium is located at the dorsal end of the sensory hair group. In the ventral half of the macula, the kino-cilium is located at the ventral end of the sensory hair group. In the intermediary portion of the macula, the sensory cells with opposite polarities are situated side-by-side. The relation between the microphonic potential and the position of the kino-cilium has been discussed.Two types of nerve terminals are found situated on the basal surface of the receptor cells. The one contains no synaptic vesicle and the other contains a cluster of synaptic vesicles and a few cored vesicles. It is considered that the former corresponds to the afferent nerve terminal and the latter to the efferent one.This investigation was supported by NIH Grant NB-06052.The author is very grateful to Prof. Taro Furukawa, Osaka City University for his invaluable advice and discussion.     

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.     

Morphology of the macula neglecta in sharks of the genus Carcharhinus

Ears from several species of carcharhinid sharks were studied by gross dissection, light microscopy, transmission electron microscopy, and scanning electron microscopy. Structures along a possible sound transmission path to the ear are described, but main consideration is given to the structure of the macula neglecta. The macula neglecta is composed of two patches of sensory epithelium which line part of the posterior canal duct. In an adult shark the larger of these contains 224,000 sensory hair cells oriented so as to detect forces directed posteroventrolaterally in the duct. The smaller patch contains 43,000 hair cells oriented so as to detect oppositely directed forces. These receptor cells project through numerous small terminals to a total for both patches of 4,700 myelinated nerve fibers. Cytostructural variations throughout the hair cell population are also reported. Estimated acoustic properties of the tissues in this complex and the processing potential of the neural elements are interpreted as suggestive of auditory function. A mechanism based on the geometry of the receptor arrays is proposed to explain behaviorally observed instantaneous sound localization from the farfield. Evolution of the macula neglecta is reviewed, and evidence for homology of the macula neglecta and amphibian papilla is presented.     

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.     

Development of the inner ear of the brown trout (Salmo trutta fario): II. Cytodifferentiation and innervation of sensory cells

The study of the sensory organs of the trout labyrinth by means of electron microscopy show that hair cells differentiate gradually in these organs; all of them produce new cells over a long period. The course of cytodifferentiation follows a similar pattern in all organs. Afferent nerve fibers and terminals are found at approximately the same time that sensory cells are being differentiated; the efferent synapses appear latter in development. The maturation of the both types of synapses is described. © 1993 Wiley-Liss, Inc.     

Regeneration of the projection and synaptic connections of tympanic receptor fibers of Locusta migratoria (Orthoptera) after axotomy

The tergite nerve N6 of the first abdominal segment of the locust Locusta migratoria contains receptor fibers, from the tympanic organ, and hair sensilla as well as motoric axons. The nerve was axotomized in nymphal instars or adults, and the regeneration of nerve fibers was studied. The sensory fibers regrow and regenerate their projection pattern within the central nervous system. They recognize their specific neuropile areas even after entering the ganglion through different pathways. The receptor fibers of the tympanic organ reestablish synaptic connections to auditory interneurons, even though the physiological characteristics of the interneurons are not fully restored. This regenerative capability contrasts with the lack of regeneration of peripheral structures in locusts, but supports the described plasticity in the auditory system of monaural locusts (Lakes, Kalmring, and Engelhard, 1990). The motor fibers do not regenerate nerves innervating muscles of the body wall.     

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.     

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.     

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.     

Presynaptic terminals in hyaline cells of normal and overstimulated chick inner ears

Hyaline cells are non-sensory epithelial cells of the vibrating part of the basilar membrane of chicks; they receive an extensive efferent innervation. Although these anatomical features suggest roles in auditory transduction, very little is known about the function of these cells. One possible way to understand function is by lesion experiments. We used synapsin-specific antibodies to study changes that occur in the pattern of efferent innervation in hyaline cells after lesion of the sensory epithelium induced by acoustic overstimulation. We found only small changes in hyaline cells after such trauma. These included a small increase in size and a small decrease in density of nerve terminals on hyaline cells. This suggests that hyaline cells and their nerve terminals are less susceptible to acoustic trauma than hair cells. Using neurofilament-specific antibodies we found little or no trauma-induced change in the density of nerve fibres that cross the basilar papilla and reach the hyaline cell region. This finding suggested that trauma to the hair cells does not necessarily lead to changes in the efferent fibres that cross the papilla and extend into the hyaline cell region. Using the trauma and the morphological parameters studied here, it appears that a moderate lesion in the hair cell region in the avian inner ear does not influence the hyaline cells or their innervation.     

THE ULTRASTRUCTURE OF THE SENSORY HAIRS AND ASSOCIATED ORGANELLES OF THE COCHLEAR INNER HAIR CELL, WITH REFERENCE TO DIRECTIONAL SENSITIVITY

From the apical end of the inner hair cell of the organ of Corti in the guinea pig cochlea protrude four to five rows of stereocilia shaped in a pattern not unlike the wings of a bird. In the area devoid of cuticular substance facing toward the tunnel of Corti lies a consistently present centriole. The ultrastructure of this centriole is similar to that of the basal body of the kinocilium located in the periphery of the sensory hair bundles in the vestibular and lateral line organ sensory cells and to that of the centrioles of other cells. The physiological implications of the anatomical orientation of this centriole are discussed in terms of directional sensitivity.     

Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea

The adult mammalian cochlea receives dual afferent innervation: the inner sensory hair cells are innervated exclusively by type I spiral ganglion neurons (SGN), whereas the sensory outer hair cells are innervated by type II SGN. We have characterized the spatiotemporal reorganization of the dual afferent innervation pattern as it is established in the developing mouse cochlea. This reorganization occurs during the first postnatal week just before the onset of hearing. Our data reveal three distinct phases in the development of the afferent innervation of the organ of Corti: (1) neurite growth and extension of both classes of afferents to all hair cells (E18-P0); (2) neurite refinement, with formation of the outer spiral bundles innervating outer hair cells (P0-P3); (3) neurite retraction and synaptic pruning to eliminate type I SGN innervation of outer hair cells, while retaining their innervation of inner hair cells (P3-P6). The characterization of this developmental innervation pattern was made possible by the finding that tetramethylrhodamine-conjugated dextran (TMRD) specifically labeled type I SGN. Peripherin and choline-acetyltransferase immunofluorescence confirmed the type II and efferent innervation patterns, respectively, and verified the specificity of the type I SGN neurites labeled by TMRD. These findings define the precise spatiotemporal neurite reorganization of the two afferent nerve fiber populations in the cochlea, which is crucial for auditory neurotransmission. This reorganization also establishes the cochlea as a model system for studying CNS synapse development, plasticity and elimination.     

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     

A STUDY OF THE ORIENTATION OF THE SENSORY HAIRS OF THE RECEPTOR CELLS IN THE LATERAL LINE ORGAN OF FISH, WITH SPECIAL REFERENCE TO THE FUNCTION OF THE RECEPTORS

The morphology of the hair bundles on top of the receptor cells in the lateral line organ of the teleost fish Lota vulgaris is described. Each receptor cell shows a distinct morphological polarization. Two groups of receptor cells can be distingiushed, one consisting of cells polarized towards the head, the other consisting of cells polarized towards the tail. In the crista ampullaris all cells are polarized in the same direction. An hypothesis is proposed for the function of the receptor cells in the lateral line organ and the labyrinth based on a correlation of morphological and functional polarization.     

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.     

Further serial transmission electron microscopy studies of auditory hair cell innervation in lizards and in a snake

Auditory hair cells of three lizard and one snake species were studied by serial transmission electron microscopy (TEM) sections of two unidirectional hair cells (UHC) and two bidirectional hair cells (BHC) and by nonserial section montages of each entire papilla cut at 2-microns intervals across the papillar width. The unidirectional hair cell region of the agamid lizard, Acanthosaura crucigera, lacked efferent innervation. Another agamid lizard, Agama agama, studied by nonserial section only, also lacked efferent innervation to the UHC. Afferent innervation to both the UHC and BHC of Acanthosaura was primarily exclusive (each nerve fiber innervates only one hair cell), although an occasional nerve fiber innervated two hair cells. Both the UHC and the BHC of the anguid, Celestus costatus, were exclusively innervated. Both hair cell types of the varanid, Varanus exanthematicus, were nonexclusively innervated (all afferent nerve fibers innervate two or more hair cells). The auditory papilla of the colubrid snake, Elaphe obsoleta, has only one type of hair cell and each is nonexclusively innervated. The numbers of afferent and efferent nerve fibers and of afferent synapses are presented in tabular form.     

Efferent control of the electrical and mechanical properties of hair cells in the bullfrog's sacculus

Background

Hair cells in the auditory, vestibular, and lateral-line systems respond to mechanical stimulation and transmit information to afferent nerve fibers. The sensitivity of mechanoelectrical transduction is modulated by the efferent pathway, whose activity usually reduces the responsiveness of hair cells. The basis of this effect remains unknown.

Methodology and Principal Findings

We employed immunocytological, electrophysiological, and micromechanical approaches to characterize the anatomy of efferent innervation and the effect of efferent activity on the electrical and mechanical properties of hair cells in the bullfrog''s sacculus. We found that efferent fibers form extensive synaptic terminals on all macular and extramacular hair cells. Macular hair cells expressing the Ca²⁺-buffering protein calretinin contain half as many synaptic ribbons and are innervated by twice as many efferent terminals as calretinin-negative hair cells. Efferent activity elicits inhibitory postsynaptic potentials in hair cells and thus inhibits their electrical resonance. In hair cells that exhibit spiking activity, efferent stimulation suppresses the generation of action potentials. Finally, efferent activity triggers a displacement of the hair bundle''s resting position.

Conclusions and Significance

The hair cells of the bullfrog''s sacculus receive a rich efferent innervation with the heaviest projection to calretinin-containing cells. Stimulation of efferent axons desensitizes the hair cells and suppresses their spiking activity. Although efferent activation influences mechanoelectrical transduction, the mechanical effects on hair bundles are inconsistent.