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Adult. A Myelinated and unmyelinated nerve (n) fibers are found within the sensory epithelium. B: An afferent synaptic complex with a presynaptic dense body (d) surrounded by clear vesicles in the sensory cell. A post-synaptic density (arrowheads) is found on the a&ent (a) fiber. C: The efferent synaptic complex consists of clear membrane-bound vesicles in the efferent (e) fiber and a postsynaptic density (arrowheads) in the sensory cell (s). D: Gap junctions (arrowheads) found between unmyelinated nerve fibers extending within the adult sensory epithelium.
Source publication
The development of the sensory epithelium of the saccular macula of Opsanus tau was studied with transmission electron microscopy. In the 10–12 somite embryo all cells of the newly formed otocyst are morphologically undefined, having an apically placed cilium with an underlying basal body and parabasal body. Junctional complexes are characterized p...
Contexts in source publication
Context 1
... the sensory epithelium, have a round, light-staining nucleus and a lightly stained cytoplasm with adjacent mitochon- dria. The cell is enveloped by a Schwann cell and its myelin sheath. Nerve processes ex- tending from the ganglion cell body are also wrapped in myelin. Myelinated and unmy- elinated fibers are found within the sensory epithelium ( Fig. 4A). Fiber diameters range from 0.5 pm to 4.2 pm. Small-diameter fibers are found throughout the whole epithelium, whereas large-diameter fibers are primarily found within the central ...
Context 2
... similar to that found in the crista ampullares and utricular mac- ula of 0. tau (Sans and Highstein, '84). M e r - ent synapses consist of a dense body surrounded by 40-50-nm clear, membrane bound vesicles in the sensory cell. The post- synaptic density lies on the afferent fiber ( adjacent to a postsynaptic density on the sen- sory cell (Fig. 4 0 . Other nerve junctions in- clude gap junctions between unmyelinated nerve fibers ( Fig. ...
Context 3
... and Highstein, '84). M e r - ent synapses consist of a dense body surrounded by 40-50-nm clear, membrane bound vesicles in the sensory cell. The post- synaptic density lies on the afferent fiber ( adjacent to a postsynaptic density on the sen- sory cell (Fig. 4 0 . Other nerve junctions in- clude gap junctions between unmyelinated nerve fibers ( Fig. ...
Citations
... Indeed, much of what we know about fish hearing comes from in-depth work on one or a few species such as Fay's goldfish work, studies of hearing and acoustic behavior of various toadfish species (e.g., Winn, 1972;Fine, 1978;Sokolowski and Popper, 1988;Bass and Marchaterre, 1989), and investigations of hearing in Atlantic cod (Gadus morhua) by Anthony Hawkins, Olav Sand, and their collaborators (reviewed in Hawkins, 2022). ...
I have been studying fish hearing since 1966. Over that time, my interests have evolved from basic mechanisms of hearing to “translational fish bioacoustics” where I help apply basic science to the protection of fishes from potential harm arising from anthropogenic sources. Yet, I am still most interested in basic science questions. Thus, this paper focuses on basic questions on fish hearing and shares my personal view of some of the interesting and important questions I think need to be asked about fish hearing by future investigators. Accordingly, I am not focusing on what has been learned, but, rather, I focus on the questions raised by what we have learned. Moreover, my focus is comparative—there are more than 34 000 extant fish species—and we know little about hearing in any one species. Indeed, most of our knowledge comes from about 100 species! Therefore, considering the immense importance of fishes, it is my contention that we need to know a great deal more about the sense that gives fishes rapid and highly directional information, often at a great distance, about the world around them.
... The aim of the present study is to describe the structure of the utricle in the adult oyster toadfish, Opsanus tau, as a model vertebrate species. As noted by Sokolowski and Popper (1988) the vestibular epithelium of adult Opsanus is not an oddity, but is similar in both gross and fine structure to that of many other fishes except the herring (Popper & Platt, 1979). The toadfish is noted for its survivability in harsh environments, such as extended exposure to cold climate or even stasis, its longevity (>40 years), its low food demands, and this vertebrate species' neural response to altered gravity that likely mimics that of man (Boyle et al., 2001). ...
The utricle provides the vestibular reflex pathways with the sensory codes of inertial acceleration of self motion and head orientation with respect to gravity to control balance and equilibrium. Here we present an anatomical description of this structure in the adult oyster toadfish, and establish a morphological basis for interpretation of subsequent functional studies. Light, scanning and transmission electron microscopy techniques were applied to visualize the sensory epithelium at varying levels of detail, its neural innervation and its synaptic organization. Scanning electron microscopy was used to visualize otolith mass and morphological polarization patterns of hair cells. Afferent nerve fibers were visualized following labeling with biocytin, and light microscope images were used to make three-dimensional (3-D) reconstructions of individual labeled afferents to identify dendritic morphology with respect to epithelial location. Transmission electron micrographs were compiled to create a serial 3-D reconstruction of a labeled afferent over a segment of its dendritic field and to examine the cell-afferent synaptic contacts. Major observations are: a well-defined striola, medial and lateral extra-striolar regions with a zonal organization of hair bundles; prominent lacinia projecting laterally; dependence of hair cell density on macular location; narrow afferent dendritic fields that follow the hair bundle polarization; synaptic specializations issued by afferents are typically directed towards a limited number of 7-13 hair cells, but larger dendritic fields in the medial extra-striola can be associated with > 20 hair cells also; and hair cell synaptic bodies can be confined to only an individual afferent or can synapse upon several afferents. This article is protected by copyright. All rights reserved.
... According to Sokolowski and Popper (1988), utricle is the endorgan that develops first in O. tau. If this is the case in H. didactylus, it is probably the reason for having a larger size at the posthatch and vocal fry stages. ...
... The fine structure of the midshipman saccule is comparable to that of the closely related oyster toadfish (Sokolowski & Popper, 1988) and ...
... The membrane specializations between afferent processes we describe have only, to our knowledge, previously been reported in oyster toadfish, where it is suggested that they are gap junctions (Sokolowski & Popper, 1988). The distances we observed between afferent membranes in the present study, 8-12 nm, is similar to the distances between membranes at support cell gap junctions, 5-10 nm, which are found in numerous vertebrates (Forge et al., 2003;Hama, 1980). ...
Dopamine (DA) is a conserved modulator of vertebrate neural circuitry, yet our knowledge of its role in peripheral auditory processing is limited to mammals. The present study combines immunohistochemistry, neural tract tracing and electron microscopy to investigate the origin and synaptic characteristics of DA fibers innervating the inner ear and the hindbrain auditory efferent nucleus in the plainfin midshipman, a vocal fish that relies upon the detection of mate calls for reproductive success. We identify a DA cell group in the diencephalon as a common source for innervation of both the hindbrain auditory efferent nucleus and saccule, the main hearing endorgan of the inner ear. We show that DA terminals in the saccule contain vesicles but transmitter release appears paracrine in nature, due to the apparent lack of synaptic contacts. In contrast, in the hindbrain, DA terminals form traditional synaptic contacts with auditory efferent neuronal cell bodies and dendrites, as well as unlabeled axon terminals, which, in turn, form inhibitory-like synapses on auditory efferent somata. Our results suggest a distinct functional role for brain-derived DA in the direct and indirect modulation of the peripheral auditory system of a vocal non-mammalian vertebrate. This article is protected by copyright. All rights reserved.
... In the inner ear, Cx30 occurs between supporting cells in the cochlear hair cell epithelium; mice lacking Cx30 show severe hearing loss [65]. There is evidence for gap junctions between supporting cells of the SE and possibly between hair cells and supporting cells in toadfish from the same family as midshipman [66]. BK channels, as noted earlier, are more abundant in the SE of reproductive midshipman, playing a prominent role in the sensitivity of SE hair cells to the full 100-400 Hz spectral range of their vocalizations [12]. ...
Background
Successful animal communication depends on a receiver’s ability to detect a sender’s signal. Exemplars of adaptive sender-receiver coupling include acoustic communication, often important in the context of seasonal reproduction. During the reproductive summer season, both male and female midshipman fish (Porichthys notatus) exhibit similar increases in the steroid-dependent frequency sensitivity of the saccule, the main auditory division of the inner ear. This form of auditory plasticity enhances detection of the higher frequency components of the multi-harmonic, long-duration advertisement calls produced repetitively by males during summer nights of peak vocal and spawning activity. The molecular basis of this seasonal auditory plasticity has not been fully resolved. Here, we utilize an unbiased transcriptomic RNA sequencing approach to identify differentially expressed transcripts within the saccule’s hair cell epithelium of reproductive summer and non-reproductive winter fish.
Results
We assembled 74,027 unique transcripts from our saccular epithelial sequence reads. Of these, 6.4 % and 3.0 % were upregulated in the reproductive and non-reproductive saccular epithelium, respectively. Gene ontology (GO) term enrichment analyses of the differentially expressed transcripts showed that the reproductive saccular epithelium was transcriptionally, translationally, and metabolically more active than the non-reproductive epithelium. Furthermore, the expression of a specific suite of candidate genes, including ion channels and components of steroid-signaling pathways, was upregulated in the reproductive compared to the non-reproductive saccular epithelium. We found reported auditory functions for 14 candidate genes upregulated in the reproductive midshipman saccular epithelium, 8 of which are enriched in mouse hair cells, validating their hair cell-specific functions across vertebrates.
Conclusions
We identified a suite of differentially expressed genes belonging to neurotransmission and steroid-signaling pathways, consistent with previous work showing the importance of these characters in regulating hair cell auditory sensitivity in midshipman fish and, more broadly, vertebrates. The results were also consistent with auditory hair cells being generally more physiologically active when animals are in a reproductive state, a time of enhanced sensory-motor coupling between the auditory periphery and the upper harmonics of vocalizations. Together with several new candidate genes, our results identify discrete patterns of gene expression linked to frequency- and steroid-dependent plasticity of hair cell auditory sensitivity.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1940-3) contains supplementary material, which is available to authorized users.
... Although the inner ear of the zebrafish does not contain a specialized hearing organ to manage hearing and balance, many genetic mechanisms of inner ear development and function are similar to those of other vertebrate species (Haddon and Lewis, 1996;Haffter et al., 1996;Whitfield et al., 2002). The zebrafish and the closely related goldfish (Carassius auratus) have three otic endorgans, the saccule, lagena, and utricle, which primarily mediate auditory and vestibular function (Sokolowski and Popper, 1988;Lanford et al., 2000;Kwak et al., 2006). The nascent otic vesicle contains two sensory epithelia corresponding to the utricular (anterior) and saccular (posterior) maculae (Kwak et al., 2006;Stooke-Vaughan et al., 2012). ...
The intercellular gap junction channels formed by connexins (CXs) are important for recycling potassium ions in the inner ear. CXs are encoded by a family of the CX gene, such as GJB2, and the mechanism leading to mutant connexin-associated diseases, including hearing loss, remains to be elucidated. In this study, using bioinformatics, we found that two zebrafish cx genes, cx27.5 and cx30.3, are likely homologous to human and mouse GJB2. During embryogenesis, zebrafish cx27.5 was rarely expressed at 1.5-3 hours post-fertilization (hpf), but a relatively high level of cx27.5 expression was detected from 6-96 hpf. However, zebrafish cx30.3 transcripts were hardly detected until 9 hpf. The temporal experiment was conducted in whole larvae. Both cx27.5 and cx30.3 transcripts were revealed significantly in the inner ear by reverse transcription polymerase chain reaction (RT-PCR) and whole-mount in situ hybridization (WISH). In the HeLa cell model, we found that zebrafish Cx27.5 was distributed intracellularly in the cytoplasm, whereas Cx30.3 was localized in the plasma membrane of HeLa cells stably expressing Cx proteins. The expression pattern of zebrafish Cx30.3 in HeLa cells was more similar to that of cells expressing human CX26 than Cx27.5. In addition, we found that Cx30.3 was localized in the cell membrane of hair cells within the inner ear by immunohistochemistry (IHC), suggesting that zebrafish cx30.3 might play an essential role in the development of the inner ear, in the same manner as human GJB2. We then performed morpholino knockdown studies in zebrafish embryos to elucidate the physiological functions of Cx30.3. The zebrafish cx30.3 morphants exhibited wild-type-like and heart edema phenotypes with smaller inner ears at 72 hpf. Based on these results, we suggest that the zebrafish Cx30.3 and mammalian CX26 may play alike roles in the inner ear. Thus, zebrafish can potentially serve as a model for studying hearing loss disorders that result from human CX26 mutations.
... A somewhat different correlation may also be possible. Although there are no embryonic studies of development of the ear in any gadiform species, studies on several other species including the oyster toadfish Opsanus tau show that the utricle is the first end organ to develop (Sokolowski & Popper 1988). If this is the case in hake, it is possible that the change in ecology and behavior of this species is delayed until the saccule is of sufficient size to detect sounds that may be involved in prey capture, and this occurs once the saccule is larger than the utricle. ...
Qualitative and quantitative observations were made of the density and growth of the sensory epithelia, hair cell number, and otoliths of the 3 pairs of end organs (saccule, lagena, and utricle) of the inner ear of European hake Merluccius merluccius (35 to 100 mm length) caught in the northwestern Mediterranean Sea. This is the period in the hake's life-history during which the transition from pelagic to epibenthic forms (settlement period) occurs. The results demonstrate a quantitative inversion in the percentage of the sensory epithelia area and the number of hair cells between the saccule and utricle over this time period. This period is also coincident with the settlement period that takes place when most individuals are ca. 50 mm, at which time the fish become epibenthic. These quantitative changes in the ear could be related to ecological changes in mobility and feeding.
... Similarly, does epithelial development prohibit synapse establishment more apical on the cell than the top of the nucleus? Although our results do not directly address these questions, it is reasonable to suggest that the extensive junctional complexes (and particularly desmosomes) between sensory hair cells and surrounding support cells in adult fishes just above the= nuclear layer (Sokolowski and Popper, 1988) might serve to limit the upper position of synapses. ...
Using transmission electron microscopy, we quantitatively analyzed the afferent and efferent synapses on 67 sensory hair cells along the saccular epithelium of the oscar (Astronotus ocellatus), a cichild fish with a non-specialized ear. The synaptic profile (number of afferent and efferent synapses per cell) varied considerably among cells. The number of synapses per hair cell ranged from three to 24, and all but six of the 67 hair cells had both afferent and efferent synapses. Statistical analysis showed that the synaptic profiles did not significantly vary anywhere on the saccular epithelium except at the edges. There, hair cells had significantly fewer efferent synapses than hair cells in other epithelial regions. This statistical variation in efferent synapse distribution in different epithelial regions corresponds with the lengths of ciliary bundles in these regions. The synapses on hair cells showed a regional specificity in position. In all cells synapses were never located more apically than the top of the nucleus. On hair cells towards the periphery, the most apical synapse on the hair cells tended to be afferent. On more centrally located cells, the most apical synapse was efferent in 92% of the cells.
Introduction A more extensive version of this paper was initially submitted for publication in a scientific journal in 1989. At the time, ethograms were becoming unfashionable and no longer suitable as subjects for stand-alone publications. Rather, they were viewed simply as tools to be used with other forms of behavioral research. As we were focused on new academic and curatorial responsibilities, we never got around to resubmitting it elsewhere.
Introduction A more extensive version of this paper was initially submitted for publication in a scientific journal in 1989. At the time, ethograms were becoming unfashionable and no longer suitable as subjects for stand-alone publications. Rather, they were viewed simply as tools to be used with other forms of behavioral research. As we were focused on new academic and curatorial responsibilities, we never got around to resubmitting it elsewhere.
