Novel afferent terminal structure in the crista ampullaris of the goldfish,Carassius auratus

Lanford, Pamela J.; Popper, Arthur N.

doi:10.1002/(sici)1096-9861(19960318)366:4<572::aid-cne2>3.0.co;2-1

Cited by 24 publications

(4 citation statements)

References 26 publications

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“…By contrast, we found no clear homology of zebrafish inner ear hair cells with mammalian Type I and Type II hair cells. The lack of molecular signatures corresponding to Type I hair cells is consistent with previous reports that one of their major features, calyx synapses, are absent from macular organs in fishes ( Lysakowski and Goldberg, 2004 , but see Lanford and Popper, 1996 for evidence of calyx synapses in goldfish cristae). These findings suggest that the diversification of inner ear hair cells into Type I and Type II cells may have largely emerged after the evolutionary split of ray-finned fishes from the lineage leading to mammals.…”

Section: Discussionsupporting

confidence: 89%

“…The striola is characterized by hair cells with taller ciliary bundles and encompasses a line of polarity reversal where hair cells change their stereocilia orientation ( Figure 1E ). Whereas distinct Type I and Type II hair cells, and in particular the calyx synapses typical of Type I cells, have not been identified in the maculae of fishes, afferent innervation with some calyx-like properties has been reported in goldfish cristae ( Lanford and Popper, 1996 ). Spatial heterogeneity in the maculae, including those of zebrafish, has also been previously noted ( Chang et al, 1992 ; Platt, 1993 ; Collin et al, 2000 ; Liu et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

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Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Shi

Beaulieu

Saunders

et al. 2023

eLife

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A major cause of human deafness and vestibular dysfunction is permanent loss of the mechanosensory hair cells of the inner ear. In non-mammalian vertebrates such as zebrafish, regeneration of missing hair cells can occur throughout life. While a comparative approach has the potential to reveal the basis of such differential regenerative ability, the degree to which the inner ears of fish and mammals share common hair cells and supporting cell types remains unresolved. Here we perform single-cell RNA sequencing of the zebrafish inner ear at embryonic through adult stages to catalog the diversity of hair cells and non-sensory supporting cells. We identify a putative progenitor population for hair cells and supporting cells, as well as distinct hair and supporting cell types in the maculae versus cristae. The hair cell and supporting cell types differ from those described for the lateral line system, a distributed mechanosensory organ in zebrafish in which most studies of hair cell regeneration have been conducted. In the maculae, we identify two subtypes of hair cells that share gene expression with mammalian striolar or extrastriolar hair cells. In situ hybridization reveals that these hair cell subtypes occupy distinct spatial domains within the three macular organs, the utricle, saccule, and lagena, consistent with the reported distinct electrophysiological properties of hair cells within these domains. These findings suggest that primitive specialization of spatially distinct striolar and extrastriolar hair cells likely arose in the last common ancestor of fish and mammals. The similarities of inner ear cell type composition between fish and mammals validate zebrafish as a relevant model for understanding inner ear-specific hair cell function and regeneration.

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Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Shi

Beaulieu

Saunders

et al. 2023

eLife

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“…1 ). However, calyces vary in their shape in different regions of amniote vestibular epithelia ( 30 ), and shorter “proto-calyces” are reported to exist in fish and amphibians ( 4 , 44 – 47 ). To address the effects of calyx geometry on the two components (

and

) of NQT, we studied both the steady-state condition and the step response ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Nonquantal transmission at the vestibular hair cell–calyx synapse: K _LV currents modulate fast electrical and slow K ⁺ potentials

Govindaraju

Quraishi

Lysakowski

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Vestibular hair cells transmit information about head position and motion across synapses to primary afferent neurons. At some of these synapses, the afferent neuron envelopes the hair cell, forming an enlarged synaptic terminal called a calyx. The vestibular hair cell–calyx synapse supports a mysterious form of electrical transmission that does not involve gap junctions, termed nonquantal transmission (NQT). The NQT mechanism is thought to involve the flow of ions from the presynaptic hair cell to the postsynaptic calyx through low-voltage-activated channels driven by changes in cleft [K + ] as K + exits the hair cell. However, this hypothesis has not been tested with a quantitative model and the possible role of an electrical potential in the cleft has remained speculative. Here, we present a computational model that captures experimental observations of NQT and identifies features that support the existence of an electrical potential ( ϕ ) in the synaptic cleft. We show that changes in cleft ϕ reduce transmission latency and illustrate the relative contributions of both cleft [K + ] and ϕ to the gain and phase of NQT. We further demonstrate that the magnitude and speed of NQT depend on calyx morphology and that increasing calyx height reduces action potential latency in the calyx afferent. These predictions are consistent with the idea that the calyx evolved to enhance NQT and speed up vestibular signals that drive neural circuits controlling gaze, balance, and orientation.

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“…Extrastriolar hair cells are often Type II hair cells, which are cylindrical in shape and have bouton afferents, although some Type I cells are also found in the periphery ( Fernandez and Goldberg, 1976 ; Baird and Lewis, 1986 ; Songer and Eatock, 2013 ). Fish do not have morphologically distinct Type I hair cells as seen in amniotes, although enlarged quasi-calyx afferent endings has been observed in goldfish cristae ( Lanford and Popper, 1996 ). Thus, zebrafish inner ear afferents are often described as Type II-like in their morphology ( Liu et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Vestibular physiology and function in zebrafish

Baeza-Loya

Raible

2023

Front. Cell Dev. Biol.

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The vestibular system of the inner ear provides information about head motion and spatial orientation relative to gravity to ensure gaze stability, balance, and postural control. Zebrafish, like humans, have five sensory patches per ear that serve as peripheral vestibular organs, with the addition of the lagena and macula neglecta. The zebrafish inner ear can be easily studied due to its accessible location, the transparent tissue of larval fish, and the early development of vestibular behaviors. Thus, zebrafish are an excellent model for studying the development, physiology, and function of the vestibular system. Recent work has made great strides to elucidate vestibular neural circuitry in fish, tracing sensory transmission from receptors in the periphery to central computational circuits driving vestibular reflexes. Here we highlight recent work that illuminates the functional organization of vestibular sensory epithelia, innervating first-order afferent neurons, and second-order neuronal targets in the hindbrain. Using a combination of genetic, anatomical, electrophysiological, and optical techniques, these studies have probed the roles of vestibular sensory signals in fish gaze, postural, and swimming behaviors. We discuss remaining questions in vestibular development and organization that are tractable in the zebrafish model.

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Novel afferent terminal structure in the crista ampullaris of the goldfish,Carassius auratus

Cited by 24 publications

References 26 publications

Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Nonquantal transmission at the vestibular hair cell–calyx synapse: K _LV currents modulate fast electrical and slow K ⁺ potentials

Vestibular physiology and function in zebrafish

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Novel afferent terminal structure in the crista ampullaris of the goldfish,Carassius auratus

Cited by 24 publications

References 26 publications

Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes

Nonquantal transmission at the vestibular hair cell–calyx synapse: K LV currents modulate fast electrical and slow K + potentials

Vestibular physiology and function in zebrafish

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Product

Resources

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Nonquantal transmission at the vestibular hair cell–calyx synapse: K _LV currents modulate fast electrical and slow K ⁺ potentials