Concurrent gradients of ribbon volume and AMPA-receptor patch volume in cochlear afferent synapses on gerbil inner hair cells

Zhang, Lichun; Engler, Sina; Koepcke, Lena; Steenken, Friederike; Köppl, Christine

doi:10.1016/j.heares.2018.03.028

Cited by 19 publications

(19 citation statements)

References 40 publications

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“…However, these differences are minor and similar to the differences reported in different studies in the same species. For example, a previous study investigating gerbils reported 57% modiolar ribbons (Zhang et al, 2018) compared to our observation of 50%. Thus, these differences could easily result from subtle differences in the methods of defining the spatial coordinates of ribbons relative to the hair cells, and, therefore, further significance to these differences is not attributed.…”

Section: Auditory Neurons and Their Contacts With The Hair Cells Icontrasting

confidence: 85%

“…When comparing the mean normalized volumes of modiolar versus pillar afferent ribbons, we observed statistically significant differences in mice, gerbils, and naked but not Damaraland mole rats. A difference Tables 1 and 5 in size in the same direction, relatively larger modiolar afferent ribbons, has been reported previously in cats (Merchan-Perez & Liberman, 1996), mice , and gerbils (Zhang et al, 2018). Furthermore, in cats, the type I afferent fibers with high thresholds and low spontaneous rates tended to associate with relatively larger ribbons on the modiolar side of the IHC whereas afferent fibers with low thresholds and high spontaneous rates tended to associate with relatively smaller ribbons on the pillar side of the IHC (Merchan-Perez & Liberman, 1996).…”

Section: Auditory Neurons and Their Contacts With The Hair Cells Isupporting

confidence: 84%

“…In cat, pillar‐modiolar differences in IHC afferent ribbon sizes correlate with pillar‐modiolar differences in afferent fiber thresholds (Merchan‐Perez & Liberman, ). Pillar‐modiolar differences in IHC afferent ribbon sizes have also been documented in mice (Liberman, Wang, & Liberman, ) and gerbils (Zhang, Engler, Koepcke, Steenken, & Koppl, ). To compare differences between the numbers and volumes of pillar and modiolar IHC afferent ribbons, we localized and quantified the volumes of ribbons (CTBP2 immunopunta) as described in Section 2.…”

Section: Resultsmentioning

confidence: 99%

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Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Barone

Douma

Reijntjes

et al. 2019

J of Comparative Neurology

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Compared to many other rodent species, naked mole rats (Heterocephalus glaber) have elevated auditory thresholds, poor frequency selectivity, and limited ability to localize sound. Because the cochlea is responsible for encoding and relaying auditory signals to the brain, we used immunofluorescence and quantitative image analysis to examine cochlear innervation in mature and developing naked mole rats compared to mice (Mus musculus), gerbils (Meriones unguiculatus), and Damaraland mole rats (Fukomys damarensis), another subterranean rodent. In comparison to mice and gerbils, we observed alterations in afferent and efferent innervation as well as their patterns of developmental refinement in naked and Damaraland mole rats. These alterations were, however, not always shared similarly between naked and Damaraland mole rats. Most conspicuously, in both naked and Damaraland mole rats, inner hair cell (IHC) afferent ribbon density was reduced, whereas outer hair cell afferent ribbon density was increased. Naked and Damaraland mole rats also showed reduced lateral and medial efferent terminal density. Developmentally, naked mole rats showed reduced and prolonged postnatal reorganization of afferent and efferent innervation. Damaraland mole rats showed no evidence of postnatal reorganization. Differences in cochlear innervation specifically between the two subterranean rodents and more broadly among rodents provides insight into the cochlear mechanisms that enhance frequency sensitivity and sound localization, maturation of the auditory system, and the evolutionary adaptations occurring in response to subterranean environments.

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Section: Auditory Neurons and Their Contacts With The Hair Cells Icontrasting

confidence: 85%

Section: Auditory Neurons and Their Contacts With The Hair Cells Isupporting

confidence: 84%

Section: Resultsmentioning

confidence: 99%

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Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Barone

Douma

Reijntjes

et al. 2019

J of Comparative Neurology

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“…Several mechanisms have been proposed to explain the different SGN firing patterns. Postsynaptic morphology shows different fiber caliber and mitochondrial content (6) as well as different amounts of AMPA receptors (7)(8)(9). The lateral olivocochlear system could provide differential efferent modulation (7,10).…”

mentioning

confidence: 99%

Intrinsic planar polarity mechanisms influence the position-dependent regulation of synapse properties in inner hair cells

Jean

Özçete

Tarchini

et al. 2019

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

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Encoding the wide range of audible sounds in the mammalian cochlea is collectively achieved by functionally diverse type I spiral ganglion neurons (SGNs) at each tonotopic position. The firing of each SGN is thought to be driven by an individual active zone (AZ) of a given inner hair cell (IHC). These AZs present distinct properties according to their position within the IHC, to some extent forming a gradient between the modiolar and the pillar IHC side. In this study, we investigated whether signaling involved in planar polarity at the apical surface can influence position-dependent AZ properties at the IHC base. Specifically, we tested the role of Gαi proteins and their binding partner LGN/Gpsm2 implicated in cytoskeleton polarization and hair cell (HC) orientation along the epithelial plane. Using high and superresolution immunofluorescence microscopy as well as patch-clamp combined with confocal Ca2+ imaging we analyzed IHCs in which Gαi signaling was blocked by Cre-induced expression of the pertussis toxin catalytic subunit (PTXa). PTXa-expressing IHCs exhibited larger CaV1.3 Ca2+-channel clusters and consequently greater Ca2+ influx at the whole-cell and single-synapse levels, which also showed a hyperpolarized shift of activation. Moreover, PTXa expression collapsed the modiolar–pillar gradients of ribbon size and maximal synaptic Ca2+ influx. Finally, genetic deletion of Gαi3 and LGN/Gpsm2 also disrupted the modiolar–pillar gradient of ribbon size. We propose a role for Gαi proteins and LGN in regulating the position-dependent AZ properties in IHCs and suggest that this signaling pathway contributes to setting up the diverse firing properties of SGNs.

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“…In the cat 6 , back-tracing experiments linked morphology to function and showed that low-SR SGNs have thinner radial fibers (peripheral neurites) with fewer mitochondria than high-SR. Low-SR SGNs preferentially innervate the modiolar (or neural) side of the IHC, where they face larger and more complex presynaptic AZs [6][7][8][9] . Larger and more complex AZs at the modiolar side of IHCs were also found in mouse [10][11][12] , guinea pig 13,14 , and gerbil 15 , suggesting some features of SGN morphology and synaptic connectivity may be shared across species. In the mouse, RNA sequencing of individual SGNs indicated three distinct subtypes [16][17][18] that were suggested to correspond to low, medium, and high-SR SGNs based on the spatial segregation of their IHC innervation.…”

Section: Introductionmentioning

confidence: 92%

A sensory cell diversifies its output by varying Ca²⁺influx-release coupling among presynaptic active zones for wide range intensity coding

Özçete¹,

Moser²

2020

Preprint

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The cochlea encodes sound intensities ranging over six orders of magnitude which is collectively achieved by functionally diverse spiral ganglion neurons (SGNs). However, the mechanisms enabling the SGNs to cover specific fractions of the audible intensity range remain elusive. Here we tested the hypothesis that intensity information, fully contained in the receptor potential of the presynaptic inner hair cell (IHC), is fractionated via heterogeneous synapses. We studied the transfer function of individual active zones (AZs) using dual-color Rhod-FF and iGluSnFR imaging of Ca 2+ and glutamate release. AZs differed in the voltage dependence of release: AZs residing at the IHCs' pillar (abneural) side activate at more hyperpolarized potentials and typically showed tight control of release by few Ca 2+ -channels. We conclude that heterogeneity of voltage dependence and release-site coupling of Ca 2+ -channels among the AZs varies synaptic transfer within individual IHCs and, thereby, likely contributes to the functional diversity of SGNs.

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Concurrent gradients of ribbon volume and AMPA-receptor patch volume in cochlear afferent synapses on gerbil inner hair cells

Cited by 19 publications

References 40 publications

Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Intrinsic planar polarity mechanisms influence the position-dependent regulation of synapse properties in inner hair cells

A sensory cell diversifies its output by varying Ca²⁺influx-release coupling among presynaptic active zones for wide range intensity coding

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Concurrent gradients of ribbon volume and AMPA-receptor patch volume in cochlear afferent synapses on gerbil inner hair cells

Cited by 19 publications

References 40 publications

Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Altered cochlear innervation in developing and mature naked and Damaraland mole rats

Intrinsic planar polarity mechanisms influence the position-dependent regulation of synapse properties in inner hair cells

A sensory cell diversifies its output by varying Ca2+influx-release coupling among presynaptic active zones for wide range intensity coding

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A sensory cell diversifies its output by varying Ca²⁺influx-release coupling among presynaptic active zones for wide range intensity coding