Mapping developmental maturation of inner hair cell ribbon synapses in the apical mouse cochlea

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Abstract

Ribbon synapses of cochlear inner hair cells (IHCs) undergo molecular assembly and extensive functional and structural maturation before hearing onset. Here, we characterized the nanostructure of IHC synapses from late prenatal mouse embryo stages (embryonic days 14–18) into adulthood [postnatal day (P)48] using electron microscopy and tomography as well as optical nanoscopy of apical turn organs of Corti. We find that synaptic ribbon precursors arrive at presynaptic active zones (AZs) after afferent contacts have been established. These ribbon precursors contain the proteins RIBEYE and piccolino, tether synaptic vesicles and their delivery likely involves active, microtubule-based transport pathways. Synaptic contacts undergo a maturational transformation from multiple small to one single, large AZ. This maturation is characterized by the fusion of ribbon precursors with membrane-anchored ribbons that also appear to fuse with each other. Such fusion events are most frequently encountered around P12 and hence, coincide with hearing onset in mice. Thus, these events likely underlie the morphological and functional maturation of the AZ. Moreover, the postsynaptic densities appear to undergo a similar refinement alongside presynaptic maturation. Blockwise addition of ribbon material by fusion as found during AZ maturation might represent a general mechanism for modulating ribbon size.

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Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates.

Adam C Furman, Sharon G Kujawa, M. Liberman (2013)

Acoustic overexposure can cause a permanent loss of auditory nerve fibers without destroying cochlear sensory cells, despite complete recovery of cochlear thresholds (Kujawa and Liberman 2009), as measured by gross neural potentials such as the auditory brainstem response (ABR). To address this nominal paradox, we recorded responses from single auditory nerve fibers in guinea pigs exposed to this type of neuropathic noise (4- to 8-kHz octave band at 106 dB SPL for 2 h). Two weeks postexposure, ABR thresholds had recovered to normal, while suprathreshold ABR amplitudes were reduced. Both thresholds and amplitudes of distortion-product otoacoustic emissions fully recovered, suggesting recovery of hair cell function. Loss of up to 30% of auditory-nerve synapses on inner hair cells was confirmed by confocal analysis of the cochlear sensory epithelium immunostained for pre- and postsynaptic markers. In single fiber recordings, at 2 wk postexposure, frequency tuning, dynamic range, postonset adaptation, first-spike latency and its variance, and other basic properties of auditory nerve response were all completely normal in the remaining fibers. The only physiological abnormality was a change in population statistics suggesting a selective loss of fibers with low- and medium-spontaneous rates. Selective loss of these high-threshold fibers would explain how ABR thresholds can recover despite such significant noise-induced neuropathy. A selective loss of high-threshold fibers may contribute to the problems of hearing in noisy environments that characterize the aging auditory system.

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Hair cell synaptic ribbons are essential for synchronous auditory signalling.

Rémy Pujol, Alexander Egner, Tobias Moser … (2005)

Hearing relies on faithful synaptic transmission at the ribbon synapse of cochlear inner hair cells (IHCs). At present, the function of presynaptic ribbons at these synapses is still largely unknown. Here we show that anchoring of IHC ribbons is impaired in mouse mutants for the presynaptic scaffolding protein Bassoon. The lack of active-zone-anchored synaptic ribbons reduced the presynaptic readily releasable vesicle pool, and impaired synchronous auditory signalling as revealed by recordings of exocytic IHC capacitance changes and sound-evoked activation of spiral ganglion neurons. Both exocytosis of the hair cell releasable vesicle pool and the number of synchronously activated spiral ganglion neurons co-varied with the number of anchored ribbons during development. Interestingly, ribbon-deficient IHCs were still capable of sustained exocytosis with normal Ca2+-dependence. Endocytic membrane retrieval was intact, but an accumulation of tubular and cisternal membrane profiles was observed in ribbon-deficient IHCs. We conclude that ribbon-dependent synchronous release of multiple vesicles at the hair cell afferent synapse is essential for normal hearing.

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Response properties of single auditory nerve fibers in the mouse.

D A Taberner, M. Liberman (2004)

The availability of transgenic and mutant lines makes the mouse a valuable model for study of the inner ear, and a powerful window into cochlear function can be obtained by recordings from single auditory nerve (AN) fibers. This study provides the first systematic description of spontaneous and sound-evoked discharge properties of AN fibers in mouse, specifically in CBA/CaJ and C57BL/6 strains, both commonly used in auditory research. Response properties of 196 AN fibers from CBA/CaJ and 58 from C57BL/6 were analyzed, including spontaneous rates (SR), tuning curves, rate versus level functions, dynamic range, response adaptation, phase-locking, and the relation between SR and these response properties. The only significant interstrain difference was the elevation of high-frequency thresholds in C57BL/6. In general, mouse AN fibers showed similar responses to other mammals: sharpness of tuning increased with characteristic frequency, which ranged from 2.5 to 70 kHz; SRs ranged from 0 to 120 sp/s, and fibers with low SR (<1 sp/s) had higher thresholds, and wider dynamic ranges than fibers with high SR. Dynamic ranges for mouse high-SR fibers were smaller (<20 dB) than those seen in other mammals. Phase-locking was seen for tone frequencies <4 kHz. Maximum synchronization indices were lower than those in cat but similar to those found in guinea pig.