Acoustic Trauma Increases Ribbon Number and Size in Outer Hair Cells of the Mouse Cochlea

Megan B Wood,Paul Albert Fuchs,Mohamed Lehar,Nathaniel Nowak,Keira Mull,Adam Goldring

doi:10.1007/s10162-020-00777-w

Megan B Wood, Paul Albert Fuchs + Show 4 more

Open Access

https://doi.org/10.1007/s10162-020-00777-w

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Abstract

Outer hair cells (OHCs) in the mouse cochlea are contacted by up to three type II afferent boutons. On average, only half of these are postsynaptic to presynaptic ribbons. Mice of both sexes were subjected to acoustic trauma that produced a threshold shift of 44.2 ± 9.1 dB 7 days after exposure. Ribbon synapses of OHCs were quantified in post-trauma and littermate controls using immunolabeling of CtBP2. Visualization with virtual reality was used to determine 3-D cytoplasmic localization of CtBP2 puncta to the synaptic pole of OHCs. Acoustic trauma was associated with a statistically significant increase in the number of synaptic ribbons per OHC. Serial section TEM was carried out on similarly treated mice. This also showed a significant increase in the number of ribbons in post-trauma OHCs, as well as a significant increase in ribbon volume compared to ribbons in control OHCs. An increase in OHC ribbon synapses after acoustic trauma is a novel observation that has implications for OHC:type II afferent signaling. A mathematical model showed that the observed increase in OHC ribbons considered alone could produce a significant increase in action potentials among type II afferent neurons during strong acoustic stimulation.

Highlights

Type II cochlear afferents are uncommon, smallcaliber, unmyelinated neurons that project to the brainstem cochlear nucleus (Brown et al 1988)
To test the effect of acoustic trauma on outer hair cells (OHCs) synapses, 6-week-old C57BL/6J mice were exposed to threshold-shift inducing noise (110 dB for 2 h)
Ribbon synapses were counted in inner hair cells (IHCs) to determine if this trauma produced the pattern of synaptopathy reported previously (Fernandez et al 2020)

Summary

Introduction

Type II cochlear afferents are uncommon, smallcaliber, unmyelinated neurons that project to the brainstem cochlear nucleus (Brown et al 1988) Their peripheral arbors extend hundreds of microns along the organ of Corti to contact numerous outer hair cells (OHCs) (Spoendlin 1969; Smith 1975; Kiang et al 1982; Berglund and Ryugo 1987; Brown 1987; Simmons and Liberman 1988). Despite those many contacts, type II afferents respond poorly, if at all, to sound (Robertson 1984; Brown 1994; Robertson et al 1999; Flores et al 2015). Immunolocalization of synaptic proteins confirms this arrangement, adding the intriguing observation that, while all type II dendritic contacts

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