Afferent and efferent innervation of the cat cochlea: Quantitative analysis with light and electron microscopy

TLDR

The study aims to map the longitudinal and radial gradients of cochlear innervation in the cat. The authors reconstructed afferent and efferent terminals from serial ultrathin sections at six to eight cochlear locations spanning octave intervals of characteristic frequency, and compared ultrastructural data with synaptophysin‑stained light‑microscopic analysis. Afferent innervation of inner hair cells increases from 10 to 30 radial fibers per cell between 0.25 and 10 kHz, with branching confined to the apical region and synaptic‑body morphology varying with side; efferent terminals are abundant but specialized only apically, with more synapses on modiolar‑side fibers; outer hair cell afferent terminals rise from ~3 to 15 per cell from base to apex, while efferent terminals peak at 9 per cell between 6–24 kHz and decline from first to third row.

Abstract

The purpose of the present study was to describe the longitudinal and radial gradients of cochlear innervation in the cat. To this end, afferent and efferent terminals of both the inner (IHC) and outer hair cell (OHC) regions were reconstructed from serial ultrathin sections at six and eight cochlear locations, respectively, corresponding to roughly octave intervals of characteristic frequency (CF). Analysis of the afferent innervation of the IHCs showed 1) the number of radial fibers per IHC rises from 10 per IHC at the 0.25 kHz region to a maximum of 30 per IHC at the 10 kHz locus; 2) branching of radial fibers is essentially restricted to regions apical to the 1.0 kHz point; and 3) there are significant differences in synaptic-body morphology for synapses on different sides of the IHC, corresponding to known differences in afferent threshold and rate of spontaneous activity. With respect to efferent innervation in the IHC area, we found 1) that there were numerous vesicle-filled terminals contacting every IHC examined; however, those with obvious synaptic specialization were confined to the most apical regions; and 2) there were roughly the same numbers of efferent synapses per radial fiber at all cochlear locations; however, at each location, radial fibers contacting the modiolar side of the hair cell (corresponding to high-threshold afferents) showed significantly more efferent synapses than radial fibers contacting the pillar side. Analysis of the OHC afferent innervation showed 1) a clear rise in numbers of terminals per OHC from roughly 3 per cell in the base to 15 per cell in the apex, 2) no systematic differences in the numbers of terminals as a function of OHC row, and 3) that synaptic bodies at the OHC afferent synapse are common only apical to the 1.0 kHz locus. Counts of efferent terminals on OHCs revealed 1) maximal numbers (9 per OHC) between the 6 and 24 kHz regions and 2) striking decrease in terminal counts from first- to third-row OHCs. Ultrastructural data on efferent innervation were compared quantitatively with light-microscopic analysis of cochleas immunostained (with antibody to synaptophysin) to reveal all vesiculated terminals.