Afferent innervation of outer and inner hair cells is normal in neonatally de‐efferented cats

Abstract

It has been hypothesized that normal pruning of exuberant branching of afferent neurons in the developing cochlea is caused by the arrival of the olivocochlear efferent neurons and the resulting competition for synaptic sites on hair cells. This hypothesis was supported by a report that afferent innervation density on mature outer hair cells (OHCs) is elevated in animals deefferented at birth, before the olivocochlear system reaches the outer hair cell area (Pujol and Carlier [1982] Dev. Brain Res. 3:151-154). In the current study, this claim was evaluated quantitatively at the electron microscopic level in four cats that were de-efferented at birth and allowed to survive for 6-11 months. A semiserial section analysis of 156 OHCs from de-efferented and normal ears showed that, although de-efferentation essentially was complete in all four cases, the number and distribution of afferent terminals on OHCs was indistinguishable from normal, and the morphology of afferent synapses was normal in both the inner hair cell area and the OHC area. Thus, the postnatal presence of an efferent system is not required for the normal development of cochlear afferent innervation, and the synaptic competition hypothesis is not supported.

Cochlear Efferent Innervation Is Sparse in Humans and Decreases with Age

“…Activation of MOC terminals in mammals elevates cochlear thresholds by decreasing intracellular receptor potentials and thereby decreasing the reverse transduction of those electrical signals into mechanical motion, as effected by the motor protein prestin in OHC membranes (Fuchs and Lauer, 2019). As in other "low-frequency" mammals (Liberman and Gao, 1995;Liberman et al, 2000), the density of MOC terminals peaks in the upper basal turn, ϳ2-4 kHz in our youngest subjects (Fig. 5), suggesting that this sound-evoked negative feedback is most important for high-frequency stimuli.…”

“…In prior studies, we have compared several alternate approaches to the quantification of MOC innervation density (i.e., counting of tunnelcrossing fascicles or measuring their summed diameter; Liberman and Gao, 1995;Liberman et al, 2000), counting the average number of MOC terminals contacting each OHC (Liberman et al, 1990(Liberman et al, , 2014, or measuring the projected silhouette areas, either manually (Maison et al, 2003) or automatically (Yin et al, 2014). In prior work, we have shown (1) that the fascicle diameters in the tunnel are highly correlated with silhouette areas of terminals under the OHCs (Liberman and Gao, 1995), (2) that immunostained silhouettes are highly correlated with maximum terminal areas extracted from serial-section electron microscopy (Liberman et al, 1990), and (3) that terminal counts are highly correlated with silhouette areas (M. C. Liberman, unpublished observations).…”

Developmental segregation in the efferent projections to auditory hair cells in the gerbil

“…This interpretation was contested by studies showing that developing cochlear efferent nerve terminals often display ultrastructural features consistent with both afferent and efferent synapses in mature animals (Sobkowicz, 1992; Bruce et al, 2000), suggesting that the previous morphologic criteria used to differentiate synapses within the developing cochlea were not sufficiently reliable. Furthermore, the synaptic competition hypothesis has been directly challenged by the observation that removal of efferent projections during early postnatal development, through surgical sectioning of the olivocochlear pathway, does not lead to any significant differences in the number or distribution of OHC afferent terminals (Liberman et al, 2000). Our data suggest an alternative explanation for the results reported by Pujol and colleagues.…”

Axodendritic versus axosomatic cochlear efferent termination is determined by afferent type in a hierarchical logic of circuit formation

“…Because type II afferent collaterals are not observable in our hands until P10 (the earliest we can label them with anti-parvalbumin), and we cannot culture cochlea this late in development, we are unable to similarly confirm whether type II afferent innervation can occur in the absence of efferents. However, given that animals without efferents formed and maintained type II afferent innervation (58) (see Discussion below), it follows that these neurons must also be able to innervate the oc-IHCs in the absence of efferents.…”