Ultrastructural differences among afferent synapses on cochlear hair cells: Correlations with spontaneous discharge rate

Abstract

The major class of cochlear afferent fibers, the type-I or radial-fiber (RF) population, has been subdivided into three functional groups according to spontaneous discharge rate (SR): those with low SR have the highest acoustic thresholds, high SR fibers have the lowest thresholds and medium SR fibers are of intermediate sensitivity (Liberman [1978] J. Acoust. Soc. Amer. 63:442-455). Existing evidence from intracellular labeling studies at the light microscopic level (Liberman [1982a] Science 216:1239-1241) suggests that a single cochlear inner hair cell makes synaptic contact with representatives of all three functional groups; however, low and medium SR fibers are spatially segregated from high SR fibers around the hair cell circumference, and low and medium SR fibers are smaller in caliber than those with high SR. The present study extends to the ultrastructural level the structure-function correlations available via intracellular labeling. Analysis is based on serial section reconstruction of the synaptic contacts between 11 radial fibers of known SR and their target hair cells. Results suggest systematic differences in synaptic ultrastructure among fibers of the three SR groups: with decreasing SR, the size and complexity of the synaptic body (a presynaptic specialization characteristic of the peripheral afferent synapses in all hair cell systems and some other peripheral receptors) tend to increase, as does the associated number of synaptic vesicles. The possible functional significance of these trends is discussed in the context of other known structural and functional differences among the three SR groups.

Olivocochlear Innervation Maintains the Normal Modiolar-Pillar and Habenular-Cuticular Gradients in Cochlear Synaptic Morphology

“…Intracellular labeling has also suggested a relation between SR and the size of the presynaptic ribbon: large ribbons were found at low SR synapses and small ribbons at high SR synapses (Merchan-Perez and Liberman 1996). In zebrafish lateral line hair cells, ribbon size is controlled by negative feedback from Ca ++ entry through presynaptic, voltage-gated Ca ++ channels (Sheets et al 2012).…”

Primary innervation of the avian and mammalian cochlear nucleus

“…High-SR fibers (>18 spikes/s) have thick peripheral processes that tend to contact the "pillar" side of the inner hair cell, whereas low-SR fibers (<18 spikes/s) have thin peripheral processes that tend to contact the modiolar side of the hair cell [98,111]. Furthermore, there is SR segregation within the spiral ganglion.…”

“…They ramify within the small cell cap, a region of small cells that lie beneath the granule cell domain. Light microscopic, drawing tube reconstruction exhibit different innervation characteristics with the IHCs [99,111], give rise to greater collateral branching in the AVCN [51], emit collaterals that preferentially innervate the small cell cap [100,177], and manifest striking specializations in the large axosomatic endings, the endbulbs of Held [185] and their synapses [178].…”

Mechanisms contributing to synaptic Ca 2+ signals and their heterogeneity in hair cells

“…Differential efferent control of SGN activity (17) seems conceptually obvious. There are also indications for differences in structure (18) and function (19) among active zones of an IHC; however, little is known about the underlying mechanism. Here, we used time-resolved confocal imaging of the fluorescence of low-affinity Ca 2ϩ indicators together with pharmacological manipulations and modeling to characterize synaptic Ca 2ϩ microdomains in IHCs of hearing mice.…”