Synaptic connections of the auditory nerve in cats: Relationship between endbulbs of held and spherical bushy cells

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Abstract
This report focuses on a class of large synaptic endings, the endbulbs of Held. These endings are located in the anteroventral cochlear nucleus and arise from the axons of type I spiral ganglion neurons. Axons were stained with horseradish peroxidase (HRP) using intracellular injections of single fibers or extracellular injections into the auditory nerve. Individual endbulbs or pairs of endbulbs that converged onto the same spherical bushy cell were examined with the aid of a light microscope and subjected to morphometric analyses. Endbulbs of fibers having low spontaneous discharge rates (SR, ≤ 18 spikes/sec) have a more complex shape than those of high SR fibers (> 18 s/s), a feature represented by systematic differences in endbulb silhouette perimeter without differences in endbulb silhouette area. Consequently, the ratio, silhouette area divided by silhouette perimeter, yields a “form factor” separating endbulbs of high SR from those of low SR. High SR fibers had ratios > 0.52 (mean = 0.63 ± 0.09), whereas low SR fibers had ratios <.52 (mean = 0.45 ± 0.06). Pairs of endbulbs with unknown physiological properties had similar form factor values, despite the wide range of values observed in the endbulb population. These data imply that endbulbs converging upon the cell body of a spherical bushy cell arise from fibers of the same SR group. Electron microscopic examination was conducted on the endbulb of one physiologically characterized and intracellularly stained auditory nerve fiber (CF = 1.4 kHz; SR = 55 s/s) and its unstained endbulb mate with the aid of serial ultrathin sections. In addition to the well-known axosomatic synapses, these endbulbs formed axodendritic synapses: 11.7% for the HRP-labeled endbulb and 13.3% for the unlabeled endbulb. The axodendritic synapses appear to occur on dendrites of nearby spherical bushy cells and may represent a mechanism whereby single endbulbs can disperse activity to multiple neurons in the cochlear nucleus. We propose that axosomatic synapses preserve fiber SR groupings, whereas axodendritic synapses may not.