Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat

In the preceding article (McCue and Guinan, 1994) we described a class of vestibular primary afferent fibers in the cat that responds vigorously to sounds at moderately high sound levels. Like their cochlear homologs, vestibular afferents and their associated hair cells receive efferent projections from brainstem neurons. In this report, we explore efferent influences on the background activity and tone-burst responses of the acoustically responsive vestibular afferents. Shock-burst stimulation of efferents excited acoustically responsive vestibular afferents; no inhibition was seen. A fast excitatory component built up within 100-200 msec of shock-burst onset and decayed with a similar time course at the end of each shock burst. During repeated 400 msec shock bursts at 1.5 sec intervals, a slow excitatory component grew over 20-40 sec and then decayed, even though the shock bursts continued. Efferent stimulation excited acoustically responsive vestibular afferents without appreciably changing an afferent's sound threshold or its average sound-evoked response. This evidence supports the hypothesis that excitation is due to efferent synapses on afferent fibers rather than on hair cells. Efferent stimulation enhanced the within-cycle modulation of afferent discharges evoked by a tone; that is, it increased the "AC gain." No appreciable change was noted in the degree of phase locking to low-frequency tones as measured by the synchronization index. Little or no improvement in the bidirectionality (linearity) of transduction was seen. Vestibular afferent responses to tones normally had one peak per cycle; however, during efferent stimulation, two peaks per cycle were sometimes seen. We hypothesize that this is caused by two driving components acting at different sound phases with the components differentially affected by efferent activity. We discuss the relationship of our findings to efferent influences on acoustic responses in cochlear afferent fibers. The acoustically responsive vestibular afferents provide a mammalian model for studying purely excitatory efferent effects in a hair cell system.