Sound-evoked activity in primary afferent neurons of a mammalian vestibular system

Abstract

Hypothesis: Some primary vestibular afferents in the cat respond to sound at moderately intense sound levels.

Background: In fish and amphibians, parts of the vestibular apparatus are involved in audition. The possibility was explored that the vestibular system in mammals is also acoustically responsive.

Methods: Microelectrodes were used to record from single afferent fibers in the inferior vestibular nerve of the cat; some acoustically responsive fibers were labeled intracellularly with biocytin.

Results: Vestibular afferents with regular spontaneous activity were unresponsive to sound, whereas a sizable fraction of vestibular afferents with irregular activity were acoustically responsive. Labeling experiments demonstrated that acoustically responsive afferents innervate the saccule, have cell bodies in Scarpa's ganglion, and project to central regions both inside and outside the traditional boundaries of the vestibular nuclei. Acoustically responsive vestibular afferents responded to sound with shorter latencies than cochlear afferents but had higher thresholds (> 90 dB sound pressure level) and responded only in the range 0.1-3.0 kHz. In contrast to cochlear afferents, efferent stimulation excited background activity and proportionately increased sound-evoked responses in these vestibular afferents, that is, there was centrally mediated enhancement of gain (gain = spike-rate/motion).

Conclusions: The evolutionary conservation of a saccular auditory pathway in mammals suggests that it confers survival advantages. Recent evidence suggests that acoustically responsive saccular afferents trigger acoustic reflexes of the sternocleidomastoid muscle, and hence measurement of such reflexes may provide a relatively simple test for saccular dysfunction.