Persistence of vestibular function in the absence of glutamatergic transmission from hair cells

Quantal synaptic transmission in vestibular endorgans is glutamatergic. Here, we investigated the vestibular phenotype of deaf Vglut3^−/− (Slc17a8^−/−) mice from the cellular to behavioral levels. In Vglut3^−/− mice, quantal synaptic transmission in utricular calyces was reduced in rate and amplitude by > 95%. In vivo recordings of spontaneous activity in the vestibular nerve revealed no significant effect of VGLUT3 deletion on afferent rate and regularity, suggesting a divergent underlying mechanism compared to the silent Vglut3^−/− auditory nerve. In behavioral studies, Vglut3^−/− mice did not exhibit considerable sensorimotor or balance deficits. Type-II vestibular hair cells (VHCs) in Vglut3^+/+ mice were strongly immunoreactive for VGLUT3, while type-I VHCs showed weak immunoreactivity. Collectively, these data support the view that non-quantal transmission is the predominant mode of neurotransmission between type-I VHCs and vestibular calyceal afferent neurons. We propose that non-quantal transmission is sufficient to support vestibular nerve physiology and behavioral function in Vglut3^−/− mice.