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

Abstract

Abstract 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.