Self-motion evokes precise spike timing in the primate vestibular system

The accurate representation of self-motion requires the efficient processing of sensory input by the vestibular system. Conventional wisdom is that vestibular information is exclusively transmitted through changes in firing rate, yet under this assumption vestibular neurons display relatively poor detection and information transmission. Here, we carry out an analysis of the system’s coding capabilities by recording neuronal responses to repeated presentations of naturalistic stimuli. We find that afferents with greater intrinsic variability reliably discriminate between different stimulus waveforms through differential patterns of precise (∼6 ms) spike timing, while those with minimal intrinsic variability do not. A simple mathematical model provides an explanation for this result. Postsynaptic central neurons also demonstrate precise spike timing, suggesting that higher brain areas also represent self-motion using temporally precise firing. These findings demonstrate that two distinct sensory channels represent vestibular information: one using rate coding and the other that takes advantage of precise spike timing.