Convergence of vestibular and proprioceptive signals in the cerebellar nodulus/uvula enhances the encoding of self-motion in primates.

Abstract

The integration of different sensory streams is required to dynamically estimate how our head and body are oriented and moving relative to gravity. This process is essential to continuously maintain stable postural control, autonomic regulation, and self-motion perception. The nodulus/uvula (NU) in the posterior cerebellar vermis is known to integrate canal and otolith vestibular input to signal angular and linear head motion in relation to gravity. However, estimating body orientation and motion requires integrating proprioceptive cues with vestibular signals. Lesion studies demonstrate that the NU is crucial for maintaining postural control, suggesting it could play an important role in combining multimodal sensory input. Using high-density extracellular recordings in rhesus monkeys, we found that the majority of vestibular-sensitive Purkinje cells also encoded dynamic neck proprioceptive input. Furthermore, Purkinje cells generally aligned their directional tuning to vestibular and proprioceptive stimulation such that self-motion encoding was enhanced. The heterogeneous response dynamics among Purkinje cells enabled their population activity to generate head or body motion encoding in the downstream nuclei neurons on which they converge. Strikingly, when we then experimentally altered the orientation of the head relative to the body, Purkinje cells modulated their responses to vestibular stimulation to account for the change in body motion in space. These findings reveal that the NU integrates proprioceptive and vestibular input synergistically to maintain robust postural control.