Distinct representations of body and head motion are dynamically encoded by Purkinje cell populations in the macaque cerebellum

The ability to accurately control our posture and perceive our spatial orientation during self-motion requires knowledge of the motion of both the head and body. However, while the vestibular sensors and nuclei directly encode head motion, no sensors directly encode body motion. Instead, the integration of vestibular and neck proprioceptive inputs is necessary to transform vestibular information into the body-centric reference frame required for postural control. The anterior vermis of the cerebellum is thought to play a key role in this transformation, yet how its Purkinje cells transform multiple streams of sensory information into an estimate of body motion remains unknown. Here, we recorded the activity of individual anterior vermis Purkinje cells in alert monkeys during passively applied whole-body, body-under-head, and head-on-body rotations. Most Purkinje cells dynamically encoded an intermediate representation of self-motion between head and body motion. Notably, Purkinje cells responded to both vestibular and neck proprioceptive stimulation with considerable heterogeneity in their response dynamics. Furthermore, their vestibular responses were tuned to head-on-body position. In contrast, targeted neurons in the deep cerebellar nuclei are known to unambiguously encode either head or body motion across conditions. Using a simple population model, we established that combining responses of similar to 40-50 Purkinje cells could explain the responses of these deep cerebellar nuclei neurons across all self-motion conditions. We propose that the observed heterogeneity in Purkinje cell response dynamics underlies the cerebellum's capacity to compute the dynamic representation of body motion required to ensure accurate postural control and perceptual stability in our daily lives.

Automated summary

Accurately controlling posture and spatial orientation during self-motion requires integration of vestibular and neck proprioceptive inputs. The anterior vermis of the cerebellum is believed to play a crucial role in transforming sensory information into an estimate of body motion. The response dynamics of Purkinje cells in the anterior vermis show heterogeneity and they encode an intermediate representation of self-motion between head and body motion. This heterogeneity is proposed to underlie the cerebellum's ability to compute the dynamic representation of body motion for postural control and perceptual stability.