Reference frames for encoding of translation and tilt in the caudal cerebellar vermis.

Abstract

Many daily behaviors rely on estimates of our body's motion and orientation in space. Vestibular signals are essential for such estimates but to contribute appropriately two key computations are required. First, ambiguous motion information from the otolith organs must be combined with spatially transformed rotational signals (e.g., from the canals) to distinguish head translation from tilt. Second, tilt and translation estimates must be transformed from a head- to a body-centered reference frame to correctly interpret the body's motion. Studies have shown that cells in the caudal cerebellar vermis (nodulus/ventral uvula, NU) reflect the output of the first set of computations to estimate translation and tilt. However, it remains unknown whether these estimates are encoded exclusively in head-centered coordinates or whether they reflect further transformation towards body-centered coordinates. Here we addressed this question by examining how the 3D spatial tuning of otolith and canal signals on translation- and tilt-selective NU Purkinje cells in male rhesus monkeys varies with changes in head-re-body and body-re-gravity orientation. We show that NU cell tuning properties are consistent with head-centered otolith signal coding during translation. Furthermore, while canal signals in the NU have been transformed into a specific world-referenced rotation signal indicating reorientation relative to gravity (tilt), as needed to resolve the tilt-translation ambiguity, the resulting tilt estimates are encoded in head-centered coordinates. Our results thus suggest that body-centered motion and orientation estimates required for postural control, navigation and reaching are computed elsewhere, either by further transforming NU outputs or via computations in other parallel pathways.Significance statement Estimates of body motion and orientation are essential for daily activities. Vestibular signals contribute vitally to such estimates but must first undergo transformations to distinguish translation from tilt and convert head-centered estimates into body-centered representations. Previous studies implicated the caudal cerebellar vermis (nodulus/uvula, NU) in computing estimates of translation and tilt. However, here we show for the first time that NU cells encode such estimates exclusively in head-centered coordinates. The NU thus reflects motion estimates appropriate for head and gaze stabilization but not the body-centered representations relevant for tasks such as body postural control and reaching. We suggest that head- versus body-centered motion and orientation estimates may be computed via at least partially distinct cerebellar pathways serving different functional roles.