Vestibular contributions to online reach execution are processed via mechanisms with knowledge about limb biomechanics.

Studies of reach control with the body stationary have shown that proprioceptive and visual feedback signals contributing to rapid corrections during reaching are processed by neural circuits that incorporate knowledge about the physical properties of the limb (an internal model). However, among the most common spatial and mechanical perturbations to the limb are those caused by our body's own motion, suggesting that processing of vestibular signals for online reach control may reflect a similar level of sophistication. We investigated this hypothesis using galvanic vestibular stimulation (GVS) to selectively activate the vestibular sensors, simulating body rotation, as human subjects reached to remembered targets in different directions (forward, leftward, rightward). If vestibular signals contribute to purely kinematic/spatial corrections for body motion, GVS should evoke reach trajectory deviations of similar size in all directions. In contrast, biomechanical modeling predicts that if vestibular processing for online reach control takes into account knowledge of the physical properties of the limb and the forces applied on it by body motion, then GVS should evoke trajectory deviations that are significantly larger during forward and leftward reaches as compared with rightward reaches. When GVS was applied during reaching, the observed deviations were on average consistent with this prediction. In contrast, when GVS was instead applied before reaching, evoked deviations were similar across directions, as predicted for a purely spatial correction mechanism. These results suggest that vestibular signals, like proprioceptive and visual feedback, are processed for online reach control via sophisticated neural mechanisms that incorporate knowledge of limb biomechanics.NEW & NOTEWORTHY Studies examining proprioceptive and visual contributions to rapid corrections for externally applied mechanical and spatial perturbations during reaching have provided evidence for flexible processing of sensory feedback that accounts for musculoskeletal system dynamics. Notably, however, such perturbations commonly arise from our body's own motion. In line with this, we provide compelling evidence that, similar to proprioceptive and visual signals, vestibular signals are processed for online reach control via sophisticated mechanisms that incorporate knowledge of limb biomechanics.

Role of Rostral Fastigial Neurons in Encoding a Body-Centered Representation of Translation in Three Dimensions.

Many daily behaviors rely critically on estimates of our body motion. Such estimates must be computed by combining neck proprioceptive signals with vestibular signals that have been transformed from a head- to a body-centered reference frame. Recent studies showed that deep cerebellar neurons in the rostral fastigial nucleus (rFN) reflect these computations, but whether they explicitly encode estimates of body motion remains unclear. A key limitation in addressing this question is that, to date, cell tuning properties have only been characterized for a restricted set of motions across head-re-body orientations in the horizontal plane. Here we examined, for the first time, how 3D spatiotemporal tuning for translational motion varies with head-re-body orientation in both horizontal and vertical planes in the rFN of male macaques. While vestibular coding was profoundly influenced by head-re-body position in both planes, neurons typically reflected at most a partial transformation. However, their tuning shifts were not random but followed the specific spatial trajectories predicted for a 3D transformation. We show that these properties facilitate the linear decoding of fully body-centered motion representations in 3D with a broad range of temporal characteristics from small groups of 5-7 cells. These results demonstrate that the vestibular reference frame transformation required to compute body motion is indeed encoded by cerebellar neurons. We propose that maintaining partially transformed rFN responses with different spatiotemporal properties facilitates the creation of downstream body motion representations with a range of dynamic characteristics, consistent with the functional requirements for tasks such as postural control and reaching.SIGNIFICANCE STATEMENT Estimates of body motion are essential for many daily activities. Vestibular signals are important contributors to such estimates but must be transformed from a head- to a body-centered reference frame. Here, we provide the first direct demonstration that the cerebellum computes this transformation fully in 3D. We show that the output of these computations is reflected in the tuning properties of deep cerebellar rostral fastigial nucleus neurons in a specific distributed fashion that facilitates the efficient creation of body-centered translation estimates with a broad range of temporal properties (i.e., from acceleration to position). These findings support an important role for the rostral fastigial nucleus as a source of body translation estimates functionally relevant for behaviors ranging from postural control to perception.

Evidence for a reference frame transformation of vestibular signal contributions to voluntary reaching.

To contribute appropriately to voluntary reaching during body motion, vestibular signals must be transformed from a head-centered to a body-centered reference frame. We quantitatively investigated the evidence for this transformation during online reach execution by using galvanic vestibular stimulation (GVS) to simulate rotation about a head-fixed, roughly naso-occipital axis as human subjects made planar reaching movements to a remembered location with their head in different orientations. If vestibular signals that contribute to reach execution have been transformed from a head-centered to a body-centered reference frame, the same stimulation should be interpreted as body tilt with the head upright but as vertical-axis rotation with the head inclined forward. Consequently, GVS should perturb reach trajectories in a head-orientation-dependent way. Consistent with this prediction, GVS applied during reach execution induced trajectory deviations that were significantly larger with the head forward compared with upright. Only with the head forward were trajectories consistently deviated in opposite directions for rightward versus leftward simulated rotation, as appropriate to compensate for body vertical-axis rotation. These results demonstrate that vestibular signals contributing to online reach execution have indeed been transformed from a head-centered to a body-centered reference frame. Reach deviation amplitudes were comparable to those predicted for ideal compensation for body rotation using a biomechanical limb model. Finally, by comparing the effects of application of GVS during reach execution versus prior to reach onset we also provide evidence that spatially transformed vestibular signals contribute to at least partially distinct compensation mechanisms for body motion during reach planning versus execution.