Neural Representation of Orientation Relative to Gravity in the Macaque Cerebellum

Abstract

Summary A fundamental challenge for maintaining spatial orientation and interacting with the world is knowledge of our orientation relative to gravity, i.e. tilt. Sensing gravity is complicated because of Einstein’s equivalence principle, where gravitational and translational accelerations are physically indistinguishable. Theory has proposed that this ambiguity is solved by tracking head tilt through multisensory integration. Here we identify a group of Purkinje cells in the caudal cerebellar vermis with responses that reflect an estimate of head tilt. These tilt-selective cells are complementary to translation-selective Purkinje cells, such that their population activities sum to the net gravito-inertial acceleration encoded by the otolith organs, as predicted by theory. These findings reflect the remarkable ability of the cerebellum for neural computation and provide novel quantitative evidence for a neural representation of gravity, whose calculation relies on long-postulated theoretical concepts such as internal models and Bayesian priors.

Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

“…Despite having similar sensitivities, responses of otolith afferents do not correlate with perceptual decisions, whereas activity of central vestibular and cortical neurons does. These results suggest that choice-related activity first emerges in brainstem and cerebellar neurons with response properties that have been sculpted by the computations necessary to code selectively for inertial self-motion, independent of changes in orientation relative to gravity (15,(28)(29)(30).…”

Gravity orientation tuning in macaque anterior thalamus

“…Thus, the underlying neuronal circuits should integrate rotation velocity signals around all three egocentric (yaw, pitch, roll) axes simultaneously. Indeed, the circuitry that produces an internal model of gravity in the cerebellum has this exact property 2–3 .…”

“…Cells were classified as either G-tuned or dG-tuned based upon whether R 2 G|dG or R 2 dG|G was significantly higher than the other using a bootstrap analysis 2,3 , or as G+dG cells if neither was significantly higher. Each bootstrap sample was produced by drawing n cycles with replacement from the cell’s dataset (consisting of n rotation cycles and including CW and CCW rotations) and re-computing T G (α), T dG (α), R 2 G|dG and R 2 dG|G .…”

The cerebellar nodulus: Perceptual and ocular processing of graviceptive input

“…Electrophysiologically, Purkinje cells in the caudal vermis show responses that reflect estimates of head-tilt relative to gravity. 4 Behaviorally, internal estimates of gravity can be quantified by setting a line along the perceived vertical -the subjective visual vertical (SVV). While estimates are very accurate when upright, systematic physiological roll-angle dependent misestimations occur: roll over-compensation ("Eeffect") for small (<60°) and large (>120-135°) whole-body roll-tilt, roll under-compensation ("Aeffect") for medium-sized (range=60-120°) angles.…”

“…The prolongation of the vestibular response is provided by a neuronal network (velocity-storage mechanism). 7 When the head is reoriented with respect to gravity early in the post-rotatory nystagmus phase, the dTc of the horizontal aVOR is reduced (tilt dumping), 6 while the velocity 4 along an axis orthogonal to the plane defined by the previous rotation and tilt axes is increased, reflecting a reorientation of the eye-rotation axis towards the gravitational vector 8 and indicating resolution of the canal-otolith conflict caused by the head-tilt. 9 In humans, bilateral (but not unilateral) 11 lesions of the nodulus and uvula result in a loss of tilt dumping.…”