Purkinje Cells in Posterior Cerebellar Vermis Encode Motion in an Inertial Reference Frame

Abstract

The ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation.

Vestibular Signals in Primate Thalamus: Properties and Origins

“…These stimuli were identical to those used previously to independently manipulate inertial and net gravitoinertial accelerations Shaikh et al, 2005b;Yakusheva et al, 2007); they consisted of pure translation (translation), pure tilt (tilt), or combined translation and tilt (tilt minus translation motion and tilt plus translation). The tilt stimulus consisted of a 0.5 Hz sinusoidal rotation from an upright position with peak amplitude of 11.3°(36°/s).…”

“…Briefly, these models assume that neural firing rate modulation is either attributable to the net acceleration or to the translational acceleration component (for details, see Angelaki et al, 2004;Green et al, 2005;Shaikh et al, 2005b;Yakusheva et al, 2007). How well each of these two models fitted the data were evaluated using a partial correlation analysis.…”

“…In particular, we showed that VN and CN neurons carried two components of linear acceleration in different proportions: (1) an estimate of net linear acceleration originating from otolith afferent signals, and (2) an estimate of gravitational acceleration derived from a tilt-related signal originating from spatially and temporally transformed canal afferent signals Yakusheva et al, 2007). Thus, a simple weighted average population code would extract either net linear acceleration (by assigning weights such that the second term is canceled) or translation (by assigning weights that give a population sum that is equal for the two components) .…”

Gravity orientation tuning in macaque anterior thalamus

“…Gravity is sensed by the otolith organs of the inner ear, but gravity and inertial accelerations must be differentiated, and this is achieved by a distributed brainstem/cerebellar circuit 1–4 using an internal model of the physical laws of nature 5–7 . We 7 have hypothesized that gravity provides a global allocentric reference for spatial orientation.…”

“…Gravity is sensed by the otolith organs of the inner ear, but gravity and inertial accelerations must be differentiated, and this is achieved by a distributed brainstem/cerebellar circuit 1–4 using an internal model of the physical laws of nature 5–7 . We 7 have hypothesized that gravity provides a global allocentric reference for spatial orientation. Head direction (HD) cells form a “neuronal compass”, encoding head orientation in the horizontal plane 8 as well as head orientation relative to vertical, as shown recently in the dorsal presubiculum of bats 9 .…”