Cerebellar re-encoding of self-generated head movements.

Guillaume P Dugué,Boris Gourévitch,Matthieu Tihy,Clément Léna

doi:10.7554/elife.26179

Abstract

Head movements are primarily sensed in a reference frame tied to the head, yet they are used to calculate self-orientation relative to the world. This requires to re-encode head kinematic signals into a reference frame anchored to earth-centered landmarks such as gravity, through computations whose neuronal substrate remains to be determined. Here, we studied the encoding of self-generated head movements in the rat caudal cerebellar vermis, an area essential for graviceptive functions. We found that, contrarily to peripheral vestibular inputs, most Purkinje cells exhibited a mixed sensitivity to head rotational and gravitational information and were differentially modulated by active and passive movements. In a subpopulation of cells, this mixed sensitivity underlay a tuning to rotations about an axis defined relative to gravity. Therefore, we show that the caudal vermis hosts a re-encoded, gravitationally polarized representation of self-generated head kinematics in freely moving rats.

Highlights

Self-orientation is largely dependent on modalities that document head movements, including neck 18 proprioception, optic flow and, most notably, vestibular inputs
Head direction cells are anchored to a reference frame aligned with gravity rather than to the animal’s locomotor plane 28 (Taube et al, 2013; Finkelstein et al, 2016; Wilson et al, 2016; Olson et al, 2016); their activity, which relies on the temporal integration of head angular velocity signals (Song & Wang, 2005), 30 requires information on head orientation relative to gravity (Yoder & Taube, 2009)
Our findings reveal that the caudal cerebellar vermis hosts gravitationally-polarized representations of head rotations in freely moving rats

Summary

Introduction

Self-orientation is largely dependent on modalities that document head movements, including neck 18 proprioception, optic flow and, most notably, vestibular inputs. Vestibular signals are essential for stabilizing gaze (du Lac et al, 1995) and for computing head direction, spatial maps and navigation 20 trajectories (Stackman et al, 2002; Yoder & Taube, 2014; Wallace et al, 2002) These signals originate from two categories of skull-anchored inertial sensors: gyroscope-like structures (semi circular canals), which transduce head angular velocity, and accelerometer-like structures (otolith organs), which are activated indifferently by accelerated linear motion and by gravity. 44 A considerable literature has described the responses of caudal vermis Purkinje cells to passively experienced head movements (Barmack & Yakhnitsa, 2011) These movements 46 only covered the lower range of frequencies and amplitudes observed during active self-motion (Carriot et al, 2015). We decided to study the encoding of head movements in 54 the caudal cerebellar vermis in freely moving rats, while monitoring the movements of their head using a miniature inertial sensor

Results

Discussion

Materials and Methods