The Macaque Cerebellar Flocculus Outputs a Forward Model of Eye Movement.

Gyutae Kim,Pablo M Blazquez,Tatyana A Yakusheva,Jean Laurens

doi:10.3389/fnint.2019.00012

Abstract

The central nervous system (CNS) achieves fine motor control by generating predictions of the consequences of the motor command, often called forward models of the movement. These predictions are used centrally to detect not-self generated sensations, to modify ongoing movements, and to induce motor learning. However, finding a neuronal correlate of forward models has proven difficult. In the oculomotor system, we can identify neuronal correlates of forward models vs. neuronal correlates of motor commands by examining neuronal responses during smooth pursuit at eccentric eye positions. During pursuit, torsional eye movement information is not present in the motor command, but it is generated by the mechanic of the orbit. Importantly, the directionality and approximate magnitude of torsional eye movement follow the half angle rule. We use this rule to investigate the role of the cerebellar flocculus complex (FL, flocculus and ventral paraflocculus) in the generation of forward models of the eye. We found that mossy fibers (input elements to the FL) did not change their response to pursuit with eccentricity. Thus, they do not carry torsional eye movement information. However, vertical Purkinje cells (PCs; output elements of the FL) showed a preference for counter-clockwise (CCW) eye velocity [corresponding to extorsion (outward rotation) of the ipsilateral eye]. We hypothesize that FL computes an estimate of torsional eye movement since torsion is present in PCs but not in mossy fibers. Overall, our results add to those of other laboratories in supporting the existence in the CNS of a predictive signal constructed from motor command information.

Highlights

An important theoretical concept in motor control is that, for optimal motor performance, a control system must includes two internal models
Neuronal recordings and clinical studies have pointed to the cerebellar cortex as one candidate site where forward models are constructed (Ghasia et al, 2008; Bhanpuri et al, 2012)
We evaluated this hypothesis by recording the activity of mossy fibers and Purkinje cells (PCs) in the FL during sinusoidal smooth pursuit eye movements at different viewing eccentricities

Summary

Introduction

An important theoretical concept in motor control is that, for optimal motor performance, a control system must includes two internal models. One model converts the desired movement into forces (inverse model), while a second model works as a predictor that decodes the output of the inverse model (forces) into its consequences (forward or predictive model; Figure 1). These two internal models allow the control system to bypass the long delays associated with sensory feedback and adapt to variations in the environment (Wolpert et al, 1998). The existence of inverse models in biological systems is widely accepted because the brain must, somehow, convert desired movements into actual motor commands. Purkinje cells (PCs) in cerebellar cortex lobules IV–VI of the non-human primate carry information related to both movement kinematics and error feedback, but not to motor command (Popa et al, 2012)

Methods

Results

Conclusion