Change in sensitivity to visual error in superior colliculus during saccade adaptation

Yoshiko Kojima,Robijanto Soetedjo

doi:10.1038/s41598-017-10242-z

Abstract

Saccadic eye movements provide a valuable model to study the brain mechanisms underlying motor learning. If a target is displaced surreptitiously while a saccade is underway, the saccade appears to be in error. If the error persists gradual neuronal adjustments cause the eye movement again to land near the target. This saccade adaptation typically follows an exponential time course, i.e., adaptation speed slows as adaptation progresses, indicating that the sensitivity to error decreases during adaptation. Previous studies suggested that the superior colliculus (SC) sends error signals to drive saccade adaptation. The objective of this study is to test whether the SC error signal is related to the decrease in the error sensitivity during adaptation. We show here that the visual activity of SC neurons, which is induced by a constant visual error that drives adaptation, decreases during saccade adaptation. This decrease of sensitivity to visual error was not correlated with the changes of primary saccade amplitude. Therefore, a possible interpretation of this result is that the reduction of visual sensitivity of SC neurons contributes an error sensitivity signal that could help control the saccade adaptation process.

Highlights

For goal directed tasks, the brain keeps the movement accurate by reducing its error
We kept the visual error at the end of the primary saccades fairly constant at 4° throughout the entire adaptation session (Fig. 1A, see Methods for details), the visual activity decreased (Fig. 1C, black arrow with “Visual activity”)
Our objective was to determine whether the visual response of superior colliculus (SC) neurons decreased during adaptation as the error sensitivity decreased

Summary

Introduction

The brain keeps the movement accurate by reducing its error. The increased complex spike activity, in turn weakens the synaptic strength of the parallel fibers on P-cells to decrease their simple spike activity This altered simple spike activity influences motor commands in the brainstem or elsewhere. Consistent with this theory, the probability of complex spike occurrence in the oculomotor vermis (OMV) increases and the frequency of simple spikes decreases during saccade adaptation (refs 9–12, cf refs 13 and 14). Stimulation of the rostral SC timed to the occurrence of complex spike enhancement during saccade adaptation drives saccade adaptation without any “natural” visual error[19, 20] This finding suggests that rostral SC stimulation can act as a surrogate error signal to drive adaptation, presumably by evoking complex spikes in the OMV.

Objectives

Methods

Results

Conclusion