The same oculomotor vermal Purkinje cells encode the different kinematics of saccades and of smooth pursuit eye movements

Marc Junker,Peter Thier,Aleksandra Smilgin,Zongpeng Sun,Peter W Dicke

doi:10.1038/srep40613

Abstract

Saccades and smooth pursuit eye movements (SPEM) are two types of goal-directed eye movements whose kinematics differ profoundly, a fact that may have contributed to the notion that the underlying cerebellar substrates are separated. However, it is suggested that some Purkinje cells (PCs) in the oculomotor vermis (OMV) of monkey cerebellum may be involved in both saccades and SPEM, a puzzling finding in view of the different kinematic demands of the two types of eye movements. Such ‘dual’ OMV PCs might be oddities with little if any functional relevance. On the other hand, they might be representatives of a generic mechanism serving as common ground for saccades and SPEM. In our present study, we found that both saccade- and SPEM-related responses of individual PCs could be predicted well by linear combinations of eye acceleration, velocity and position. The relative weights of the contributions that these three kinematic parameters made depended on the type of eye movement. Whereas in the case of saccades eye position was the most important independent variable, it was velocity in the case of SPEM. This dissociation is in accordance with standard models of saccades and SPEM control which emphasize eye position and velocity respectively as the relevant controlled state variables.

Highlights

Saccades and smooth pursuit eye movements (SPEM) are two synergistic types of eye movements which allow the visual system to exploit the advantages of foveal vision for the analysis of objects of interest (‘targets’)
Are these ‘dual’ Purkinje cells (PCs) representative of oculomotor vermis (OMV) PCs at large or are they oddities with little if any functional relevance? if these PC units are representative of the whole population rather than oddities, this would probably suggest that such PCs offer a hitherto unknown functional contribution to an aspect of eye movements shared by saccades and SPEM
In our previous work on smooth-pursuit- related OMV PC simple spike (SS) units, we explored the kinematic preferences in more detail by modeling the relationship between discharge and the early, open-loop SPEM based on a linear combination of eye acceleration, velocity and position

Summary

Introduction

Saccades and smooth pursuit eye movements (SPEM) are two synergistic types of eye movements which allow the visual system to exploit the advantages of foveal vision for the analysis of objects of interest (‘targets’). Whereas saccades shift the target image onto the fovea, SPEM are deployed to stabilize it there despite movements of the target relative to the observer The kinematics of these two types of goal-directed eye movements differ profoundly. In our previous work on smooth-pursuit- related OMV PC SS units, we explored the kinematic preferences in more detail by modeling the relationship between discharge and the early, open-loop SPEM based on a linear combination of eye acceleration, velocity and position. This analysis clearly indicated that eye velocity is the most relevant kinematic parameter[22]. We report that many PC SS units are sensitive to saccades and SPEM and, that different kinematic parameters are emphasized during SPEM and saccades

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