Frontal cortical control of smooth-pursuit

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Abstract

To maintain optimal clarity of objects moving slowly in three dimensional space, frontal eyed-primates use both smooth-pursuit and vergence (depth) eye movements to track precisely those objects and maintain their images on the foveae of left and right eyes. The caudal parts of the frontal eye fields contain neurons that discharge during smooth-pursuit. Recent results have provided a new understanding of the roles of the frontal eye field pursuit area and suggest that it may control the gain of pursuit eye movements, code predictive visual signals that drive pursuit, and code commands for smooth eye movements in a three dimensional coordinate frame.

Introduction

The smooth-pursuit eye movement system has developed in response to several requirements imposed on it by the evolution of binocular visual fields and high acuity fovea. It is used for accurate tracking of small objects of interest moving slowly and smoothly in fronto-parallel planes to maintain clear vision (Figure 1a; 1., 2.). To accomplish this, visual target-motion signals must be spatially (i.e. direction) and temporally (i.e. speed) processed, and the strength of this visual-motor transmission for pursuit (i.e. gain) must be appropriately controlled 3., 4.. In addition, during head movement, the pursuit system must interact with the vestibular system to maintain the accuracy of eye movements in space so that eye-velocity-in-space (i.e. gaze velocity) matches target velocity [5]. Furthermore, because of the long latencies (of around 100 ms) between changes in the target movement and the initiation of changes in pursuit movements, prediction must be used to compensate for the delays [6]. Also, adaptation is necessary to maintain efficient tracking performance in the face of changing sensory input and motor performance 7., 8.. Finally, in daily life interesting objects move in 3D space. To track them we use conjugate smooth-pursuit that moves both eyes in the same direction and the disconjugate vergence system that moves left and right eyes in opposite directions (Figure 1a; [2]). As both systems are used to maintain target images, these two systems must be synthesized. Which portions of the brain accomplish this synthesis? Here, I discuss these points and the potential involvement of the frontal eye fields (FEF).

Section snippets

The organization of the smooth pursuit system

A great deal is known about the anatomy of the pursuit system, in particular the portions of the frontal cortex that are involved, and how it might be organized. Figure 1b summarizes the major structures that are related to smooth-pursuit and their interconnections and vestibular inputs 1., 2., 9., 10., 11.•, 12.. The primate frontal cortex contains two areas related to smooth-pursuit: the caudal parts of the FEF in the fundus and posterior bank of the arcuate sulcus, and the supplementary eye

The functional relationship between smooth-pursuit and vestibular systems

The importance of vestibular inputs to the pursuit system is demonstrated by the finding that virtually all brain areas known to be related to pursuit, including cerebellar and cerebral cortical areas (Figure 1b), also respond to vestibular input 2., 17., 24., 25.•, 26., 27., 28.•, 29.•, 30., 31., 32.. As smooth-pursuit in a head restrained condition cannot dissociate eye movements in the orbit from eye movements in space (i.e. gaze, Figure 1c), passive whole body rotation has routinely been

Gain control

For accurate and efficient performance of smooth pursuit, the gain of eye velocity commands must be controlled 3., 4.. This ‘gain control’ is necessary to enhance the responses to relevant sensory inputs, and to select and to emphasize specific motor responses. In models of pursuit (e.g. Figure 1c), the gain also must be controlled so that the positive feedback loop does not create inaccurate eye movements. FEF gain control has been demonstrated by electrical stimulation of the FEF pursuit area

Prediction in smooth-pursuit

Prediction of target trajectory is used in the pursuit system to maintain retinal images near the foveae during tracking of moving targets 6., 40., 41.. Prediction should occur not only on the motor side as preparation and perseverance of ongoing movements [6] but also on the sensory and/or perception side [42]. An example is a visual response that anticipates the eventually renewed direction and speed of the target movement of a temporarily occluded visual input. Such a mechanism may use

Adaptation in smooth-pursuit

Smooth-pursuit shows adaptive responses to changes in conditions of ramp target motion 7., 8.. As the latency of smooth-pursuit to a ramp target motion is about 100 ms, the initial eye movement within about 100 ms of onset of pursuit is driven entirely by visual inputs. This open loop response and the later response that allows visual feedback have been analyzed separately. Adaptation in smooth-pursuit was induced by repeated presentation of a small target that moved at one speed for about 100 ms

Pursuit eye movements in 3D space

Traditionally, smooth-pursuit and vergence systems are thought to have separate neural substrates [2]. Indeed, at cerebral cortical, cerebellar and brainstem levels, signals related to vergence eye movements and the visual signals that elicit them have been found to be coded independently of signals related to fronto-parallel smooth-pursuit 2., 52., 53., 54.. Contrary to this common view, the majority of caudal FEF pursuit neurons are strongly modulated during both frontal- and depth-pursuit,

Conclusions and future studies

This review summarizes recent insights into understanding the roles that the caudal FEF might play in pursuit eye movements. Caudal FEF pursuit neurons are involved in voluntary coordination of binocular smooth gaze movements for targets in 3D space, in prediction of target trajectory, and in task-dependent gain control. To better understand the specific role of the caudal FEF, it will be necessary to examine the nature of its role in adaptive control and to specify how the FEF participates in

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

I thank CRS Kaneko for his valuable comments on this review. This work was supported in part by Japanese Ministry of Education, Culture, Science, Sports and Technology (15016004 14658266), Marna Cosmetics and Toyota Riken.

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