Cognitive processes involved in smooth pursuit eye movements

Abstract

Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.

Introduction

Ocular pursuit is a mechanism that enables tracking of moving objects in extra-personal space with the eyes alone. It is an example of a sensorimotor feedback system and although, at first sight, it appears relatively simple, it reveals surprising complexities. If the observer is pursuing a single small moving object the main aim is generally to maintain a clear view of that object. There are two goals for this behaviour. One is to reduce the motion of the object’s image on the retina, since image motion creates blur and impairs visual acuity. Eye velocity thus needs to match object velocity as closely as possible. For this purpose, retinal velocity error information is sensed by neural mechanisms in the retina and specialized areas in visual association cortex and used to control the magnitude and timing of smooth eye movements. A second goal is to maintain the object’s image close to the fovea, the area of highest acuity on the retina. If the eye does not keep up with the motion of the object, as often happens, the visual system senses the positional error created and realigns the eye, normally with very rapid saccadic movements. Ocular pursuit hardly ever involves purely smooth eye movement. There is generally some saccadic activity and the manner in which smooth and saccadic responses interact is important in understanding the manner in which the system operates.

Although there are direct sensorimotor links that can control smooth eye movements, it has become evident that cognitive processes play a large part in pursuit. Attention, selection, learning and prediction are all of importance in different contexts. Pursuit is normally thought of as a voluntary process and, certainly, volition plays an important part in the initial process of selecting which target to pursue. However, reflexive processes are also evident, since involuntary smooth eye movements can be induced by the motion of even very small targets in certain circumstances. Yet, when confronted by multiple moving objects (e.g., when driving) it is possible to select which object to follow. Recent evidence shows that only the first fraction of a second of exposure to multiple moving objects is driven by the average of those inputs – thereafter, a decision is made to follow a single object. In these circumstances, volition may simply serve to selectively enhance the visual feedback for a chosen target and thus override the effects of other stimuli. This may be particularly important when attempting to track a moving target as it passes over a structured background, since the relative movement of the eye across the background would otherwise reduce smooth eye velocity. However, other evidence indicates that inhibition of motion information from the background may also be important. Consideration of these issues indicates that, although retinal error input is important, there are many ways in which the information may be modified by cognitive processes. Another example is afforded by the ability to track apparent motion stimuli. These may be created in a number of different ways but what they have in common is that the sensory information is incomplete or degraded. Nevertheless, pursuit is still possible.

Another area of performance in which cognitive factors play an important part is in predictive behaviour. Although there are considerable time delays in visual motion processing, these can largely be overcome by predictive mechanisms. This is evident in the fact that tracking of periodic target motion evokes smaller phase errors than predicted from the visual processing delays. This implies that the subject can, for example, change smooth eye movement direction before sensory information has been processed. Yet, it appears that the ability to use volitional control to actively initiate smooth movement is very poor. So, it is difficult to imagine how volitional control of smooth movement could, of itself, influence this process. However, it has been shown that the key factor controlling the ability to initiate anticipatory smooth pursuit is the expectation of future object motion created by past experience. In effect, expectation appears to gate the output of anticipatory smooth movements. Another cognitive factor that plays a large part in predictive pursuit is learning. Anticipatory movements are of no use if they are not appropriate in direction, timing and speed. It is now apparent that these attributes can be learned very rapidly from prior exposure if motion stimuli are repeated, as they are during periodic target motion. Finally, but of equal importance, it is essential that there is an ability to compare the predictive estimate with current sensory input. Thus, another essential cognitive factor is mismatch (or conflict) detection, the ability to compare the predictive estimate with current visual feedback and to modify it if necessary.

This article aims to review the behavioural evidence about the operation of the pursuit system that has accumulated over many years, but, in particular, will emphasize developments that have moved the study away from the rather mechanistic views of early investigators to consider more cognitive aspects of system performance.