Cognitive processes involved in smooth pursuit eye movements
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.
Section snippets
Ramp and step-ramp stimuli
Smooth pursuit initiation (see glossary): The simplest way to examine the pursuit system is by considering the response to the unexpected movement of a target that suddenly starts to move at constant velocity (a ramp motion stimulus). Fig. 1A shows typical eye displacement responses to ramp stimuli of varying velocity. There is normally a reaction time of ∼100–130 ms before smooth movements start (Robinson, 1965), although much shorter latencies of 70–100 ms have been recorded (Behrens et al.,
Gain control – active versus passive mechanisms
When humans are confronted with multiple moving stimuli (e.g., a typical street scene) they have to select which of the moving objects is of particular interest and follow that specific object (see Section 3.2). How is this accomplished? One possible explanation is that the motion of that stimulus is selectively enhanced in relation to other stimuli, resulting in an increase in open-loop gain associated with that target. Various experiments have shown clear differences in the magnitude of
The importance of predictive behaviour in general motor control
There are two main aims of predictive behaviour. One is to simply overcome delays in the processing of sensory information. The other is to allow movements to be pre-programmed and thus temporarily dissociated from their sensory input, in order to allow more than one motor response to be executed simultaneously. Prediction is evident in two ways: (a) when a tracked target temporarily disappears, smooth eye movement, whether constant velocity (Becker & Fuchs, 1985) or sinusoidal (Whittaker &
Conclusions
The findings discussed here emphasise the important role that cognitive processing plays in the initiation and maintenance of ocular pursuit. Although the basic information needed to drive pursuit is ultimately extracted from visual input, cognitive control exerts a strong influence over the manner in which that information is used to control the eye. Although there is a strong tradition of using oculomotor tests for assessment of dysfunction in movement disorders, neuro-ophthalmology and
References (169)
Visual-vestibular interaction in the control of head and eye movement: the role of visual feedback and predictive mechanisms
Progress in Neurobiology
(1993)- et al.
Velocity step responses of the human gaze pursuit system. Experiments with sigma-movement
Vision Research
(1985) - et al.
Human motion perception and smooth eye movements show similar directional biases for elongated apertures
Vision Research
(1998) - et al.
Stimulus conditions that enhance anticipatory slow eye movements
Vision Research
(1988) - et al.
Predictive smooth pursuit eye movements near abrupt changes in motion direction
Vision Research
(1992) Dynamic visual acuity, eye movements and peripheral acuity for moving targets
Vision Research
(1972)- et al.
Visual and cognitive control of attention in smooth pursuit
Progress in Brain Research
(2002) - et al.
Characteristics of smooth eye movements with stabilized targets
Vision Research
(1984) - et al.
Characterization of prediction in the primate visual smooth pursuit system
BioSystems
(1995) - et al.
Optokinetic reactions in man elicited by localized retinal motion stimuli
Vision Research
(1979)
Explaining the symptoms of schizophrenia: Abnormalities in the awareness of action
Brain Research Reviews
Eye movements and the afterimage-1. Tracking the afterimage
Vision Research
Volitional scaling of anticipatory ocular pursuit velocity using precues
Cognitive Brain Research
The relationship of anticipatory smooth eye movement to smooth pursuit initiation
Vision Research
Smooth-pursuit initiation in the presence of a textured background in monkey
Vision Research
Effects of attention shifts to stationary objects during steady-state smooth pursuit eye movements
Vision Research
Shared attentional control of smooth eye movement and perception
Vision Research
Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit
Vision Research
The effect of expectations on slow oculomotor control IV. Anticipatory smooth eye movements depend on prior target motions
Vision Research
Sensitivity of smooth eye movement to small differences in target velocity
Vision Research
Voluntary selection of the target for smooth eye movement in the presence of superimposed, full-field stationary and moving stimuli
Vision Research
The effect of expectations on slow oculomotor control-I. Periodic target steps
Vision Research
The effect of expectations on slow oculomotor control-II. Single target displacements
Vision Research
Neural correlates of target choice for pursuit and saccades in the primate superior colliculus
Neuron
Decreases in the latency of smooth pursuit and saccadic eye movements produced by the “gap paradigm” in the monkey
Vision Research
Suppression of optokinesis during smooth pursuit eye movements revisited: The role of extra-retinal information
Vision Research
Cancellation of self-induced retinal image motion during smoot pursuit eye movements
Vision Research
Anticipatory movement timing using prediction and external cues
The Journal of Neuroscience
Smooth pursuit eye movements in response to unpredictable target waveforms
Vision Research
Model emulates human smooth pursuit system producing zero-latency target tracking
Biology Cybernetics
The mechanism of prediction in human smooth pursuit eye movements
Journal of Physiology (London)
Pursuit of intermittently illuminated moving targets in the human
Journal of Physiology (London)
Ocular pursuit responses to repeated, single-cycle sinusoids reveal behavior compatible with predictive pursuit
Journal of Neurophysiology
Evidence for a link between the extra-retinal component of random-onset pursuit and the anticipatory pursuit of predictable object motion
Journal of Neurophysiology
The influence of briefly presented randomised target motion on the extra-retinal component of ocular pursuit
Journal of Neurophysiology
Predicting the duration of ocular pursuit in humans
Experimental Brain Research
The interaction of conflicting retinal motion stimuli in oculomotor control
Experimental Brain Research
The remembered pursuit task: evidence for segregation of timing and velocity storage in predictive oculomotor control
Experimental Brain Research
Predictive velocity estimation in the pursuit reflex response to pseudo-random and step displacement stimuli in man
Journal of Physiology (London)
Volitional control of anticipatory ocular pursuit responses under stabilized image conditions in humans
Experimental Brain Research
Volitional control of anticipatory ocular smooth pursuit after viewing, but not pursuing, a moving target: evidence for a re-afferent velocity store
Experimental Brain Research
The influence of display characteristics on active pursuit and passively induced eye movements
Experimental Brain Research
Factors affecting the predictability of pseudo-random motion stimuli in the pursuit reflex of man
Journal of Physiology (London)
Sequence learning in human ocular smooth pursuit
Experimental Brain Research
Directional defects in pursuit and motion perception in humans with unilateral cerebral lesions
Brain
Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target
Experimental Brain Research
Smooth pursuit eye movements and optokinetic nystagmus elicited by intermittently illuminated stationary patterns
Experimental Brain Research
Human ocular pursuit during the transient disappearance of a moving target
Journal of Neurophysiology
Predictive smooth ocular pursuit during the transient disappearance of a visual target
Journal of Neurophysiology
Ocular pursuit to a predictable velocity and/or position change during the occlusion of a moving target
Society of Neuroscience Abstract
Cited by (242)
Eye movements during optic flow perception
2023, Vision ResearchCharacterizing motion prediction in small autonomous swarms
2023, Applied Ergonomics