Smooth pursuit eye movements in normal and dyslexic children

This paper describes a detailed study of horizontal eye movements associated with visual tracking of a smoothly moving target. Essentially all children, even at target velocities as low as 5 degrees/sec., show some saccadic eye movements superimposed on smooth tracking movements. Detailed analysis of pursuit eye-movements from a group of 26 poor readers and 34 normal controls (8 to 13 yr.) showed that about 25% of poor readers have an abnormally raised saccadic component in smooth pursuit. This suggests that studies of eye movements during tracking of smoothly moving targets at low velocity, combined with a quantitative approach to data analysis, may be useful for early detection of a significant proportion of poor-reading children.     

Infant attention and the development of smooth pursuit tracking.

The effect of attention on smooth pursuit and saccadic tracking was studied in infants at 8, 14, 20, and 26 weeks of age. A small rectangle was presented moving in a sinusoidal pattern in either the horizontal or vertical direction. Attention level was distinguished with a recording of heart rate. There was an increase across age in overall tracking, the gain of the smooth pursuit eye movements, and an increase in the amplitude of compensatory saccades at faster tracking speeds. One age change was an increase in the preservation of smooth pursuit tracking ability as stimulus speed increased. A second change was the increasing tendency during attentive tracking to shift from smooth pursuit to saccadic tracking when the stimulus speed increased to the highest velocities. This study shows that the development of smooth pursuit and targeted saccadic eye movements is closely related to the development of sustained attention in this age range.     

Neurophysiology and neuroanatomy of smooth pursuit: Lesion studies

Smooth pursuit impairment is recognized clinically by the presence of saccadic tracking of a small object and quantified by reduction in pursuit gain, the ratio of smooth eye movement velocity to the velocity of a foveal target. Correlation of the site of brain lesions, identified by imaging or neuropathological examination, with defective smooth pursuit determines brain structures that are necessary for smooth pursuit. Paretic, low gain, pursuit occurs toward the side of lesions at the junction of the parietal, occipital and temporal lobes (area V5), the frontal eye field and their subcortical projections, including the posterior limb of the internal capsule, the midbrain and the basal pontine nuclei. Paresis of ipsiversive pursuit also results from damage to the ventral paraflocculus and caudal vermis of the cerebellum. Paresis of contraversive pursuit is a feature of damage to the lateral medulla. Retinotopic pursuit paresis consists of low gain pursuit in the visual hemifield contralateral to damage to the optic radiation, striate cortex or area V5. Craniotopic paresis of smooth pursuit consists of impaired smooth eye movement generation contralateral to the orbital midposition after acute unilateral frontal or parietal lobe damage. Omnidirectional saccadic pursuit is a most sensitive sign of bilateral or diffuse cerebral, cerebellar or brainstem disease. The anatomical and physiological bases of defective smooth pursuit are discussed here in the context of the effects of lesion in the human brain.     

Neurophysiology and neuroanatomy of smooth pursuit: Lesion studies

Smooth pursuit impairment is recognized clinically by the presence of saccadic tracking of a small object and quantified by reduction in pursuit gain, the ratio of smooth eye movement velocity to the velocity of a foveal target. Correlation of the site of brain lesions, identified by imaging or neuropathological examination, with defective smooth pursuit determines brain structures that are necessary for smooth pursuit. Paretic, low gain, pursuit occurs toward the side of lesions at the junction of the parietal, occipital and temporal lobes (area V5), the frontal eye field and their subcortical projections, including the posterior limb of the internal capsule, the midbrain and the basal pontine nuclei. Paresis of ipsiversive pursuit also results from damage to the ventral paraflocculus and caudal vermis of the cerebellum. Paresis of contraversive pursuit is a feature of damage to the lateral medulla. Retinotopic pursuit paresis consists of low gain pursuit in the visual hemifield contralateral to damage to the optic radiation, striate cortex or area V5. Craniotopic paresis of smooth pursuit consists of impaired smooth eye movement generation contralateral to the orbital midposition after acute unilateral frontal or parietal lobe damage. Omnidirectional saccadic pursuit is a most sensitive sign of bilateral or diffuse cerebral, cerebellar or brainstem disease. The anatomical and physiological bases of defective smooth pursuit are discussed here in the context of the effects of lesion in the human brain.     

Fixation disengagement and eye-movement latency

We examined eye-movement latencies to a target that appeared during visual fixation of a stationary stimulus, a moving stimulus, or an extrafoveal stimulus. The stimulus at fixation was turned off either before target onset (gap condition) or after target onset (overlap condition). Consistent with previous research, saccadic latencies were shorter in gap conditions than they were in overlap conditions (the gap effect). In Experiment 1, a gap effect was observed for vergence eye movements. In Experiment 2, a gap effect was observed for saccades directed at a target that appeared during visual pursuit of a moving stimulus. In Experiment 3, a gap effect was observed for saccades directed at a target that appeared during extrafoveal fixation. The present results extend reports of the gap effect for saccadic shifts during visual fixation to (a) vergence shifts during visual fixation, (b) saccadic shifts during smooth visual pursuit, and (c) saccadic shifts during extrafoveal fixation. The present findings are discussed with respect to the incompatible goals of fixation-locking and fixation-shifting oculomotor responses.     

Effects of directional uncertainty on visually-guided joystick pointing

Reaction times generally follow the predictions of Hick's law as stimulus-response uncertainty increases, although notable exceptions include the oculomotor system. Saccadic and smooth pursuit eye movement reaction times are independent of stimulus-response uncertainty. Previous research showed that joystick pointing to targets, a motor analog of saccadic eye movements, is only modestly affected by increased stimulus-response uncertainty; however, a no-uncertainty condition (simple reaction time to 1 possible target) was not included. Here, we re-evaluate manual joystick pointing including a no-uncertainty condition. Analysis indicated simple joystick pointing reaction times were significantly faster than choice reaction times. Choice reaction times (2, 4, or 8 possible target locations) only slightly increased as the number of possible targets increased. These data suggest that, as with joystick tracking (a motor analog of smooth pursuit eye movements), joystick pointing is more closely approximated by a simple/choice step function than the log function predicted by Hick's law.     

Kinematic property of target motion conditions gaze behavior and eye-hand synergy during manual tracking

This study investigated how frequency demand and motion feedback influenced composite ocular movements and eye-hand synergy during manual tracking. Fourteen volunteers conducted slow and fast force-tracking in which targets were displayed in either line-mode or wave-mode to guide manual tracking with target movement of direct position or velocity nature. The results showed that eye-hand synergy was a selective response of spatiotemporal coupling conditional on target rate and feedback mode. Slow and line-mode tracking exhibited stronger eye-hand coupling than fast and wave-mode tracking. Both eye movement and manual action led the target signal during fast-tracking, while the latency of ocular navigation during slow-tracking depended on the feedback mode. Slow-tracking resulted in more saccadic responses and larger pursuit gains than fast-tracking. Line-mode tracking led to larger pursuit gains but fewer and shorter gaze fixations than wave-mode tracking. During slow-tracking, incidences of saccade and gaze fixation fluctuated across a target cycle, peaking at velocity maximum and the maximal curvature of target displacement, respectively. For line-mode tracking, the incidence of smooth pursuit was phase-dependent, peaking at velocity maximum as well. Manual behavior of slow or line-mode tracking was better predicted by composite eye movements than that of fast or wave-mode tracking. In conclusion, manual tracking relied on versatile visual strategies to perceive target movements of different kinematic properties, which suggested a flexible coordinative control for the ocular and manual sensorimotor systems.     

The extraretinal signal from the pursuit-eye-movement system: its role in the perceptual and the egocentric localization systems

The accuracy of perceptual judgment of the distance of a moving target tracked at various velocities by pursuit eye movements was examined in relation to the amount of two types of eye movement (smooth pursuit eye movement and compensatory saccade) involved in eye tracking. The perceptually judged distance became shorter as the amount of pursuit-eye-movement component in eye tracking increased. A detailed analysis of the eye-movement data and the size of perceptual underestimation indicated that the underestimation was mainly caused by inaccurate extraretinal information derived from the pursuit-eye-movement system, which underestimated the distance at a constant ratio, irrespective of the velocity of tracking. Egocentric localization was not affected by the mode of eye movements, indicating that the egocentric localization system functions without interference from the inaccurate information from the pursuit-eye-movement system.     

Distractor interference during smooth pursuit eye movements

When 2 targets for pursuit eye movements move in different directions, the eye velocity follows the vector average (S. G. Lisberger & V. P. Ferrera, 1997). The present study investigates the mechanisms of target selection when observers are instructed to follow a predefined horizontal target and to ignore a moving distractor stimulus. Results show that at 140 ms after distractor onset, horizontal eye velocity is decreased by about 25%. Vertical eye velocity increases or decreases by 1 degrees /s in the direction opposite from the distractor. This deviation varies in size with distractor direction, velocity, and contrast. The effect was present during the initiation and steady-state tracking phase of pursuit but only when the observer had prior information about target motion. Neither vector averaging nor winner-take-all models could predict the response to a moving to-be-ignored distractor during steady-state tracking of a predefined target. The contributions of perceptual mislocalization and spatial attention to the vertical deviation in pursuit are discussed.     

Eye movements in response to real and apparent motions of acoustic targets.

Monitoring of eye movements resulting from the tracking of sound displacements in total darkness confirmed the generally accepted idea that smooth pursuit cannot be induced in the absence of a real visible target. Exclusively saccadic movements were obtained with real and apparent displacements of a constant frequency source and with frequency variations associated to spatially calibrated positions through training for 5 Ss. Smooth pursuit eye movements were only observed if S was allowed to point and follow with his hand the perceived position of acoustic targets.     

Visual short-term memory during smooth pursuit eye movements

Visual short-term memory (VSTM) was probed while observers performed smooth pursuit eye movements. Smooth pursuit keeps a moving object stabilized in the fovea. VSTM capacity for position was reduced during smooth pursuit compared with a condition with eye fixation. There was no difference between a condition in which the items were approximately stabilized on the retina because they moved with the pursuit target and a condition in which the items moved across the retina because they were stationary in space. The reduction of capacity for position was eliminated when miniature items were presented on the pursuit target. Similarly, VSTM capacity for color did not differ between smooth pursuit and fixation. The results suggest that visuospatial attention is tied to the target during smooth pursuit, which impairs VSTM for the position of peripheral objects. Sensory memory during smooth pursuit was only slightly impaired.     

Contrast sensitivity during horizontal visual pursuit: dynamic sensitivity functions.

The contrast sensitivity functions of college students for grating targets presented at angular velocities of 0, 30, 60, and 90 deg s-1 were determined for target durations of 200 and 600 ms. The most pronounced effects of target movement were evident at the mid to high spatial frequencies in which sensitivity was markedly reduced as velocity increased. These adverse effects were greatest in the 200 ms condition, in which performance was largely limited to the saccadic eye movement system. In the 600 ms condition, in which both saccadic and smooth pursuit eye movements were possible, contrast sensitivity for the low-frequency target actually improved significantly for the 30 and 60 deg s-1 targets, whereas only adverse effects of target motion were found for targets of mid and high spatial frequencies. The results are discussed in terms of the limitations of traditional visual assessment procedures and the practical and theoretical benefits of conceptualizing the joint effects of target composition and target movement.     

Visual localization and estimation of extent of target motion during ocular pursuit: a common mechanism?

The ability to localize a visual target and to estimate the distance through which it moves was studied during ocular pursuit. In the first experiment observers had to localize the position of a visually tracked moving target when they heard an acoustic signal. The signal was sounded near the beginning or near the end of the motion. The distance between the perceived positions was shorter than the distance between the corresponding physical positions of the target. The 'shortening' became more pronounced with higher tracking velocity. In another condition the observers estimated the length of the motion path between two successive sound signals, one presented near the beginning and one near the end of the motion. The length of path travelled was underestimated, the effect being stronger with higher tracking velocity. In the second experiment this effect of velocity on the underestimation of distance was shown to exist only during ocular pursuit and not during steady fixation. The hypothesis that localization and estimation of distance during ocular pursuit share a common mechanism is discussed.     

Decrement of the Müller-Lyer illusion with saccadic and tracking eye movements

Subjects viewed the Müller-Lyer illusion, making either saccadic or smooth tracking eye movements between the apexes of the arrow heads. The decrement in the magnitude of the illusion was significantly greater for Ss in the saccadic viewing condition. Saccadic and smooth tracking eye movements are separately controlled,and information about eye position is more readily available from the efferent signals issued to control a saccadic eye movement. The experimental findings were consistent with the hypothesis that Ss in the saccadic condition learned a new afferent efferent association. The results support a theory that visual perception is determined by efferent readiness activated by visual afferent stimulation.     

Increased saccadic rate during smooth pursuit eye movements in patients at Ultra High Risk for developing a psychosis

Abnormalities in eye tracking are consistently observed in schizophrenia patients and their relatives and have been proposed as an endophenotype of the disease. The aim of this study was to investigate the performance of patients at Ultra High Risk (UHR) for developing psychosis on a task of smooth pursuit eye movement (SPEM). Forty-six UHR patients and twenty-eight age and education matched controls were assessed with a task of SPEM and psychiatric questionnaires. Our results showed that both the corrective and non-corrective saccadic rates during pursuit were higher in the UHR group. There were however no differences in smooth pursuit gain between the two groups. The saccadic rate was related to positive UHR symptoms. Our findings indicate that abnormalities in SPEM are already present in UHR patients, prior to a first psychotic episode. These abnormalities occur only in the saccadic system.     

Smooth pursuit eye movement and schizotypy in the community

Deficits in smooth pursuit eye movements are well documented in schizophrenia and schizotypic psychopathology. The status of eye tracking dysfunction (ETD) as an endophenotype for schizophrenia liability is relatively robust. However, the relation of ETD to schizophrenia-related deviance in the general population has not been confirmed. This study examined smooth pursuit eye tracking and schizotypal personality features in the general population. Smooth pursuit eye movement and schizotypal features were measured in 300 adult community subjects. The sample included both sexes, subjects with a wide age and educational range, and subjects with no prior history of psychosis. Primary outcome measures were peak gain (eye velocity/target velocity), catch-up saccade rate, and schizotypal feature scores. Total schizotypal features were significantly associated with decreased peak gain and were associated at the trend level with increased catch-up saccade rate. These associations were essentially unchanged after controlling for age, sex, and intellectual level effects. These data confirm a hypothesized association between schizotypal features and poorer eye tracking performance (principally, peak gain) in the general population as well as support the conceptualization of ETD as an endophenotype for schizophrenia liability.     

Auditory clicks distort perceived velocity but only when the system has to rely on extraretinal signals

Previous work has found that repetitive auditory stimulation (click trains) increases the subjective velocity of subsequently presented moving stimuli. We ask whether the effect of click trains is stronger for retinal velocity signals (produced when the target moves across the retina) or for extraretinal velocity signals (produced during smooth pursuit eye movements, when target motion across the retina is limited). In Experiment 1, participants viewed leftward or rightward moving single dot targets, travelling at speeds from 7.5 to 17.5 deg/s. They estimated velocity at the end of each trial. Prior presentation of auditory click trains increased estimated velocity, but only in the pursuit condition, where estimates were based on extraretinal velocity signals. Experiment 2 generalized this result to vertical motion. Experiment 3 found that the effect of clicks during pursuit disappeared when participants tracked across a visually textured background that provided strong local motion cues. Together these results suggest that auditory click trains selectively affect extraretinal velocity signals. This novel finding suggests that the cross-modal integration required for auditory click trains to influence subjective velocity operates at later stages of processing.     

A revised analysis of the role of efference in motion perception

The analysis of motion perception historically has included efferent as well as afferent mechanisms to account for the perception of motion during eye movement. The application of efferent mechanisms to motion perception has been limited, however, by several illusions which are apparently inconsistent with the notion that oculomotor mechanisms contribute to motion perception. An alternative account is presented of the manner in which efference may contribute to the perception of motion. It is proposed that distinct smooth eye-movement systems contribute differentially to object motion perception. Specifically, activity in the smooth pursuit system gives rise to the perception of object motion, whereas activity in the smooth component of reflexive eye movements does not. Tracking of a moving object results in object motion perception as a result of efference in the pursuit system. However, the pursuit system may be activated to oppose the smooth component of reflexive eye movements in order to preserve fixation on a stationary object. In such cases neither the fixated object nor the eye is moving but illusory movement results from the efference in the pursuit system. A number of illusory movement phenomena are interpreted in terms of this model.     

Parallel ocular and manual tracking responses to a continuously moving visual target

Continuous ocular and manual tracking of the same visual target moving horizontally in sinusoids at 0.75 Hz was measured by lag, RMS Error, and Gain. The best measures of accuracy of tracking, error and lag, were remarkably similar in the two systems and were affected similarly by presence of a background and changes in predictability of target movement. Details of within-system performance varied despite the over-all parallels. Gain was different in adjustment of proportion of saccadic to pursuit movement was affected by the presence of the hand, even though this did not affect tracking accuracy. The over-all parallel of response adjustment suggests that a suprasystem decision-maker sets general response goals and each motor system adjusts output details to match these goals.     

Manual coordination with intermittent targets: Velocity information for prospective control

Tracking a moving target requires that information concerning the current and future state of a target is available, allowing prospective control of the tracking effector. Eye movement research has shown that prospective visual tracking is achievable during conditions of both visible and occluded targets. The ability to track visually occluded targets has been interpreted as individuals integrating target velocity into eye movement motor plans. It has not been fully established that velocity plays a similar role in other types of tracking behavior. To examine whether target velocity is also used in manual tracking, numerical predictions and a validation experiment were conducted. Predictions indicated that, if individuals utilize target velocity during coordination, increases in visual occlusion periods should yield increased phase lag between target and hand, proportional to the occlusion period. Predictions also suggest that increased occlusion yields increased coordination variability. An experiment having participants coordinate with the same stimuli and occlusion conditions was conducted to verify the predictions. Comparison of prediction and experimental results provides strong agreement that individuals use target velocity to prospectively control coordinated movements.