Spatial integration in human smooth pursuit

When viewing a moving object, details may appear blurred if the object's motion is not compensated for by the eyes. Smooth pursuit is a voluntary eye movement that is used to stabilize a moving object. Most studies of smooth pursuit have used small, foveal targets as stimuli (e.g. Lisberger SG and Westbrook LE. J Neurosci 1985;5:1662-1673.). However, in the laboratory, smooth pursuit is poorer when a small object is tracked across a background, presumably due to a conflict between the primitive optokinetic reflex and smooth pursuit. Functionally, this could occur if the motion signal arising from the target and its surroundings were averaged, resulting in a smaller net motion signal. We asked if the smooth pursuit system could spatially summate coherent motion, i.e. if its response would improve when motion in the peripheral retina was in the same direction as motion in the fovea. Observers tracked random-dot cinematograms (RDC) which were devoid of consistent position cues to isolate the motion response. Either the height or the density of the display was systematically varied. Eye speed at the end of the open-loop period was greater for cinematograms than for a single spot. In addition, eye acceleration increased and latency decreased as the size of the aperture increased. Changes in the density produced similar but smaller effects on both acceleration and latency. The improved pursuit for larger motion stimuli suggests that neuronal mechanisms subserving smooth pursuit spatially average motion information to obtain a stronger motion signal.     

Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys

1. Our goal was to assess whether visual motion signals related to changes in image velocity contribute to pursuit eye movements. We recorded the smooth eye movements evoked by ramp target motion at constant speed. In two different kinds of stimuli, the onset of target motion provided either an abrupt, step change in target velocity or a smooth target acceleration that lasted 125 ms followed by prolonged target motion at constant velocity. We measured the eye acceleration in the first 100 ms of pursuit. Because of the 100-ms latency from the onset of visual stimuli to the onset of smooth eye movement, the eye acceleration in this 100-ms interval provides an estimate of the open-loop response of the visuomotor pathways that drive pursuit. 2. For steps of target velocity, eye acceleration in the first 100 ms of pursuit depended on the "motion onset delay," defined as the interval between the appearance of the target and the onset of motion. If the motion onset delay was > 100 ms, then the initial eye movement consisted of separable early and late phases of eye acceleration. The early phase dominated eye acceleration in the interval from 0 to 40 ms after pursuit onset and was relatively insensitive to image speed. The late phase dominated eye acceleration in the interval 40-100 ms after the onset of pursuit and had an amplitude that was proportional to image speed. If there was no delay between the appearance of the target and the onset of its motion, then the early component was not seen, and eye acceleration was related to target speed throughout the first 100 ms of pursuit. 3. For step changes of target velocity, the relationship between eye acceleration in the first 40 ms of pursuit and target velocity saturated at target speeds > 10 degrees /s. In contrast, the relationship was nearly linear when eye acceleration was measured in the interval 40-100 ms after the onset of pursuit. We suggest that the first 40 ms of pursuit are driven by a transient visual motion input that is related to the onset of target motion (motion onset transient component) and that the next 60 ms are driven by a sustained visual motion input (image velocity component). 4. When the target accelerated smoothly for 125 ms before moving at constant speed, the initiation of pursuit resembled that evoked by steps of target velocity. However, the latency of pursuit was consistently longer for smooth target accelerations than for steps of target velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys

Step-ramp target motion evokes a characteristic sequence of presaccadic smooth eye movement in the direction of the target ramp, catch-up targets to bring eye position close to the position of the moving target, and postsaccadic eye velocities that nearly match target velocity. I have analyzed this sequence of eye movements in monkeys to reveal a strong postsaccadic enhancement of pursuit eye velocity and to document the conditions that lead to that enhancement. Smooth eye velocity was measured in the last 10 ms before and the first 10 ms after the first saccade evoked by step-ramp target motion. Plots of eye velocity as a function of time after the onset of the target ramp revealed that eye velocity at a given time was much higher if measured after versus before the saccade. Postsaccadic enhancement of pursuit was recorded consistently when the target stepped 3 degrees eccentric on the horizontal axis and moved upward, downward, or away from the position of fixation. To determine whether postsaccadic enhancement of pursuit was invoked by smear of the visual scene during a saccade, I recorded the effect of simulated saccades on the presaccadic eye velocity for step-ramp target motion. The 3 degrees simulated saccade, which consisted of motion of a textured background at 150 degrees/s for 20 ms, failed to cause any enhancement of presaccadic eye velocity. By using a strategically selected set of oblique target steps with horizontal ramp target motion, I found clear enhancement for saccades in all directions, even those that were orthogonal to target motion. When the size of the target step was varied by up to 15 degrees along the horizontal meridian, postsaccadic eye velocity did not depend strongly either on the initial target position or on whether the target moved toward or away from the position of fixation. In contrast, earlier studies and data in this paper show that presaccadic eye velocity is much stronger when the target is close to the center of the visual field and when the target moves toward versus away from the position of fixation. I suggest that postsaccadic enhancement of pursuit reflects activation, by saccades, of a switch that regulates the strength of transmission through the visual-motor pathways for pursuit. Targets can cause strong visual motion signals but still evoke low presaccadic eye velocities if they are ineffective at activating the pursuit system.     

Properties of memory-guided saccades toward targets flashed during smooth pursuit in human subjects

PURPOSE: This study in human subjects investigated whether or not the saccade system can monitor smooth changes of the eye position in total darkness. METHODS: The authors studied the properties of memory-guided saccades toward targets flashed during pursuit eye movements (target velocities of 15 degrees/s, 30 degrees/s, and 45 degrees/s) in four normal human subjects. Subjects were instructed to execute memory-guided saccades toward the position of the flashed target in total darkness when the pursuit target was extinguished. RESULTS: The vector of the saccade was more highly correlated with the vector of "spatial error" (the vector from the position of the eye at the time of the saccade to the position of the flashed target in space) than with the vector of "retinal error" (the vector from the position of the eye at the time of the presentation of the flashed target to the position of the flashed target). The amplitude and direction errors of memory-guided saccades were correlated with the amplitude of the retinal error but not with amplitude of eye deviation after the presentation of the flashed target. Pursuit velocity did not affect the error of the saccade. CONCLUSIONS: These findings suggest that the saccade system can monitor smooth changes of the eye position in total darkness, regardless of the velocity of pursuit, and that the accuracy of memory-guided saccades is dependent only on the amplitude of the retinal error.     

Smooth pursuit eye movement deficits after pontine nuclei lesions in humans

Eye movements were recorded electroculographically in four patients with basal pontine lesions, demonstrated by MRI. The most prominent eye movement abnormality observed was mild to severe impairment of smooth pursuit and optokinetic nystagmus, mainly ipsilateral to the lesion. This abnormality is thought to result from damage to the pontine nuclei, which form a crucial relay between the cerebral cortex and the cerebellum controlling smooth pursuit. Abnormalities of saccades and the vestibulo-ocular reflex in one patient are also discussed.     

The relationship between curvature and velocity in two-dimensional smooth pursuit eye movements

Curvature and tangential velocity of voluntary hand movements are constrained by an empirical relation known as the Two-Thirds Power Law. It has been argued that the law reflects the working of central control mechanisms, but it is not known whether these mechanisms are specific to the hand or shared also by other types of movement. Three experiments tested whether the power law applies to the smooth pursuit movements of the eye, which are controlled by distinct neural motor structures and a peculiar set of muscles. The first experiment showed that smooth pursuit of elliptic targets with various curvature-velocity relationships was most accurate when targets were compatible with the Two-Thirds Power Law. Tracking errors in all other cases reflected the fact that, irrespective of target kinematics, eye movements tended to comply with the law. Using only compatible targets, the second experiment demonstrated that kinematics per se cannot account for the pattern of pursuit errors. The third experiment showed that two-dimensional performance cannot be fully predicted on the basis of the performance observed when the horizontal and vertical components of the targets used in the first condition were tracked separately. We conclude that the Two-Thirds Power Law, in its various manifestations, reflects neural mechanisms common to otherwise distinct control modules.     

The effect of the gap paradigm on the latency of human smooth pursuit of eye movement

When a temporal gap is introduced between the extinction of a central fixation target and the illumination of an eccentric target (the gap paradigm), normal human subjects initiate saccadic eye movements towards the eccentric target at lower latency than when there is no gap. The aim of this study was to examine the latency of human smooth pursuit eye movements using a modified gap paradigm. Smooth pursuit latency was reduced in gap tasks, and the magnitude of reduction was related to the duration of the gap. The distribution of smooth pursuit latencies was also altered. It thus appears that human smooth pursuit latency is modulated in a similar manner to saccade latency in gap tasks.     

Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation

We studied the eye movements evoked by applying small amounts of current (2-50 microA) within the oculomotor vermis of two monkeys. We first compared the eye movements evoked by microstimulation applied either during maintained pursuit or during fixation. Smooth, pursuitlike changes in eye velocity caused by the microstimulation were directed toward the ipsilateral side and occurred at short latencies (10-20 ms). The amplitudes of these pursuitlike changes were larger during visually guided pursuit toward the contralateral side than during either fixation or visually guided pursuit toward the ipsilateral side. At these same sites, microstimulation also often produced abrupt, saccadelike changes in eye velocity. In contrast to the smooth changes in eye velocity, these saccadelike effects were more prevalent during fixation and during pursuit toward the ipsilateral side. The amplitude and type of evoked eye movements could also be manipulated at single sites by changing the frequency of microstimulation. Increasing the frequency of microstimulation produced increases in the amplitude of pursuitlike changes, but only up to a certain point. Beyond this point, the value of which depended on the site and whether the monkey was fixating or pursuing, further increases in stimulation frequency produced saccadelike changes of increasing amplitude. To quantify these effects, we introduced a novel method for classifying eye movements as pursuitlike or saccadelike. The results of this analysis showed that the eye movements evoked by microstimulation exhibit a distinct transition point between pursuit and saccadelike effects and that the amplitude of eye movement that corresponds to this transition point depends on the eye movement behavior of the monkey. These results are consistent with accumulating evidence that the oculomotor vermis and its associated deep cerebellar nucleus, the caudal fastigial, are involved in the control of both pursuit and saccadic eye movements. We suggest that the oculomotor vermis might accomplish this role by altering the amplitude of a motor error signal that is common to both saccades and pursuit.     

Quantitative evaluation of saccadic and smooth pursuit eye movements. Is it reliable?

PURPOSE: The authors evaluated the reliability of the coefficients of the (1) amplitude/duration and (2) amplitude/peak velocity relationships of the mean precision values and the mean latency values (saccadic eye movements) and the coefficients of the target velocity/gain relationship (smooth pursuit eye movements). They computed test-retest maximum variability limits for these parameters. METHODS: After a 1-week interval, saccadic and smooth pursuit eye movements were recorded twice from 20 healthy subjects; 12 of these subjects underwent a third recording session. The estimate of the intraclass coefficient of reliability, R, was adopted to evaluate the reliability of eye movement quantitative analysis. RESULTS: The data demonstrated that the reliability was fairly good for the amplitude/peak velocity relationship, was good for the precision, and was excellent for the amplitude/duration, the target velocity/gain relationships, and the latency. CONCLUSIONS: Quantitative analysis of both saccadic and smooth pursuit eye movements is reliable. One statistic used to estimate reliability, ie, the within-subjects mean square value, also enables the determination of test-retest normal variability values for both the variances and the differences of measurements.     

Anticipatory saccades during smooth pursuit eye movements and familial transmission of schizophrenia

BACKGROUND: Smooth pursuit eye movement (SPEM) abnormalities are a putative marker of genetic risk for schizophrenia. Accurate SPEM performance requires the subject to activate neural systems responsible for smooth pursuit tracking, while simultaneously suppressing activity of neurons responsible for saccadic movements that would move the eye ahead of the target. This study examined whether specific aspects of SPEM dysfunction cosegregate with genetic risk in parents of schizophrenic probands. METHODS: Eighteen probands and their parents had SPEM recorded. Parents with an ancestral history of schizophrenia were hypothesized to be more likely than their spouses without such a history to carry a genetic risk for schizophrenia. RESULTS: Ten families had a single parent with a positive ancestral history for schizophrenia. The frequency of anticipatory saccades, which were mostly small, and the fraction of total eye movement that they represented were the only measures that differentiated the more likely genetic carrier parents in these families from their spouses and age-matched normals. CONCLUSIONS: Failure to suppress saccadic anticipation of target motion during smooth pursuit appears an aspect of SPEM dysfunction related to presumed genetic risk for schizophrenia.     

Study of non-visually induced smooth pursuit eye movements and their predictability using pseudorandom target motion

It has been found that the smooth pursuit eye movements (SPEM) are elicited by not only visual stimuli but also non-visual information such as the subject's fingertip movement and a moving sound source. We have already reported the quantitative analysis of SPEM which were induced by somatosensory and acoustic information. In the previous study, we used a sinusoidal waveform that could be highly predictable. Since it is wellknown that predictive control has an important role in the normal SPEM, we expect the predictive control to function in non-visually induced SPEM (NVSPEM). We quantitatively analyzed NVSPEM and normal SPEM evoked by pseudorandom target motion in ten human subjects who had no ocular, oculomotor or vestibular disorders. NVSPEM were induced by the following two non-visual targets: 1, subjects' fingertip motion as a somatosensory target ("Somato"), 2, a small loudspeaker (3-cm diameter.) generating white noise with an intensity of about 60 dB (A) as an acoustic target ("Acoustic"). A servo-controlled swing arm of 50cm was used to drive the subject's fingertip and the acoustic target of the small loudspeaker. The horizontal motion of the swing arm was controlled by a personal computer. The pseudorandom target motion was generated by mixing four sinusoids (0.1, 0.2, 0.4, 0.8 Hz) of which the phases were randomly selected and the peak velocities were equally set at 19 deg/s. The mean peak velocity of the target was 26.2 deg/s and the amplitude was limited within 15 deg. Horizontal eye movements were recorded by DC electro-oculography and on an analogue datatape. The experiment was performed for 30 s in complete darkness so that the subjects' fingertip and loudspeaker as such remain invisible to the subject. Signals from the data recorder were smoothed by a low pass analogue filter of 20Hz, after digitization with a sampling frequency of 200 Hz and precision of 12 bits, and stored on a computer. The slow and quick eye movement components, both of which were present in each class of horizontal eye movement investigated, were identified and separated by a computer. Then we developed a method of automatic quantitative analysis of ocular tracking eye movement. Gain and phase values for the smooth pursuit eye movements were obtained in each condition. In the lower frequency area, the gain elicited by the pseudorandom stimulation was lower than the smooth pursuit gain for sinusoidal (predictable) stimulation in all conditions. In the highest frequency, gain values did not differ significantly among the three. For the sinusoidal stimulation, the phase of the smooth component of "Visual" always had a lag and that of "Somato" and "Acoustic" had a lead in lower frequencies. All conditions had a phase shift, decreasing with increasing frequency. For the pseudorandom stimulation the phase of the SPEM had a lead only in the lowest frequency (0.1 Hz). On the other hand, in the NVSPEM the phases of the three lower frequencies had a lead which had a tendency of a larger phase lead with decreasingly frequency. In the highest frequency (0.8 Hz), we could see a short phase lag. These findings support the idea that SPEM and NVSPEM have a mutual or similar physiologic system and overlap part of the anatomical pathway.     

Smooth pursuit in 1- to 4-month-old human infants

The ability of human infants < or = 4 months of age to pursue objects smoothly with their eyes was assessed by presenting small target spots moving with hold-ramp-hold trajectories at ramp velocities of 4-32 deg/sec. Infants as young as 1 month old followed such target motions with a combination of smooth-pursuit and saccadic eye movements interrupted occasionally by periods when the eyes remained stationary. The slowest targets produced variable performance, but targets moving 8-32 deg/sec produced consistent pursuit behavior, even in the youngest infants. By the fourth month, eye-movement latency decreased and smooth-pursuit gain and the percentage of smooth pursuit per trial increased for all target velocities, though these measures had not yet reached adult levels.     

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°/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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Bilateral eye movements enhance the retrieval of episodic memories.

Two experiments examining effects of eye movements on episodic memory retrieval are reported. Thirty seconds of horizontal saccadic eye movements (but not smooth pursuit or vertical eye movements) preceding testing resulted in selective enhancement of episodic memory retrieval for laboratory (Experiment 1) and everyday (Experiment 2) events. Eye movements had no effects on implicit memory. Eye movements were also associated with more conservative response biases relative to a no eye movement condition. Episodic memory improvement induced by bilateral eye movements is hypothesized to reflect enhanced interhemispheric interaction, which is associated with superior episodic memory (S. D. Christman & R. E. Propper. 2001). Implications for neuropsychological mechanisms underlying eye movement desensitization and reprocessing (F. Shapiro, 1989, 2001), a therapeutic technique for posttraumatic stress disorder, are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effect of a moving distractor on the initiation of smooth-pursuit eye movements

As a step toward understanding the mechanism by which targets are selected for smooth-pursuit eye movements, we examined the behavior of the pursuit system when monkeys were presented with two discrete moving visual targets. Two rhesus monkeys were trained to select a small moving target identified by its color in the presence of a moving distractor of another color. Smooth-pursuit eye movements were quantified in terms of the latency of the eye movement and the initial eye acceleration profile. We have previously shown that the latency of smooth pursuit, which is normally around 100 ms, can be extended to 150 ms or shortened to 85 ms depending on whether there is a distractor moving in the opposite or same direction, respectively, relative to the direction of the target. We have now measured this effect for a 360 deg range of distractor directions, and distractor speeds of 5-45 deg/s. We have also examined the effect of varying the spatial separation and temporal asynchrony between target and distractor. The results indicate that the effect of the distractor on the latency of pursuit depends on its direction of motion, and its spatial and temporal proximity to the target, but depends very little on the speed of the distractor. Furthermore, under the conditions of these experiments, the direction of the eye movement that is emitted in response to two competing moving stimuli is not a vectorial combination of the stimulus motions, but is solely determined by the direction of the target. The results are consistent with a competitive model for smooth-pursuit target selection and suggest that the competition takes place at a stage of the pursuit pathway that is between visual-motion processing and motor-response preparation.     

Unilateral saccadic pursuit in patients with sensory stroke: sign of a pontine tegmentum lesion

BACKGROUND AND PURPOSE: Pure hemisensory syndrome can be caused by small strokes occurring in a number of regions, including the thalamus and pons. Differentiation of the pontine sensory syndrome from the thalamic sensory syndrome has generally been made on the basis of distribution of sensory loss and involvement of specific sensory modalities but not without uncertainties and difficulties. Because the pontine tegmentum plays a pivotal role in generating horizontal eye movement, we attempted to discriminate these 2 syndromes by analyzing horizontal eye movements in stroke patients with pure hemisensory syndrome. METHODS: Horizontal saccade, pursuit, vestibulo-ocular reflex (VOR), and VOR cancellation (VORC) were evaluated using electro-oculography in 6 patients with hemisensory syndromes, 3 due to pontine stroke and 3 due to thalamic stroke, and all were verified by MRI or CT. In addition, somatosensory evoked potentials (SEPs) were recorded. RESULTS: Smooth pursuit and VORC directed toward the side of the lesion were impaired unilaterally in patients with pontine sensory stroke, whereas those 2 movements were intact bilaterally in patients with thalamic sensory stroke. Saccade and VOR were preserved in all patients. SEPs were normal in all patients with pontine and thalamic sensory strokes. No difference was found in the pattern of sensory disturbance between the 2 types of stroke patients. CONCLUSIONS: Ipsilateral impairment of the smooth pursuit system may be a sign of a pontine lesion in patients with hemisensory stroke.     

Retinal masking during pursuit eye movements: Implications for spatiotopic visual persistence.

White (1976) reported that presentation of a masking stimulus during a pursuit eye movement interfered with the perception of a target stimulus that shared the same spatial, rather than retinal, coordinates as the mask. This finding has been interpreted as evidence for the existence of spatiotopic visual persistence. We doubted White's results because they implied a high degree of position constancy during pursuit eye movements, contrary to previous research, and because White did not monitor Ss' eye position during pursuit; if White's Ss did not make continuous pursuit eye movements, it might appear that masking was spatial when in fact it was retinal. We attempted to replicate White's results and found that when eye position was monitored to ensure that subjects made continuous pursuit movements, masking was retinal rather than spatial. Ss' phenomenal impressions also indicated that retinal, rather than spatial, factors underlay performance in this task. The implications of these and other results regarding the existence of spatiotopic visual persistence are discussed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Saccade amplitude influences pointing movement kinematics

The amplitude of open-loop pointing movements to step displacements in target position is influenced by the amplitude of simultaneously produced saccadic eye movements. The time course over which this occurs was addressed in the present study. Analysis of the pointing kinematics showed that saccade amplitude had its effect only during the initial acceleration of the hand. Moreover, the magnitude of the initial acceleration was correlated with the difference in the onset times of the eye and hand movements: the closer in time the saccadic and pointing responses were initiated the larger the initial hand acceleration. Taken together, these results demonstrate that saccades influence the kinematics of simultaneously produced limb movements but only over a limited time frame.