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)     

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)     

Neuronal responses in visual areas MT and MST during smooth pursuit target selection

We recorded the activity of single neurons in the middle temporal (MT) and middle superior temporal (MST) visual areas in two macaque monkeys while the animals performed a smooth pursuit target selection task. The monkeys were presented with two moving stimuli of different colors and were trained to initiate smooth pursuit to the stimulus that matched the color of a previously given cue. We designed these experiments so that we could separate the component of the neuronal response that was driven by the visual stimulus from an extraretinal component that predicted the color or direction of the selected target. We found that for all cells in MT and MST the response was primarily determined by the visual stimulus. However, 14% (8 of 58) of MT neurons and 26% (22 of 84) of MST neurons had a small predictive component that was significant at the P < or = 0.05 level. In some cells, the predictive component was clearly related to the color of the intended target, but more often it was correlated with the direction of the target. We have previously documented a systematic shift in the latency of smooth pursuit that depends on the relative direction of motion of the two stimuli. We found that neither the latency nor the amplitude of neuronal responses in MT or MST was correlated with behavioral latency. These results are consistent with a model for target selection in which a weak selection bias for the intended target is amplified by a competitive network that suppresses motion signals related to the nonintended stimulus. It is possible that the predictive component of neuronal responses in MT and MST contributes to the selection bias. However, the strength of the selection bias in MT and MST is not sufficient to account for the high degree of selectivity shown by pursuit behavior.     

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.     

Prediction of complex two-dimensional trajectories by a cerebellar model of smooth pursuit eye movement

A neural network model based on the anatomy and physiology of the cerebellum is presented that can generate both simple and complex predictive pursuit, while also responding in a feedback mode to visual perturbations from an ongoing trajectory. The model allows the prediction of complex movements by adding two features that are not present in other pursuit models: an array of inputs distributed over a range of physiologically justified delays, and a novel, biologically plausible learning rule that generated changes in synaptic strengths in response to retinal slip errors that arrive after long delays. To directly test the model, its output was compared with the behavior of monkeys tracking the same trajectories. There was a close correspondence between model and monkey performance. Complex target trajectories were created by summing two or three sinusoidal components of different frequencies along horizontal and/or vertical axes. Both the model and the monkeys were able to track these complex sum-of-sines trajectories with small phase delays that averaged 8 and 20 ms in magnitude, respectively. Both the model and the monkeys showed a consistent relationship between the high- and low-frequency components of pursuit: high-frequency components were tracked with small phase lags, whereas low-frequency components were tracked with phase leads. The model was also trained to track targets moving along a circular trajectory with infrequent right-angle perturbations that moved the target along a circle meridian. Before the perturbation, the model tracked the target with very small phase differences that averaged 5 ms. After the perturbation, the model overshot the target while continuing along the expected nonperturbed circular trajectory for 80 ms, before it moved toward the new perturbed trajectory. Monkeys showed similar behaviors with an average phase difference of 3 ms during circular pursuit, followed by a perturbation response after 90 ms. In both cases, the delays required to process visual information were much longer than delays associated with nonperturbed circular and sum-of-sines pursuit. This suggests that both the model and the eye make short-term predictions about future events to compensate for visual feedback delays in receiving information about the direction of a target moving along a changing trajectory. In addition, both the eye and the model can adjust to abrupt changes in target direction on the basis of visual feedback, but do so after significant processing delays.     

Saccade latency toward auditory targets depends on the relative position of the sound source with respect to the eyes

The latency of saccadic eye movements evoked by the presentation of auditory and visual targets was studied while starting eye position was either 0 or 20 deg right, or 20 deg left. The results show that for any starting position the latency of visually elicited saccades increases with target eccentricity with respect to the eyes. For auditory elicited saccades and for any starting position the latency decreases with target eccentricity with respect to the eyes. Therefore auditory latency depends on a retinotopic motor error, as in the case of visual target presentation.     

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.     

Specific phosphatidylethanolamine dependence of Serratia marcescens cytotoxin activity

A region of dorsomedial frontal cortex (DMFC) has been implicated in planning and executing saccadic eye movements; hence it has been referred to as a supplementary eye field (SEF). Recently, activity related to executing smooth-pursuit eye movements has been recorded from the DMFC, and microstimulation here has been shown to evoke smooth eye movements. This report documents neuronal activity present in smooth-pursuit tasks where the predictability of target motion was manipulated. The activity of many neurons in the DMFC reached a peak when a predictable change in target motion occurred. Furthermore, the peak activity of some cells was systematically shifted by manipulating the duration of the target event, indicating that the network these neurons were in could learn the temporal characteristics of new target motion. Finally, the activity of most neurons tested was greater when target motion was predictable than when it was unpredictable. The results suggest that the DMFC participates in planning smooth-pursuit eye movements based on past stimulus history.     

Smooth-pursuit eye movements: A comparison of two measurement techniques for studying schizophrenia.

Conducted simultaneous recording of smooth-pursuit eye movements by EOG and infrared reflection techniques with 5 psychiatric patients (1 with psychotic depression, 1 with organic brain syndrome, and 3 with schizophrenia) and 5 normal controls. Results show good correspondence between the 2 methods. The parameter of pursuit arrests, previously used to quantify smooth-pursuit performance, was not well correlated in the 2 methods. The natural logarithm of the signal/noise ratio obtained from harmonic regression of digitized and standardized eye movement data provides a valid quantitative assessment of smooth pursuit and suggests that such scoring of EOG records is effective and generally free of artifacts. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A note on formal learning theory

Previous investigations have challenged the generality of the claim that perceived motion in an effective stimulus for smooth pursuit eye movements. The experiments extend the scope of these investigations. Three experiments test the hypothesis that perceived motion can serve as the stimulus for pursuit when the eye movement does not generate constraining retinal error information. Observers viewed retinally stabilized displays that elicited the perception that a stationary target was moving or that a moving target was moving faster than it was actually moving. The results failed to confirm the hypothesis. Relevant literature is reviewed. We conclude that perceived movement can act as a stimulus for pursuit only when the "perceptual target" has no retinal counterpart.     

Eye-hand coordination: Oculomotor control in rapid aimed limb movements.

Three experiments are reported in which Ss produced rapid wrist rotations to a target while the position of their eyes was being monitored. In Experiment 1, Ss spontaneously executed a saccadic eye movement to the target around the same time as the wrist began to move. Experiment 2 revealed that wrist-rotation accuracy suffered if Ss were not allowed to move their eyes to the target, even when visual feedback about the moving wrist was unavailable. In Experiment 3, wrist rotations were equally accurate when Ss produced either a saccadic or a smooth-pursuit eye movement to the target. However, differences were observed in the initial-impulse and error-correction phases of the wrist rotations, depending on the type of eye movement involved. The results suggest that aimed limb movements use information from the oculomotor system about both the static position of the eyes and the dynamic characteristics of eye movements. Furthermore, the information that governs the initial impulse is different from that which guides final error corrections. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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.     

Passover and plague

Patients with unilateral neglect following right hemisphere damage may have difficulty in moving towards contralesional targets. To test the hypothesis that this impairment arises from competing motor programs triggered by irrelevant ipsilesional stimuli, we examined 16 right hemisphere patients, eight with left visual neglect and eight without, in addition to eight healthy control subjects. In experiment 1 subjects performed sequences of movements using their right hand to targets on the contralesional or ipsilesional side of the responding limb. The locations of successive targets in each sequence were either predictable or unpredictable. In separate blocks of trials, targets appeared either alone or with a simultaneous distractor located at the immediately preceding target location. Neglect patients were significantly slower to execute movements to contralesional targets, but only for unpredictable movements and in the presence of a concurrent ipsilesional distractor. In contrast, healthy controls and right hemisphere patients without neglect showed no directional asymmetries of movement execution. In experiment 2 subjects were required to interrupt a predictable, reciprocating sequence of leftward and rightward movements in order to move to an occasional, unpredictable target that occurred either in the direction opposite to that expected, or in the same direction but twice the extent. Neglect patients were significantly slower in reprogramming the direction and extent of movements towards contralesional versus ipsilesional targets, and they also made significantly more errors when executing such movements. Right hemisphere patients without neglect showed a similar bias in reprogramming direction (but not extent) for contralesional targets, whereas healthy controls showed no directional asymmetry in either condition. On the basis of these findings we propose that neglect involves a competitive bias in favour of motor programs for actions directed towards ipsilesional versus contralesional events. We suggest that programming errors and increased latencies for contralesional movements arise because the damaged right hemisphere can no longer effectively inhibit the release of inappropriate motor programs towards ipsilesional events.     

Attentional capture and aging: Implications for visual search performance and oculomotor control.

Two studies examined potential age-related differences in attentional capture. Subjects were instructed to move their eyes as quickly as possible to a color singleton target and to identify a small letter located inside it. On half the trials, a new stimulus (i.e., a sudden onset) appeared simultaneously with the presentation of the color singleton target. The onset was always a task-irrelevant distractor. Response times were lengthened, for both young and old adults, whenever an onset distractor appeared, despite the fact that Ss reported being unaware of the appearance of the abrupt onset. Eye scan strategies were also disrupted by the appearance of the onset distractors. On about 40% of the trials on which an onset appeared, Ss made an eye movement to the task-irrelevant onset before moving their eyes to the target. Fixations close to the onset were brief, suggesting parallel programming of a reflexive eye movement to the onset and goal-directed eye movement to the target. Results are discussed in terms of age-related sparing of the attentional and oculomotor processes that underlie attentional capture. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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.     

Attentional capture of objects referred to by spoken language.

Participants saw a small number of objects in a visual display and performed a visual detection or visual-discrimination task in the context of task-irrelevant spoken distractors. In each experiment, a visual cue was presented 400 ms after the onset of a spoken word. In experiments 1 and 2, the cue was an isoluminant color change and participants generated an eye movement to the target object. In experiment 1, responses were slower when the spoken word referred to the distractor object than when it referred to the target object. In experiment 2, responses were slower when the spoken word referred to a distractor object than when it referred to an object not in the display. In experiment 3, the cue was a small shift in location of the target object and participants indicated the direction of the shift. Responses were slowest when the word referred to the distractor object, faster when the word did not have a referent, and fastest when the word referred to the target object. Taken together, the results demonstrate that referents of spoken words capture attention. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Delayed retinal feedback of eye movements: A dynamic basis of perceptual disabilities.

Investigated temporal factors in vision in relation to the delay of the retinal feedback of ocular movements in eye tracking. A hybrid real-time computer system and dynamic programing methods were used to calibrate photoelectric eye-movement transducers in viewing visual targets, to yoke these targets to eye motion, to introduce feedback delays in eye-movement-retinal interaction, and to measure error in eye tracking. Results indicate that feedback delay affected the accuracy of both the compensatory and the pursuit tracking in a significant way, with a somewhat greater effect being found for pursuit movements. Since delay reduced smooth pursuit motions to saccadic reactions that varied in size with the delay interval, it is suggested that ocular dynamics and guidance in space perception are governed by time-specific neuron mechanisms of the central visual system. Findings negate classical theory of ocular dynamics and perception of direction by proving that directional guidance of the eyes is determined by directional specificity and temporal specificity of the feedback processes of pursuit and saccadic movements of the eyes and is not caused primarily by learned temporal association between visual and tactual sensory processes. It is concluded that major disabilities and distortions in vision, which are not reducible to traditionally defined optometric and ophthalmologic factors, may be produced by built-in developmental perturbations of ocular feedback timing. Findings emphasize dynamic optometric measurements in understanding common and elusive distortions of visual perception. (19 ref.) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Detection of cortical activities on eye movement using functional magnetic resonance imaging

Cortical activity during eye movement was examined with functional magnetic resonance imaging. Horizontal saccadic eye movements and smooth pursuit eye movements were elicited in normal subjects. Activity in the frontal eye field was found during both saccadic and smooth pursuit eye movements at the posterior margin of the middle frontal gyrus and in parts of the precentral sulcus and precentral gyrus bordering the middle frontal gyrus (Brodmann's areas 8, 6, and 9). In addition, activity in the parietal eye field was found in the deep, upper margin of the angular gyrus and of the supramarginal gyrus (Brodmann's areas 39 and 40) during saccadic eye movement. Activity of V5 was found at the intersection of the ascending limb of the inferior temporal sulcus and the lateral occipital sulcus during smooth pursuit eye movement. Our results suggest that functional magnetic resonance imaging is useful for detecting cortical activity during eye movement.