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.     

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.     

Directional organization of eye movement and visual signals in the floccular lobe of the monkey cerebellum

The floccular lobe of the monkey is critical for the generation of visually-guided smooth eye movements. The present experiments reveal physiological correlates of the directional organization in the primate floccular lobe by examining the selectivity for direction of eye motion and visual stimulation in the firing of individual Purkinje cells (PCs) and mossy fibers. During tracking of sinusoidal target motion along different axes in the frontoparallel plane, PCs fell into two classes based on the axis that caused the largest modulation of simple-spike firing rate. For "horizontal" PCs, the response was maximal during horizontal eye movements, with increases in firing rate during pursuit toward the side of recording (ipsiversive). For "vertical" PCs, the response was maximal during eye movement along an axis just off pure vertical, with increases in firing rate during pursuit directed downward and slightly contraversive. During pursuit of target motion at constant velocity, PCs again fell into horizontal and vertical classes that matched the results from sinusoidal tracking. In addition, the directional tuning of the sustained "eye velocity" and transient "visual" components of the neural responses obtained during constant velocity tracking were very similar. PCs displayed very broad tuning approximating a cosine tuning curve; the mean half-maximum bandwidth of their tuning curves was 170-180 degrees. Other cerebellar elements, related purely to eye movement and presumed to be mossy fibers, exhibited tuning approximately 40 degrees narrower than PCs and had best directions that clustered around the four cardinal directions. Our data indicate that the motion signals encoded by PCs in the monkey floccular lobe are segregated into channels that are consistent with a coordinate system defined by the vestibular apparatus and eye muscles. The differences between the tuning properties exhibited by PCs compared with mossy fibers indicate that a spatial transformation occurs within the floccular lobe.     

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.     

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)     

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

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.     

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)     

Eye movement impairment and schizotypal psychopathology

OBJECTIVE: Eye movement dysfunction in relation to a smooth pursuit task has been documented in schizophrenic patients and in patients with the related personality disorder, schizotypal personality disorder. To investigate which quantitative measures are associated with the eye movement dysfunction and whether the dysfunction is more related to the psychotic-like or the deficit-like symptoms of schizotypal personality disorder, ratings of eye movements in several groups of subjects were compared. METHOD: The study groups consisted of 26 patients with schizotypal personality disorder, 42 patients with other personality disorders (22 who also had two or more schizotypal personality traits and 20 who had fewer than two), and 37 normal comparison subjects. Smooth pursuit eye tracking of sinusoidal and constant velocity targets was recorded by an infrared eye tracking system. Two raters evaluated pursuit gain and large and small saccades in the direction of the target and in the direction opposite to that of the target (quantitative ratings) and constant velocity (qualitative rating). RESULTS: Patients with schizotypal personality disorder and patients with other personality disorders and two or more schizotypal traits, but not those with fewer than two schizotypal traits, had significantly poorer qualitative ratings of tracking than the normal comparison subjects. Neither gain nor any of the saccadic measures significantly differed between groups. The number of large saccades in the direction of the target was the only quantitative variable that predicted low qualitative ratings. Qualitatively poor tracking was associated with the deficit-like, but not the psychotic-like, symptoms of schizotypal personality disorder. CONCLUSIONS: Patients with schizotypal personality disorder demonstrate qualitatively poorer tracking than comparison groups, and the impaired tracking is associated with deficit-like symptoms.     

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)     

The Role of Stimulus-Driven and Goal-Driven Control in Saccadic Visual Selection.

Four experiments were conducted to investigate the role of stimulus-driven and goal-driven control in saccadic eye movements. Participants were required to make a speeded saccade toward a predefined target presented concurrently with multiple nontargets and possibly 1 distractor. Target and distractor were either equally salient (Experiments 1 and 2) or not (Experiments 3 and 4). The results uniformly demonstrated that fast eye movements were completely stimulus driven, whereas slower eye movements were goal driven. These results are in line with neither a bottom-up account nor a top-down notion of visual selection. Instead, they indicate that visual selection is the outcome of 2 independent processes, one stimulus driven and the other goal driven, operating in different time windows. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ocular responses to motion parallax stimuli: the role of perceptual and attentional factors

When human subjects are presented with visual displays consisting of random dots moving sideways at different velocities, they perceive transparent surfaces, moving in the same direction but located at different distances from themselves. They perceive depth from motion parallax, without any additional cues to depth, such as relative size, occlusion or binocular disparity. Simultaneously, large-field visual motion triggers compensatory eye movements which tend to offset such motion, in order to stabilize the visual image of the environment. In a series of experiments, we investigated how such reflexive eye movements are controlled by motion parallax displays, that is, in a situation where a complete stabilization of the visual image is never possible. Results show that optokinetic nystagmus, and not merely active visual pursuit of singular elements, is triggered by such displays. Prior to the detection of depth from motion parallax, eye tracking velocity is equal to the average velocity of the visual image. After detection, eye tracking velocity spontaneously matches the slowest velocity in the visual field, but can be controlled by attentional factors. Finally, for a visual stimulation containing more than three velocities, subjects are no longer able to perceptually dissociate between different surfaces in depth, and eye tracking velocity remains equal to the average velocity of the visual image. These data suggest that, in the presence of flow fields containing motion parallax, optokinetic eye movements are modulated by perceptual and attentional factors.     

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)     

The aftereffect of tracking eye movements

When observers tracked moving stripes across a background either of stationary stripes, or of stripes moving in the opposite direction, they saw a clear motion aftereffect when the stripes stopped moving. The direction of this aftereffect was opposite to that of the previously tracked stripes, and was thus the same as the direction of the retinal movement of the non-tracked stripes. This aftereffect of tracking was shown not to depend upon slippage of the tracked contours on the retina during tracking, or upon the saccadic phase of optokinetic nystagmus. The effect showed storage over a period of time with the eyes shut. It appears that the effect is due to induced movement, and arises originally from stimulation of the retina by background contours in the tracking phase. This was shown by confining the view of the moving target to one eye, while permitting both eyes to be exposed to background stimulation during tracking. After such stimulation the magnitude of the aftereffect was equal in the two eyes.     

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.     

When distractors and to-be-remembered items compete for the control of action: A new perspective on serial memory for spatial information.

In serial memory for spatial information, performance is impaired when distractors are interpolated between to-be-remembered (TBR) stimuli (Tremblay, Nicholls, Parmentier, & Jones, 2005). The so-called sandwich effect, combined with the use of eye tracking, served as a tool for examining the role of the oculomotor system in serial memory for spatial information. Participants had to recall the order in which sequences of TBR locations were presented. In some trials, to-be-ignored blue dots were presented after each TBR location. Our results show that response locations shift toward the location of the distractors, and this deviation is related to the eye movement deviation toward the distractor location. These results suggest that TBR and to-be-ignored locations are encoded onto a common map that could lie within the oculomotor system. Interference in memory for spatial information is interpreted in light of a model of oculomotor behavior (Godijn & Theeuwes, 2002b). (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Eye movements, prematurity and developmental co-ordination disorder

Horizontal pursuit eye movements were investigated in two separate groups of children: One group exhibited developmental co-ordination disorder (n = 8) whilst another group of children were born prematurely (n = 8). Both studies found a reduced gain in pursuit eye movements when the respective populations were compared with control groups (n = 32). A difference was also found in the ability of some children to temporally synchronize their tracking response to the stimulus, which was indicative of poor predictive control rather than lags in the control system. We suggest that horizontal eye movements may be a sensitive indicator of more general motor deficits during childhood development.     

Visual search for motion–form conjunctions: Is form discriminated within the motion system?

Motion-form conjunction search can be more efficient when the target is moving (a moving 45° tilted line among moving vertical and stationary 45° tilted lines) rather than stationary. This asymmetry may be due to aspects of form being discriminated within a motion system representing only moving items, whereas discrimination of stationary items relies on a static form system (J. Driver & P. McLeod, 1992). Alternatively, it may be due to search exploiting differential motion velocity and direction signals generated by the moving-target and distractor lines. To decide between these alternatives, 4 experiments systematically varied the motion-signal information conveyed by the moving target and distractors while keeping their form difference salient. Moving-target search was found to be facilitated only when differential motion-signal information was available. Thus, there is no need to assume that form is discriminated within the motion system. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Gaze perception requires focused attention: Evidence from an interference task.

The direction of another person's gaze is difficult to ignore when presented at the center of attention. In 6 experiments, perception of unattended gaze was investigated. Participants made directional (left-right) judgments to gazing-face or pointing-hand targets, which were accompanied by a distractor face or hand. Processing of the distractor was assessed via congruency effects on target response times. Congruency effects were found from the direction of distractor hands but not from the direction of distractor gazes (Experiment 1). This pattern persisted even when distractor sizes were increased to compensate for their peripheral presentation (Experiments 2 and 5). In contrast, congruency effects were exerted by profile heads (Experiments 3 and 4). In Experiment 6, isolated eye region distractors produced no congruency effects, even when they were presented near the target. These results suggest that, unlike other facial information, gaze direction cannot be perceived outside the focus of attention. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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.