Blink effects on ongoing smooth pursuit eye movements in humans

Blinks are known to affect eye movements, e.g., saccades, slow and fast vergence, and saccade-vergence interaction, in two ways: by superimposition of blink-associated eye movements and changes of the central premotor activity in the brainstem. The goal of this study was to determine, for the first time, the effects of trigeminal evoked blinks on ongoing smooth pursuit eye movements which could be related to visual sensory or premotor neuronal changes. This was compared to the effect of a target disappearing for 100–300 ms duration during ongoing smooth pursuit (blank paradigm) in order to control for the visual sensory effects of a blink. Eye and blink movements were recorded in eight healthy subjects with the scleral search coil technique. Blink-associated eye movements during the first 50% of the blink duration were non-linearly superimposed on the smooth pursuit eye movements. Immediately after the blink-associated eye movements, the pursuit velocity slowly decreased by an average of 3.2±2.1°/s. This decrease was not dependent on the stimulus direction. The pursuit velocity decrease caused by blinks which occluded the pupil more than 50% could be explained mostly by blanking the visual target. However, small blinks that did not occlude the pupil (<10% of lid closure) also decreased smooth pursuit velocity. Thus, this blink effect on pursuit velocity cannot be explained by blink-associated eye movements or by the blink having blanked the visual input. We propose that part of this effect might either be caused by incomplete visual suppression during blinks and/or a change in the activity of omnipause neurons.     

Cancelling of pursuit and saccadic eye movements in humans and monkeys

The countermanding paradigm provides a useful tool for examining the mechanisms responsible for cancelling eye movements. The key feature of this paradigm is that, on a minority of trials, a stop signal is introduced some time after the appearance of the target, indicating that the subject should cancel the incipient eye movement. If the delay in giving the stop signal is too long, subjects fail to cancel the eye movement to the target stimulus. By modeling this performance as a race between a go process triggered by the appearance of the target and a stop process triggered by the appearance of the stop signal, it is possible to estimate the processing interval associated with cancelling the movement. We have now used this paradigm to analyze the cancelling of pursuit and saccades. For pursuit, we obtained consistent estimates of the stop process regardless of our technique or assumptions--it took 50-60 ms to cancel pursuit in both humans and monkeys. For saccades, we found different values depending on our assumptions. When we assumed that saccade preparation was under inhibitory control up until movement onset, we found that saccades took longer to cancel (humans: approximately 110, monkeys: approximately 80 ms) than pursuit. However, when we assumed that saccade preparation includes a final "ballistic" interval not under inhibitory control, we found that the same rapid stop process that accounted for our pursuit results could also account for the cancelling of saccades. We favor this second interpretation because cancelling pursuit or saccades amounts to maintaining a state of fixation, and it is more parsimonious to assume that this involves a single inhibitory process associated with the fixation system, rather than two separate inhibitory processes depending on which type of eye movement will not be made. From our behavioral data, we estimate that this ballistic interval has a duration of 9-25 ms in monkeys, consistent with the known physiology of the final motor pathways for saccades, although we obtained longer values in humans (28-60 ms). Finally, we examined the effect of trial sequence during the countermanding task and found that pursuit and saccade latencies tended to be longer if the previous trial contained a stop signal than if it did not; these increases occurred regardless of whether the preceding trial was associated with the same or different type of eye movement. Together, these results suggest that a common inhibitory mechanism regulates the initiation of pursuit and saccades.     

An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans

Both optokinetic nystagmus (OKN) and smooth-pursuit eye movements (SPEM) are subclasses of so-called slow eye movements. However, optokinetic responses are reflexive whereas smooth pursuit requires the voluntary tracking of a moving target. We used functional magnetic resonance imaging (fMRI) to determine the neural basis of OKN and SPEM, and to uncover whether the two underlying neural systems overlap or are independent at the cortical level. The results showed a largely overlapping neural circuitry. A direct comparison between activity during the execution of OKN and SPEM yielded no oculomotor-related area exclusively dedicated to one or the other eye movement type. Furthermore, the performance of SPEM evoked a bilateral deactivation of the human equivalent of the parietoinsular vestibular cortex. This finding might indicate that the reciprocally inhibitory visual–vestibular interaction involves not only OKN but also SPEM, which are both linked with the encoding of object-motion and self-motion. Moreover, we could show differential activation patterns elicited by look-nystagmus and stare-nystagmus. Look-nystagmus is characterized by large amplitudes and low-frequency resetting eye movements rather resembling SPEM. Look-nystagmus evoked activity in cortical oculomotor centers. By contrast, stare-nystagmus is usually characterized as being more reflexive in nature and as showing smaller amplitudes and higher frequency resetting eye movements. Stare-nystagmus failed to elicit significant signal changes in the same regions as look-nystagmus/SPEM. Thus, less reflexive eye movements correlated with more pronounced signal intensity. Finally, on the basis of a general investigation of slow eye movements, we were interested in a cortical differentiation between subtypes of SPEM. We compared activity associated with predictable and unpredictable SPEM as indicated by appropriate visual cues. In general, predictable and unpredictable SPEM share the same neural network, yet information about the direction of an upcoming target movement reduced the cerebral activity level.     

Object motion computation for the initiation of smooth pursuit eye movements in humans

Pursuing an object with smooth eye movements requires an accurate estimate of its two-dimensional (2D) trajectory. This 2D motion computation requires that different local motion measurements are extracted and combined to recover the global object-motion direction and speed. Several combination rules have been proposed such as vector averaging (VA), intersection of constraints (IOC), or 2D feature tracking (2DFT). To examine this computation, we investigated the time course of smooth pursuit eye movements driven by simple objects of different shapes. For type II diamond (where the direction of true object motion is dramatically different from the vector average of the 1-dimensional edge motions, i.e., VA not equal IOC = 2DFT), the ocular tracking is initiated in the vector average direction. Over a period of less than 300 ms, the eye-tracking direction converges on the true object motion. The reduction of the tracking error starts before the closing of the oculomotor loop. For type I diamonds (where the direction of true object motion is identical to the vector average direction, i.e., VA = IOC = 2DFT), there is no such bias. We quantified this effect by calculating the direction error between responses to types I and II and measuring its maximum value and time constant. At low contrast and high speeds, the initial bias in tracking direction is larger and takes longer to converge onto the actual object-motion direction. This effect is attenuated with the introduction of more 2D information to the extent that it was totally obliterated with a texture-filled type II diamond. These results suggest a flexible 2D computation for motion integration, which combines all available one-dimensional (edge) and 2D (feature) motion information to refine the estimate of object-motion direction over time.     

Smooth pursuit eye movements in children

Smooth pursuit eye movements consists of slow eye movements that approximate the velocity of the eyes to that of a small moving target, so that target image is kept at or near the fovea. Little information on smooth pursuit is available in children. We used an infrared eye tracker to record smooth pursuit in 38 typically developing children, aged 8–19 years. Participants followed a visual target moving sinusoidally at ±10° amplitude, horizontally and vertically at 0.25 or 0.5 Hz. The mean horizontal smooth pursuit gains, the ratio of eye to target velocities, were 0.84 at 0.25 Hz and 0.73 at 0.5 Hz. Mean vertical smooth pursuit gains were 0.68 at 0.25 Hz and 0.45 at 0.5 Hz. Smooth pursuit gains were significantly lower for vertical in comparison to horizontal tracking, and for 0.5 Hz in comparison to 0.25 Hz tracking (P<0.0001). Smooth pursuit gains increased with age (P<0.01, Pearson’s correlation tests), with horizontal gains attaining reported adult values by mid adolescence. Vertical gains had large variability among participants. The median phase, the time interval between eye and target velocities, varied between 39 and 86 ms. Phase was not influenced by age. We conclude that smooth pursuit gains are lower in children than gains reported in adults. Vertical pursuit gain is significantly lower than horizontal pursuit gain. Gains improve with age and approach adult values in mid adolescence. Children have larger phases than reported adults values indicating that prediction in the smooth pursuit system is less mature in children.     

Visuo-motor pathways in humans revealed by event-related fMRI

Whether different brain networks are involved in generating unimanual responses to a simple visual stimulus presented in the ipsilateral versus contralateral hemifield remains a controversial issue. Visuo-motor routing was investigated with event-related functional magnetic resonance imaging (fMRI) using the Poffenberger reaction time task. A 2 hemifield x 2 response hand design generated the "crossed" and "uncrossed" conditions, describing the spatial relation between these factors. Both conditions, with responses executed by the left or right hand, showed a similar spatial pattern of activated areas, including striate and extrastriate areas bilaterally, SMA, and M1 contralateral to the responding hand. These results demonstrated that visual information is processed bilaterally in striate and extrastriate visual areas, even in the "uncrossed" condition. Additional analyses based on sorting data according to subjects' reaction times revealed differential crossed versus uncrossed activity only for the slowest trials, with response strength in infero-temporal cortices significantly correlating with crossed-uncrossed differences (CUD) in reaction times. Collectively, the data favor a parallel, distributed model of brain activation. The presence of interhemispheric interactions and its consequent bilateral activity is not determined by the crossed anatomic projections of the primary visual and motor pathways. Distinct visuo-motor networks need not be engaged to mediate behavioral responses for the crossed visual field/response hand condition. While anatomical connectivity heavily influences the spatial pattern of activated visuo-motor pathways, behavioral and functional parameters appear to also affect the strength and dynamics of responses within these pathways.     

Smooth pursuit eye movements elicited by somatosensory stimulation

Smooth pursuit eye movements approaching the qualitative and quantitative characteristics of those elicited by a moving visual target were obtained in complete darkness with a moving tactile stimulus. Pursuit eye movements in response to tactile stimulation have longer latencies to onset and to offset of pursuit, are more often interrupted by saccades, and provide less accurate stimulus localization than those in response to moving visual stimuli. The evocation of pursuit eye movements by a somatosensory input suggests that within the appropriate velocity domain a spatially changing sensory input from any modality may be sufficient to elicit ocular pursuit.     

Smooth pursuit eye movements to isoluminant targets

At slow speeds, chromatic isoluminant stimuli are perceived to move much slower than comparable luminance stimuli. We investigated whether smooth pursuit eye movements to isoluminant stimuli show an analogous slowing. Beside pursuit speed and latency, we studied speed judgments to the same stimuli during fixation and pursuit. Stimuli were either large sine wave gratings or small Gaussians blobs moving horizontally at speeds between 1 and 11 degrees /s. Targets were defined by luminance contrast or color. Confirming prior studies, we found that speed judgments of isoluminant stimuli during fixation showed a substantial slowing when compared with luminance stimuli. A similarly strong and significant effect of isoluminance was found for pursuit initiation: compared with luminance targets of matched contrasts, latencies of pursuit initiation were delayed by 50 ms at all speeds and eye accelerations were reduced for isoluminant targets. A small difference was found between steady-state eye velocities of luminance and isoluminant targets. For comparison, we measured latencies of saccades to luminance and isoluminant stimuli under similar conditions, but the effect of isoluminance was only found for pursuit. Parallel psychophysical experiments revealed that different from speed judgments of moving isoluminant stimuli made during fixation, judgments during pursuit are veridical for the same stimuli at all speeds. Therefore information about target speed seems to be available for pursuit eye movements and speed judgments during pursuit but is degraded for perceptual speed judgments during fixation and for pursuit initiation.     

Detection of speed changes during pursuit eye movements

The human visual system is strikingly insensitive to speed changes attributed to the need to infer visual acceleration, observed during stationary fixation, indirectly by comparing velocities integrated over time. The objective of this study was to test if smooth pursuit eye movements improve the detection of speed changes. This was expected for two reasons: first, pursuit reduces the retinal image slip velocity, leading to smaller Weber fractions for velocity changes; secondly, pursuit provides acceleration-dependent retinal position cues unavailable during stationary fixation such as displacements of the target image away from the fovea due to unexpected changes in target velocity. In a first set of experiments thresholds for just noticeable speed changes were measured in ten healthy human subjects confronted with a horizontally moving target, changing its velocity unpredictably during its ramp-like movement. During stationary fixation, the Weber fraction averaged 0.13 for a starting velocity of the target being 15°/s. Smooth pursuit of the same target significantly reduced the Weber fraction down to 0.08. In a second set of experiments, the discrimination of speed changes was tested in patients (n=10) with pursuit disturbances characterized by increased retinal image slip and unidirectional retinal image displacements. These patients showed a strong perceptual bias to report speed increments and an insensitivity to speed decrements. We argue that this asymmetry is a necessary consequence of a mechanism exploiting retinal position errors for the detection of speed change, confronted with directionally biased errors due to the pursuit impairment. In summary, the detection of speed changes is facilitated by pursuit eye movements but is highly susceptible to pursuit insufficiencies.     

Mixture analysis of smooth pursuit eye movements in schizophrenia

The goal of this study was to replicate and extend previous findings indicating that the eye movement data of schizophrenic patients is best represented by the mixture of two groups, one of which has distinctly poor performance. Forty-nine schizophrenic patients and 32 normal controls had their smooth pursuit eye movements quantified by calculating the root mean square (RMS) deviation between the target and eye waveforms. Based on the finding of mixture in the distribution of RMS error, the patients were divided in to low (better tracking) and high (worse tracking) RMS error subgroups. The high RMS error patient had abnormally decreased gain. Both patient subgroups had abnormally increased frequency of catch-up saccades and increased phase lag. Distinguishing between these two subgroups may be useful in clarifying the pathophysiology of abnormal pursuit and its relationship to heterogeneity in schizophrenia.     

Saccadic and smooth pursuit eye movements in the monkey

1. Voluntary eye movements were measured in the chronic, unanaesthetized monkey. A training technique is described which conditions the animals to follow a large variety of target trajectories.2. The eye movements of the monkey are not qualitatively different from those of man. In response to random target motions the monkey also employs a combination of saccadic and smooth pursuit movements.3. Monkeys execute their saccades more rapidly than humans.4. Monkeys are capable of attaining smooth pursuit velocities which are twice as fast as those of man.5. Most of the critical experiments showing the separate nature of the saccadic and smooth pursuit modes in man have been performed on monkeys with similar results.6. Therefore, if one remains aware of the quantitative differences between the two primates, results of neurophysiological studies of the occulomotor system of the monkey can be expected to have considerable relevance when extrapolated to man.     

Learning on multiple timescales in smooth pursuit eye movements

We commonly think of motor learning as a gradual process that makes small, adaptive steps in a consistent direction. We now report evidence that learning in pursuit eye movements could start with large, transient short-term alterations that stoke a more gradual long-term process. Monkeys tracked a target that started moving horizontally or vertically. After 250 ms of motion had produced a preinstruction eye velocity close to target velocity, an orthogonal component of target motion created an instructive change in target direction that was randomly in one of the two directions along the orthogonal axis. The preinstruction eye velocity in each trial expressed single-trial learning as a bias toward the direction of the instruction in the prior trial. The single-trial learning was forgotten within 4 to 10 s. Two observations implied that single-trial learning was not simply cognitive anticipation. First, the magnitude of the trial-over-trial change in eye velocity depended on the ongoing eye velocity at the time of the instruction in the prior trial. Single-trial learning was negligible if the prior trial had provided a well-timed cue without evoking any preinstruction eye velocity. Second, regular alternation of the direction of the instructive target motion caused reactive rather than anticipatory trial-over-trial changes in eye velocity. Humans showed very different responses that appeared to be based on cognitive anticipation rather than learning. We suggest that single-trial learning results from a low-level learning mechanism and may be a necessary prerequisite for longer-term modifications that are more permanent.     

Improved visual sensitivity during smooth pursuit eye movements

When we view the world around us, we constantly move our eyes. This brings objects of interest into the fovea and keeps them there, but visual sensitivity has been shown to deteriorate while the eyes are moving. Here we show that human sensitivity for some visual stimuli is improved during smooth pursuit eye movements. Detection thresholds for briefly flashed, colored stimuli were 16% lower during pursuit than during fixation. Similarly, detection thresholds for luminance-defined stimuli of high spatial frequency were lowered. These findings suggest that the pursuit-induced sensitivity increase may have its neuronal origin in the parvocellular retino-thalamic system. This implies that the visual system not only uses feedback connections to improve processing for locations and objects being attended to, but that a whole processing subsystem can be boosted. During pursuit, facilitation of the parvocellular system may reduce motion blur for stationary objects and increase sensitivity to speed changes of the tracked object.     

Target selection for predictive smooth pursuit eye movements

Previous work has indicated that after exposure to a moving stimulus, people are able to produce predictive smooth eye movements prior to reappearance of the stimulus. Here, we investigated whether subjects are able to extract relevant velocity information from two simultaneously presented targets and use this information to produce a subsequent predictive response. A trial consisted of a series of two or five presentations of moving stimuli, preceded 500 ms earlier by an audio warning cue. In the first one or four presentations, subjects fixated during the presentation of two moving targets and in the final presentation they tracked a single moving target. During fixation, two moving targets were presented concurrently, originating from the fixation point and moving horizontally to the right at differing velocities (10, 20, 30 or 40°/s), with each target being presented at the same velocity throughout a trial. In the tracking presentation, the fixation cross was extinguished and only a single target was presented, which the subjects were required to track with their eyes. To cue which of the two targets would be presented, the appropriate target was presented statically at the same time as the audio warning cue. A significant relationship was found between eye velocity 100 ms after the start of the tracking target (i.e. prior to visual feedback) and the cued target velocity. Thus, subjects were able to make predictive eye movements that were of appropriate velocity for the cued target, despite fixating and being uncertain which target was relevant, during previous exposure.     

Perceived motion direction during smooth pursuit eye movements

Although many studies have been devoted to motion perception during smooth pursuit eye movements, relatively little attention has been paid to the question of whether the compensation for the effects of these eye movements is the same across different stimulus directions. The few studies that have addressed this issue provide conflicting conclusions. We measured the perceived motion direction of a stimulus dot during horizontal ocular pursuit for stimulus directions spanning the entire range of 360 degrees. The stimulus moved at either 3 or 8 degrees/s. Constancy of the degree of compensation was assessed by fitting the classical linear model of motion perception during pursuit. According to this model, the perceived velocity is the result of adding an eye movement signal that estimates the eye velocity to the retinal signal that estimates the retinal image velocity for a given stimulus object. The perceived direction depends on the gain ratio of the two signals, which is assumed to be constant across stimulus directions. The model provided a good fit to the data, suggesting that compensation is indeed constant across stimulus direction. Moreover, the gain ratio was lower for the higher stimulus speed, explaining differences in results in the literature.     

Judging object velocity during smooth pursuit eye movements

Our tendency to constantly shift our gaze and to pursue moving objects with our eyes introduces obvious problems for judging objects' velocities. The present study examines how we deal with these problems. Specifically, we examined when information on rotations (such as eye movements) is obtained from retinal, and when from extra-retinal sources. Subjects were presented with a target moving across a textured background. Moving the background allowed us to manipulate the retinal information on rotation independently of the extra-retinal information. The subjects were instructed to pursue the target with their eyes. At some time during the presentation the target's velocity could change. We determined how various factors influence a subject's perception of such changes in velocity. Under more or less natural conditions, there was no change in perceived target velocity as long as the relative motion between target and background was maintained. However, experiments using conditions that are less likely to occur outside the laboratory reveal how extra-retinal signals are involved in velocity judgements.     

Frontal eye field lesions impair predictive and visually-guided pursuit eye movements

Summary The study initially explored the frontal eye field's (FEF) control of predictive eye movements, i.e., eye movements driven by previous rather than current sensory signals. Five monkeys were trained to pursue horizontal target motion, including sinusoidal targets and random-walk targets which sometimes deviated from a sine motion. Some subjects also tracked other target trajectories and optokinetic motion. FEF ablations or cold lesions impaired predictive pursuit, but also degraded visually guided foveal pursuit of all targets. Unilateral lesions impaired pursuit of targets moving in both horizontal orbital fields and in both directions of movement. Saccadic estimates of target motion were generally accurate. The slow-phase velocity of optokinetic pursuit (collected after 54 s of OKN) also appeared normal. Pursuit recovered over 1–3 weeks after surgery but the deficits were then reinstated by removal of FEF in the other hemisphere. Thereafter, a slight deficit persisted for up to 10 weeks of observation in two subjects. The pattern of symptoms suggests that FEF lies subsequent to parietal area MST and prior to the pontine nuclei in controlling pursuit eye movements.