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.     

Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position

Anatomical and physiological studies have shown that the "frontal pursuit area" (FPA) in the arcuate cortex of monkeys is involved in the control of smooth pursuit eye movements. To further analyze the signals carried by the FPA, we examined the activity of pursuit-related neurons recorded from a discrete region near the arcuate spur during a variety of oculomotor tasks. Pursuit neurons showed direction tuning with a wide range of preferred directions and a mean full width at half-maximum of 129 degrees. Analysis of latency using the "receiver operating characteristic" to compare responses to target motion in opposite directions showed that the directional response of 58% of FPA neurons led the initiation of pursuit, while 19% led by 25 ms or more. Analysis of neuronal responses during pursuit of a range of target velocities revealed that the sensitivity to eye velocity was larger during the initiation of pursuit than during the maintenance of pursuit, consistent with two components of firing related to image motion and eye motion. FPA neurons showed correlates of two behavioral features of pursuit documented in prior reports. 1) Eye acceleration at the initiation of pursuit declines as a function of the eccentricity of the moving target. FPA neurons show decreased firing at the initiation of pursuit in parallel with the decline in eye acceleration. This finding is consistent with prior suggestions that the FPA plays a role in modulating the gain of visual-motor transmission for pursuit. 2) A stationary eccentric cue evokes a smooth eye movement opposite in direction to the cue and enhances the pursuit evoked by subsequent target motions. Many pursuit neurons in the FPA showed weak, phasic visual responses for stationary targets and were tuned for the positions about 4 degrees eccentric on the side opposite to the preferred pursuit direction. However, few neurons (12%) responded during the preparation or execution of saccades. The responses to the stationary target could account for the behavioral effects of stationary, eccentric cues. Further analysis of the relationship between firing rate and retinal position error during pursuit in the preferred and opposite directions failed to provide evidence for a large contribution of image position to the firing of FPA neurons. We conclude that FPA processes information in terms of image and eye velocity and that it is functionally separate from the saccadic frontal eye fields, which processes information in terms of retinal image position.     

Oculomotor prediction of accelerative target motion during occlusion: long-term and short-term effects

The present study examined the influence of long-term (i.e., between-trial) and short-term (i.e., within-trial) predictive mechanisms on ocular pursuit during transient occlusion. To this end, we compared ocular pursuit of accelerative and decelerative target motion in trials that were presented in random or blocked-order. Catch trials in which target acceleration was unexpectedly modified were randomly interleaved in blocked-order trials. Irrespective of trial order, eye velocity decayed following target occlusion and then recovered towards the different levels of target velocity at reappearance. However, the recovery was better scaled in blocked-order trials than random-order trials. In blocked-order trials only, the reduced gain of smooth pursuit during occlusion was compensated by a change in saccade amplitude and resulted in total eye displacement (TED) that was well matched to target displacement. Subsidiary analysis indicated that three repeats of blocked-order trials was sufficient for participants to modify eye displacement compared to that exhibited in random-order trials, although more trials were required before end-occlusion eye velocity was better scaled. Finally, we found that participants exhibited evidence of a scaled response to an unexpected change in target acceleration (i.e., catch trials), although there were also transfer effects from the preceding blocked-order trials. These findings are consistent with the suggestion that on-the-fly prediction (short-term effect) is combined with memorised information from previous trials (long-term effect) to generate a persistent and veridical prediction of occluded target motion.     

Visual motion processing for the initiation of smooth-pursuit eye movements in humans

We have used the initiation of pursuit eye movements as a tool to reveal properties of motion processing in the neural pathways that provide inputs to the human pursuit system. Horizontal and vertical eye position were recorded with a magnetic search coil in six normal adults. Stimuli were provided by individual trials of ramp target motion. Analysis was restricted to the first 100 ms of eye movement, which precedes the onset of corrective feedback. By recording the transient response to target motion at speeds the pursuit motor system can achieve, we investigated the visual properties of images that initiate pursuit. We have found effects of varying the retinal location, the direction, the velocity, the intensity, and the size of the stimulus. Eye acceleration in the first 100 ms of pursuit depended on both the direction of target motion and the initial position of the moving target. For horizontal target motion, eye acceleration was highest if the stimulus was close to the center of the visual field and moved toward the vertical meridian. For vertical target motion, eye acceleration was highest when the stimulus moved upward or downward within the lower visual field. The shape of the relationship between eye acceleration and initial target position was similar for target velocities ranging from 1.0 to 45 degrees/s. The initiation of pursuit showed two components that had different visual properties and were expressed early and late in the first 100 ms of pursuit. In the first 20 ms, instantaneous eye acceleration was in the direction of target motion but did not depend on other visual properties of the stimulus. At later times (e.g., 80-100 ms after pursuit initiation), instantaneous eye acceleration was strongly dependent on each property we tested. Targets that started close to and moved toward the position of fixation evoked the highest eye accelerations. For high-intensity targets, eye acceleration increased steadily as target velocity increased. For low-intensity targets, eye acceleration was selective for target velocities of 30-45 degrees/s. The properties of pursuit initiation in humans, including the differences between the early and late components, are remarkably similar to those reported by Lisberger and Westbrook (12) in monkeys. Our data provide evidence that the cell populations responsible for motion processing are similar in humans and monkeys and imply that the functional organization of the visual cortex is similar in the two species.     

Differential effects of blinks on horizontal saccade and smooth pursuit initiation in humans

Blinks executed during eye movements affect kinetic eye movement parameters, e.g., peak velocity of saccades is decreased, their duration is increased, but their amplitude is not altered. This effect is mainly explained by the decreased activity of premotor neurons in the brainstem: omni-pause neurons (OPN) in the nucleus raphe interpositus. Previous studies examined the immediate effect of blinks directly on eye movements but not their effect when they are elicited several hundred milliseconds before the eye movements. In order to address this question we tested blinks elicited before the target onset of saccades and pursuit and compared the results to the gap effect: if a fixation light is extinguished for several hundred milliseconds, the reaction time (latency) for subsequent saccades or smooth pursuit eye movements is decreased. Monocular eye and lid movements were recorded in nine healthy subjects using the scleral search-coil system. Laser stimuli were front-projected onto a tangent screen in front of the subjects. Horizontal step-ramp smooth pursuit of 20 deg/s was elicited in one session, or 5 deg horizontal visually guided saccades in another experimental session. In one-third of the trials (smooth pursuit or saccades) the fixation light was extinguished for 200 ms before stimulus onset (gap condition), and in another third of the trials reflexive blinks were elicited by a short airpuff before the stimulus onset (blink condition). The last third of the trials served as controls (control condition). Stimulus direction and the three conditions were randomized for saccades and smooth pursuit separately. The latency of the step-ramp smooth pursuit in the blink condition was found to be decreased by 10 ms, which was less than in the gap condition (38 ms). However, the initial acceleration and steady-state velocity of smooth pursuit did not differ in the three conditions. In contrast, the latency of the saccades in the gap condition was decreased by 39 ms, but not in the blink condition. Saccade amplitude, peak velocity, and duration were not different in the three conditions. There was also no difference in blink amplitude and duration of pupil occlusion in the blink condition, neither in saccades nor in smooth pursuit. The latency reduction of smooth pursuit, but not of saccades, may neither be explained by the brief pupil occlusion nor by visual suppression, warning signals, or the startle response. Whether the effects are caused by the influence of blinks on OPNs or other premotor structures remains to be tested.     

Apparent motion produces multiple deficits in visually guided smooth pursuit eye movements of monkeys

We used apparent motion targets to explore how degraded visual motion alters smooth pursuit eye movements. Apparent motion targets consisted of brief stationary flashes with a spatial separation (Deltax), temporal separation (Deltat), and apparent target velocity equal to Deltax/Deltat. Changes in pursuit initiation were readily observed when holding target velocity constant and increasing the flash separation. As flash separation increased, the first deficit observed was an increase in the latency to peak eye acceleration. Also seen was a paradoxical increase in initial eye acceleration. Further increases in the flash separation produced larger increases in latency and resulted in decreased eye acceleration. By varying target velocity, we were able to discern that the visual inputs driving pursuit initiation show both temporal and spatial limits. For target velocities above 4-8 degrees /s, deficits in the initiation of pursuit were seen when Deltax exceeded 0.2-0.5 degrees, even when Deltat was small. For target velocities below 4-8 degrees /s, deficits appeared when Deltat exceeded 32-64 ms, even when Deltax was small. Further experiments were designed to determine whether the spatial limit varied as retinal and extra-retinal factors changed. Varying the initial retinal position of the target for motion at 18 degrees /s revealed that the spatial limit increased as a function of retinal eccentricity. We then employed targets that increased velocity twice, once from fixation and again during pursuit. These experiments revealed that, as expected, the spatial limit is expressed in terms of the flash separation on the retina. The spatial limit is uninfluenced by either eye velocity or the absolute velocity of the target. These experiments also demonstrate that "initiation" deficits can be observed during ongoing pursuit, and are thus not deficits in initiation per se. We conclude that such deficits result from degradation of the retino-centric motion signals that drive pursuit eye acceleration. For large flash separations, we also observed deficits in the maintenance of pursuit: sustained eye velocity failed to match the constant apparent target velocity. Deficits in the maintenance of pursuit depended on both target velocity and Deltat and did not result simply from a failure of degraded image motion signals to drive eye acceleration. We argue that such deficits result from a low gain in the eye velocity memory that normally supports the maintenance of pursuit. This low gain may appear because visual inputs are so degraded that the transition from fixation to tracking is incomplete.     

Combined smooth and saccadic ocular pursuit during the transient occlusion of a moving visual object

Accurate ocular pursuit during a transient occlusion interval would minimize retinal position and velocity error, and could provide an advantage when discriminating object characteristics at reappearance. This study was designed to examine how the smooth and saccadic response extrapolates the trajectory of a moving visual object during a transient occlusion. We confirmed that subjects could not maintain unity gain smooth pursuit during the transient occlusion. Eye velocity decayed significantly without visual feedback but then in the majority of subjects, there was a recovery that brought eye velocity back towards object velocity. However, eye velocity did not increase to a level that eliminated the developing position error. Subjects corrected for the resulting error in eye position by releasing saccades that generally placed the eye ahead of the occluded object’s extrapolated position. The majority of saccadic correction occurred between 220 and 600 ms of the occlusion interval, and when combined with the smooth response enabled accurate pursuit of a 10°/s object for up to 1,200 ms of occlusion. The lack of saccadic correction after 600 ms of occlusion combined with the reduced eye velocity resulted in significant undershoot of eye position at the moment of object reappearance when pursuing an 18°/s object. We suggest that extra-retinal information regarding eye velocity and smooth eye displacement could be available from a continually updating efference copy of eye motion in MST, whereas a veridical representation of extrapolated object velocity and displacement could be obtained from persistent activity in FEF.     

Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes

1. We have identified a visually driven output from the flocculus of the monkey by studying the simple-spike responses of Purkinje cells (P-cells) during the initiation of smooth-pursuit eye movements. We report on two groups of P-cells that appear to be the horizontal and vertical gaze-velocity P-cells (GVP-cells) studied previously during periodic target and head motion. 2. During pursuit of periodic target motion, one group of P-cells prefers downward motion (down GVP-cells), and the other prefers motion toward the side of recording (ipsi GVP-cells). The two groups have mean directional preferences that are nearly orthogonal, but their responses during pursuit of sinusoidal target motion and sinusoidal vestibular stimulation are in other respects quantitatively similar. 3. During the initiation of pursuit to step-ramp target motion, GVP-cells show a large transient change in simple-spike firing rate followed by a sustained change in firing that persists during steady-state pursuit. 4. The transient response is directionally selective, so that GVP-cells show a pulse of simple spikes for pursuit in the ON-direction and a dip in simple-spike firing for pursuit in the OFF-direction. The amplitude of the transient response is too large to be explained by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 5. To test whether the transient change in simple-spike firing was related to a visual input or to an eye-acceleration input to the flocculus, we recorded the firing of ipsi GVP-cells during a rapid eye acceleration caused by a transient vestibular stimulus in darkness. Most GVP-cells showed little or no transient response under these conditions, even though eye acceleration was greater than during the initiation of pursuit. We conclude that the transient response at the initiation of pursuit is probably caused by visual mossy-fiber inputs to the flocculus. 6. The sustained change in simple-spike firing is also directionally selective, with large increases in simple-spike firing for pursuit in the ON-direction and smaller decreases for pursuit in the OFF-direction. For pursuit in the ON-direction, the amplitude of the sustained response is well predicted by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 7. To determine whether the sustained response was driven by visual inputs, we recorded simple-spike firing when image motion was prevented by electronically stabilizing the target image on the fovea during steady-state pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)     

Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields.

The role of the supplementary eye fields (SEF) during smooth pursuit was investigated with electrical microstimulation. We found that stimulation in the SEF increased the acceleration and velocity of the eyes in the direction of target motion during smooth pursuit initiation but not during sustained pursuit. The increase in eye velocity during initiation will be referred to as pursuit facilitation and was observed at sites where saccades could not be evoked with the same stimulation parameters. On average, electrical stimulation increased eye velocity by approximately 20%. At most sites, the threshold for a significant facilitation was 50 microA with a stimulation frequency of 300 Hz. Facilitation of pursuit initiation depended on the timing of stimulation trains. The effect was most pronounced if the stimulation was delivered before smooth pursuit initiation. On average, eye velocity in stimulation trials increased linearly as a function of eye velocity in control trials, and this function had a slope greater than one, suggesting a multiplicative influence of the stimulation. Stimulation during a fixation task did not evoke smooth eye movements. The latency of catch-up saccades was increased during facilitation, but their accuracy was not affected. Saccades toward stationary targets were not affected by the stimulation. The results are further evidence that the SEF plays a role in smooth pursuit in addition to its known role in saccade planning and suggest that this role may be to control the gain of smooth pursuit during initiation. The covariance between pursuit facilitation and the timing of the catch-up saccade as a result of stimulation suggests that these different eye movements systems are coordinated to achieve a common goal.     

The influence of stationary and moving textured backgrounds on smooth-pursuit initiation and steady state pursuit in humans

 We investigated the effects of stationary and moving textured backgrounds on the initiation and steady state of ocular pursuit using horizontally moving targets. We found that the initial eye acceleration was slightly reduced when a stationary textured background was employed, as compared to experiments with a homogeneous background. When a moving textured background was introduced, the initial eye acceleration was significantly larger when the target and the background moved in opposite directions than when the target and the background moved in the same direction. The use of stationary and moving textured backgrounds resulted in comparable effects on the initial eye acceleration when they were presented either as a large field or as a narrow, horizontal small field, only covering the trajectory of the target. Moreover, small-field stationary backgrounds slightly reduced the eye velocity during steady state pursuit. A small-field background moving in the opposite direction to the target distinctly reduced eye velocity, while a target and a background moving in the same direction sometimes even improved pursuit performance, when compared with a homogeneous background. The influences of small-field textured backgrounds on steady state pursuit were comparable with those of large-field backgrounds in both stationary and moving conditions. Received: 14 December 1996 / Accepted: 30 December 1996     

Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey.

1. We have investigated the mechanism of a directional deficit in vertical pursuit eye movements in a monkey that was unable to match upward eye speed to target speed but that had pursuit within the normal range for downward or horizontal target motion. Except for a difference in the axis of deficient pursuit, the symptoms in this monkey were similar to those seen with lesions in the frontal or parietal lobes of the cerebral cortex in humans or monkeys. Our evaluation of vertical pursuit in this monkey suggests a new interpretation for the role of the frontal and parietal lobes in pursuit. 2. The up/down asymmetry was most pronounced for target motion at speeds greater than or equal to 2 degree/s. For target motion at 15 or 30 degree/s, upward step-ramp target motion evoked a brief upward smooth eye acceleration, followed by tracking that consisted largely of saccades. Downward step-ramp target motion evoked a prolonged smooth eye acceleration, followed by smooth, accurate tracking. 3. Varying the amplitude of the target step revealed that the deficit was similar for targets moving across all locations of the visual field. Eye acceleration in the interval 0-20 ms after the onset of pursuit was independent of initial target position and was symmetrical for upward and downward target motion. Eye acceleration in the interval 60-80 ms after the onset of pursuit showed a large asymmetry. For upward target motion, eye acceleration in this interval was small and did not depend on initial target position. For downward target motion, eye acceleration depended strongly on initial target position and was large when the target started close to the position of fixation. 4. We next attempted to understand the mechanism of the up/down asymmetry by evaluating the monkey's vertical motion processing and vertical eye movements under a variety of tracking conditions. For spot targets, the response to upward image motion was similar to that in normal monkeys if the image motion was presented during downward pursuit. In addition, the monkey with deficient upward pursuit was able to use upward image motion to make accurate saccades to moving targets. We conclude that the visual processing of upward image motion was normal in this monkey and that an asymmetry in visual motion processing could not account for the deficit in his upward pursuit. 5. Upward smooth eye acceleration was normal when the spot target was moved together with a large textured pattern.(ABSTRACT TRUNCATED AT 400 WORDS)     

Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements

Eye movement deficits caused by ocular muscle weakness vary according to the position of the eye in the orbit and the direction of eye movement. We studied the ability of both the saccadic and pursuit eye-movement systems to compensate for these anisotropic deficits in four patients with ocular muscle weakness. The eye-position dependence of each patient's motor deficit was characterized by plotting the position of the weak eye against that of the normal eye (in various orbital positions) when fusion was prevented, thus giving a static eye-position curve from which relative muscle strength could be inferred. Movements of the weak eye were smaller and slower than those made by the normal eye, so that the weak eye required more time to acquire a visual target. When patients were forced to view monocularly with their weak eye for several days, both the saccadic and pursuit systems showed changes in the movements of the normal eye consistent with an increased central innervation designed to decrease the time it takes to bring the target's image onto the fovea of the weak eye and to keep it there. These adaptive changes varied with eye position and movement direction and compensated for the weak muscle in both its agonistic and antagonistic actions. Saccadic adaptation consisted of a change in the relationship between saccadic amplitude and retinal error (distance between the target's image and the fovea) to compensate for hypometria (undershoot) and a readjustment of the ratio of the phasic (pulse) and tonic (step) components of the saccadic innervation to suppress postsaccadic ocular drift. Pursuit adaptation consisted of an increase in the relationship between eye acceleration and the rate of motion of the image of the target on the retina during the initial phase of tracking as well as an increase in the velocity during tracking of a target moving at a constant velocity. These changes reflect an increase in pursuit innervation that would cause the weak eye's velocity to approach target velocity sooner. The average acceleration of the normal eye during the initial period of tracking (130 ms) increased by as much as threefold. The corresponding maximum smooth eye velocity increased so that, for example, the pursuit response to a 15 degree/s target movement could be over 50 degree/s in the normal eye.     

Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control

This study examined the extent to which human subjects predict future target motion for the control of smooth ocular pursuit. Subjects were required to pursue an accelerating target (0, 4 or 8 degrees/s2) that underwent a transient occlusion, and consequently reappeared with the same or increased velocity. Presentations were received in a random or blocked order. Subjects exhibited anticipatory smooth pursuit prior to target motion onset, which in blocked presentations was scaled to the velocity generated by the target acceleration. In random presentations subjects also exhibited anticipatory smooth pursuit, but this was reflected in a more generalized response. During the transient occlusion all subjects exhibited a reduction in eye velocity, which was followed in the majority by a recovery prior to target reappearance. In random presentations, eye velocity decayed and recovered to a level that followed on from the response to the initial ramp. In blocked presentations, there was evidence of improved scaling throughout, which culminated in a significant increase in eye velocity between the start and end of the transient occlusion (8 degrees/s2 only). These findings are difficult to reconcile with reflexive accounts of oculomotor control that perpetuate current eye motion, and hence generate a simple form of prediction using a direct efference copy ("eye-velocity memory"). Rather, they are more consistent with the scaling of smooth pursuit eye movements by means of a more-persistent velocity-based representation, which plays a significant role in both random and blocked stimulus presentations.     

Role of retinal slip in the prediction of target motion during smooth and saccadic pursuit

Visual tracking of moving targets requires the combination of smooth pursuit eye movements with catch-up saccades. In primates, catch-up saccades usually take place only during pursuit initiation because pursuit gain is close to unity. This contrasts with the lower and more variable gain of smooth pursuit in cats, where smooth eye movements are intermingled with catch-up saccades during steady-state pursuit. In this paper, we studied in detail the role of retinal slip in the prediction of target motion during smooth and saccadic pursuit in the cat. We found that the typical pattern of pursuit in the cat was a combination of smooth eye movements with saccades. During smooth pursuit initiation, there was a correlation between peak eye acceleration and target velocity. During pursuit maintenance, eye velocity oscillated at approximately 3 Hz around a steady-state value. The average gain of smooth pursuit was approximately 0.5. Trained cats were able to continue pursuing in the absence of a visible target, suggesting a role of the prediction of future target motion in this species. The analysis of catch-up saccades showed that the smooth-pursuit motor command is added to the saccadic command during catch-up saccades and that both position error and retinal slip are taken into account in their programming. The influence of retinal slip on catch-up saccades showed that prediction about future target motion is used in the programming of catch-up saccades. Altogether, these results suggest that pursuit systems in primates and cats are qualitatively similar, with a lower average gain in the cat and that prediction affects both saccades and smooth eye movements during pursuit.     

Target acceleration can be extracted and represented within the predictive drive to ocular pursuit

Given sufficient exposure to stimulus presentation, the oculomotor system generates a representation of the stimulus characteristics, which is then used to predict the upcoming target motion. In addition to compensating for the perceptual-motor delay, these predictive processes perpetuate eye motion during a transient occlusion and compensate for the loss of visual input. At present, however, it is not well understood whether and how the oculomotor system extracts and represents target acceleration for subsequent predictive control. To this end, we used a target occlusion paradigm where both position and velocity of the target during the occlusion and at reappearance could not be predicted without extracting target acceleration before target disappearance. We found that the oculomotor response during the blanking period was not influenced by target acceleration when the initial exposure was 200 ms. However, smooth and saccadic eye movements did discriminate between the different levels of acceleration after an initial 500- or 800-ms exposure. In the event that the smooth response during the occlusion did not match well the target trajectory and thus eliminate a developing displacement error, there was an increased saccadic displacement. Still, the combined response during the blanking period did not eliminate retinal slip and position error at target reappearance. These results indicate that information on target acceleration can be extracted on-line, during pursuit of a visible ramp, and then used to drive a predictive oculomotor response in the absence of visual input.     

Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit

We studied the effects on smooth pursuit eye movements of ablation of the dorsal cerebellar vermis (lesions centered on lobules VI and VII) in three monkeys in which the cerebellar nuclei were spared. Following the lesion the latencies to pursuit initiation were unchanged. Monkeys showed a small decrease (up to 15%) in gain during triangular-wave tracking. More striking were changes in the dynamic properties of pursuit as determined in the open-loop period (the 1st 100 ms) of smooth tracking. Changes included a decrease in peak eye acceleration (e.g., in one monkey from approximately 650 degrees /s(2), prelesion to approximately 220-380 degrees /s(2), postlesion) and a decrease in the velocity at the end of the open-loop period [e.g., in another monkey from a gain (eye velocity/target velocity at 100 ms of tracking) of 0.93, prelesion to 0.53, postlesion]. In individual monkeys, the pattern of deficits in the open-loop period of pursuit was usually comparable to that of saccades, especially when comparing the changes in the acceleration of pursuit to the changes in the velocity of saccades. These findings support the hypothesis that saccades and the open-loop period of pursuit are controlled by the cerebellar vermis in an analogous way. Saccades could be generated by eye velocity commands to bring the eyes to a certain position and pursuit by eye acceleration commands to bring the eyes toward a certain velocity. On the other hand, changes in gain during triangular-wave tracking did not correlate with either the saccade or the open-loop pursuit deficits, implying different contributions of the oculomotor vermis to the open loop and to the sustained portions of pursuit tracking. Finally, in a pursuit adaptation paradigm (x0.5 or x2, calling for a halving or doubling of eye velocity, respectively) intact animals could adaptively adjust eye acceleration in the open-loop period. The main pattern of change was a decrease in peak acceleration for x0.5 training and an increase in the duration of peak acceleration for x2 training. Following the lesion in the oculomotor vermis, this adaptive capability was impaired. In conclusion, as for saccades, the oculomotor vermis plays a critical role both in the immediate on-line and in the short-term adaptive control of pursuit.     

Contextual effects on smooth-pursuit eye movements

Segregating a moving object from its visual context is particularly relevant for the control of smooth-pursuit eye movements. We examined the interaction between a moving object and a stationary or moving visual context to determine the role of the context motion signal in driving pursuit. Eye movements were recorded from human observers to a medium-contrast Gaussian dot that moved horizontally at constant velocity. A peripheral context consisted of two vertically oriented sinusoidal gratings, one above and one below the stimulus trajectory, that were either stationary or drifted into the same or opposite direction as that of the target at different velocities. We found that a stationary context impaired pursuit acceleration and velocity and prolonged pursuit latency. A drifting context enhanced pursuit performance, irrespective of its motion direction. This effect was modulated by context contrast and orientation. When a context was briefly perturbed to move faster or slower eye velocity changed accordingly, but only when the context was drifting along with the target. Perturbing a context into the direction orthogonal to target motion evoked a deviation of the eye opposite to the perturbation direction. We therefore provide evidence for the use of absolute and relative motion cues, or motion assimilation and motion contrast, for the control of smooth-pursuit eye movements.     

Modulation of pursuit eye movements by stimulation of cortical areas MT and MST

1. Many cells in the superior temporal sulcus (STS) of the monkey that represent the foveal region of the visual field discharge during pursuit eye movements. Damage to these areas produces a deficit in the maintenance of pursuit eye movements when the target towards the side of the brain with the lesion. In the present experiments, we electrically stimulated these areas to better localize and understand the mechanisms underlying this directional pursuit deficit. 2. Monkeys were trained to pursue a moving target using a step-ramp task in which the target first stepped to an eccentric position and then moved smoothly across the screen. Trains of stimulation were applied after the monkey had begun to pursue the target to study stimulation effects of maintenance of pursuit. 3. Stimulation during pursuit frequently produced eye acceleration toward the side of the brain stimulated. Eye speed increased during pursuit toward the side stimulated and decreased during pursuit away from the side stimulated. This increase in velocity toward the side of the brain where stimulation presumably activated cells is consistent with the decrease in pursuit velocity toward the side of the brain after cells were removed by chemical lesions. 4. The increase or decrease in pursuit speed following stimulation produced a slip of the target on the retina. The pursuit system seemed to be insensitive to this slip during the period of stimulation, however, since the effect of stimulation during pursuit of a stabilized image (open-loop condition) was similar to that resulting from stimulation under normal pursuit conditions (closed-loop). This insensitivity to visual motion during stimulation suggests that the stimulation substitutes for that visual input. 5. The separation of eye and target position that resulted from stimulation did produce catch-up saccades. This provides added evidence that alteration of middle temporal area (MT) and medial superior temporal area (MST) modifies visual-motion but not visual-position information. 6. Stimulation that produced eye acceleration during pursuit produced only a slight effect during fixation of a stationary target. The effectiveness of the stimulation also increased as the speed of the pursuit increased between 5 and 25 degrees/s. These observations, which show that pursuit velocity altered the effect of stimulation, suggest that the stimulation acted on visual motion processing before information about the pursuit movement itself is incorporated. Since this stimulation produces directional pursuit effects, we hypothesize that the directional bias for pursuit originates in the visual signal conveyed to the pursuit system.(ABSTRACT TRUNCATED AT 400 WORDS)     

Topographic and directional organization of visual motion inputs for the initiation of horizontal and vertical smooth-pursuit eye movements in monkeys

1. The goal of our study was to determine the properties of the visual inputs for pursuit eye movements. In a previous study we presented horizontal target motion along the horizontal meridian and showed that targets were more effective if they moved across the center of the visual field. We have now analyzed the topographic weighting of the inputs for pursuit in greater detail, using targets that moved in all directions and across a wide area of the visual field. 2. Monkeys were rewarded for tracking targets that started at 48 positions in the visual field. The initial positions were spaced equally around 4 circles that were centered at the position of fixation and had radii of 3, 6, 9, and 12 degrees. Targets moved horizontally or vertically at 30 degrees/s. We measured the smooth eye acceleration in the first 80 ms after the initiation of pursuit, before there had been time for visual feedback to affect the position or velocity of the retinal images from the target. 3. For both horizontal and vertical target motion, there were major differences between the early and late intervals in the first 80 ms of pursuit. In the first 20 ms eye acceleration was largely independent of initial target position. In later intervals eye acceleration decreased sharply as a function of initial target eccentricity. The later intervals also showed a pronounced toward/away asymmetry such that the initiation of pursuit was more vigorous for target motion toward than for motion away from the horizontal or vertical meridian. 4. Comparison of the topographic organization of the middle temporal visual area (MT) with our data on pursuit suggests that the topography of cortical maps is smoothed when the visual signals are transmitted to the pursuit system. For example, the superior visual hemifield is underrepresented in cortical motion processing areas, but target motion in the superior and inferior visual hemifields is equally effective for the initiation of pursuit. 5. We investigated the directional organization of the visual inputs for pursuit by presenting targets that started at 6 degrees eccentric and moved in 16 different directions. Horizontal target motion always evoked larger eye accelerations than did vertical target motion. Target motion in oblique directions evoked intermediate values of eye acceleration. 6. Our data show two classes of variation in pursuit performance. First, some subjects showed ideosyncratic variations that were restricted to one hemifield or one direction of target motion. We attribute these variations to differences among subjects in the physiology of visual pathways.(ABSTRACT TRUNCATED AT 400 WORDS)     

A non-visual mechanism for voluntary cancellation of the vestibulo-ocular reflex

Summary Squirrel monkeys were trained to cancel their vestibulo-ocular reflex (VOR) by fixating a visual target that was head stationary during passive vestibular stimulation. The monkeys were seated on a vestibular turntable, and their heads were restrained. A small visual target (0.2°) was projected from the vestibular turntable onto a tangent screen. The monkeys' ability to suppress their VOR by fixating a head stationary target while the turntable was moving was compared to their ability to pursue the target when it was moved in the same manner.Squirrel monkeys were better able to suppress their VOR when the turntable was moved at high velocities than they were able to pursue targets that were moving at high velocities. The gaze velocity gain during VOR cancellation began to decrease when the head velocity was above 80°/s, and was greater than 0.6 when the head velocity was above 150°/s. However, gaze velocity gain during smooth pursuit decreased significantly when the target velocity was greater than 60°/s, and was less than 0.4 when the target velocity was 150°/s or more.The latency of VOR suppression was significantly shorter than the latency of smooth pursuit while the monkey was cancelling its VOR. When an unpredictable step change in head acceleration was generated while the monkey was cancelling its VOR, the VOR evoked by the head acceleration step began to be suppressed shortly after the initiation of the step ( 30 ms). On the other hand, the latency of the smooth pursuit eye movement elicited when the visual target was accelerated in the same manner during VOR cancellation was 100 ms. The comparison between these two results suggests that the monkeys did not use visual information related to target motion to suppress their VOR at an early latency.The monkeys' ability to suppress the VOR evoked by an unexpected change in head acceleration depended on the size of the head acceleration step. The VOR evoked by unexpected step changes in head acceleration was progressively less suppressed at an early latency as the size of the acceleration step increased, and was not suppressed at an early latency when the step change in head acceleration was greater than 500°/s².During smooth pursuit eye movements, unexpected step changes in head acceleration evoked a VOR that was suppressed at an early latency ( 50 ms) if the head movement was in the same direction as the ongoing smooth pursuit eye movement. The amount of early VOR suppression increased as the pursuit eye velocity increased.We conclude that squirrel monkeys utilize a fast, non-visual mechanism for cancelling their VOR while they are fixating a visual target and their head is moving. This non-visual mechanism appears to be turned on when the head is moving and the monkey is fixating a head stationary target. The mechanism probably utilizes a voluntarily gated vestibular signal to cancel the signals in VOR pathways at the level of the extraocular motorneurons. Although the VOR cancellation mechanism is not capable of completely suppressing the VOR evoked by large unexpected changes in head acceleration, we suggest that it is capable of suppressing the VOR generated by most voluntary head movements during combined eye and head gaze pursuit and that the function of this gated VOR cancellation system is to extend the range and accuracy of eye-head tracking movements.