Inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection

The frontal pursuit area (FPA) lies posterior to the frontal eye fields in the frontal cortex and contains neurons that are directionally selective for pursuit eye movements. Lesions of the FPA (alternately called "FEFsem") cause deficits in pursuit acceleration and velocity, which are largest for movements directed toward the lesioned side. Conversely, stimulation of the FPA evokes pursuit from fixation and increases the gain of the pursuit response. On the basis of these properties, it has been hypothesized that the FPA could underlie the selection of pursuit direction. To test this possibility, we manipulated FPA activity and measured the effect on target selection behavior in rhesus monkeys. First, we unilaterally inactivated the FPA with the GABA agonist muscimol. We then measured the monkeys' performance on a pursuit-choice task. Second, we applied microstimulation unilaterally to the FPA during pursuit initiation while monkeys performed the same pursuit-choice task. Both of these manipulations produced significant effects on pursuit metrics; the inactivation decreased pursuit velocity and acceleration, and microstimulation evoked pursuit directly. Despite these changes, both manipulations failed to significantly alter choice behavior. These results show that FPA activity is not necessary for pursuit target selection.     

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.     

Supplementary eye fields stimulation facilitates anticipatory pursuit

Anticipatory movements are motor responses occurring before likely sensory events in contrast to reflexive actions. Anticipatory movements are necessary to compensate for delays present in sensory and motor systems. Smooth pursuit eye movements are often used as a paradigmatic example for the study of anticipation. However, the neural control of anticipatory pursuit is unknown. A previous study suggested that the supplementary eye fields (SEFs) could play a role in the guidance of smooth pursuit to predictable target motion. In this study, we favored anticipatory responses in monkeys by making the parameters of target motion highly predictable and electrically stimulated the SEF before and during this behavior. Stimulation sites were restricted to regions of the SEF where saccades could not be evoked at the same low currents. We found that electrical microstimulation in the SEF increased the velocity of anticipatory pursuit movements and decreased their latency. These effects will be referred to as anticipatory pursuit facilitation. The degree of facilitation was the largest if the stimulation train was delivered near the end of the fixation period, before the moment when anticipatory pursuit usually begins. No anticipatory smooth eye movements could be evoked during fixation without an expectation of target motion. These results suggest that the SEF pursuit area might be involved in the process of guiding anticipatory pursuit.     

Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. II. Relation to vector averaging pursuit

When monkeys view two targets moving in different directions and are given no cues about which to track, the initiation of smooth pursuit is a vector average of the response evoked by each target singly. In the present experiments, double-target stimuli consisted of two identical targets moving in opposite directions along the preferred axis of pursuit for the neuron under study for 200 ms, followed by the continued motion for 800 ms of one target chosen randomly. Among the neurons that showed directional modulation during pursuit, recordings revealed three groups. The majority (32/60) showed responses that were intermediate to, and statistically different from, the responses to either target presented alone. Another large group (22/60) showed activity that was statistically indistinguishable from the response to the target moving in the preferred (n = 15) or opposite (n = 7) direction of the neuron under study. The minority (6/60) showed statistically higher firing during averaging pursuit than for either target presented singly. We conclude that many pursuit-related neurons in the frontal pursuit area (FPA) carry signals related to the motor output during averaging pursuit, while others encode the motion of one target or the other. Microstimulation with 200-ms trains of pulses at 50 microA while monkeys performed the same double-target tasks biased the averaging eye velocity in the direction of evoked eye movements during fixation. The effect of stimulation was compared with the predictions of three different models that placed the site of vector averaging upstream from, at, or downstream from the sites where the FPA regulates the gain of pursuit. The data were most consistent with a site for pursuit averaging downstream from the gain control, both for double-target stimuli that presented motion in opposite directions and in orthogonal directions. Thus the recording and stimulation data suggest that the FPA is both downstream and upstream from the sites of vector averaging. We resolve this paradox by suggesting that the site of averaging is really downstream from the site of gain control, while feedback of the eye velocity command from the brain stem and/or cerebellum is responsible for the firing of FPA neurons in relation to the averaged eye velocity. We suggest that eye velocity feedback allows FPA neurons to continue firing during accurate tracking, when image motion is small, and that the persistent output from the FPA is necessary to keep the internal gain of pursuit high and permit accurate pursuit.     

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.     

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.     

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.     

The initial vestibulo-ocular reflex and its visual enhancement and cancellation in humans

The gain (ratio of eye velocity to head velocity) of the initial horizontal vestibulo-ocular reflex (VOR) was calculated in 12 normal subjects over 350 ms during impulsive, unpredictable whole body rotation under three conditions: (1) darkness; (2) visual enhancement of the VOR, while the subjects fixated a stationary target; and (3) visual cancellation of the reflex, while subjects fixated a target that rotated with the head. The gain of the initial 80 ms of compensatory eye movement increased significantly during visual fixation in 5 subjects and decreased during attempted VOR cancellation in 3 subjects, when compared with VOR gain in darkness. Compensatory vestibular smooth eye movements were slowed, becoming curved at the onset of VOR cancellation, at mean latencies ranging from 78 to 149 ms in individual subjects (group mean 128 ms). At about 190 ms, quick phases moved the eyes in the same direction as head and target motion. The subsequent vestibular eye movements were about 50% slower than the initial smooth eye movements, indicating more effective cancellation. Visual enhancement of the VOR can occur prior to the onset of pursuit, providing evidence that fixation and smooth pursuit are distinct ocular motor systems. Visual cancellation of the VOR also begins prior to smooth pursuit initiation and becomes more effective after the latency of smooth pursuit.     

Predictive responses of periarcuate pursuit neurons to visual target motion

The smooth pursuit eye movement system uses retinal information about the image-slip-velocity of the target in order to match the eye-velocity-in-space (i.e., gaze-velocity) to the actual target velocity. To maintain the target image on the fovea during smooth gaze tracking, and to compensate for the long delays involved in processing visual motion information and/or eye velocity commands, the pursuit system must use prediction. We have shown recently that both retinal image-slip-velocity and gaze-velocity signals are coded in the discharge of single pursuit-related neurons in the simian periarcuate cortex. To understand how periarcuate pursuit neurons are involved in predictive smooth pursuit, we examined the discharge characteristics of these neurons in trained Japanese macaques. When a stationary target abruptly moved sinusoidally along the preferred direction at 0.5 Hz, the response delays of pursuit cells seen at the onset of target motion were compensated in succeeding cycles. The monkeys were also required to continue smooth pursuit of a sinusoidally moving target while it was blanked for about half of a cycle at 0.5 Hz. This blanking was applied before cell activity normally increased and before the target changed direction. Normalized mean gain of the cells' responses (re control value without blanking) decreased to 0.81(+/-0.67 SD), whereas normalized mean gain of the eye movement (eye gain) decreased to 0.65 (+/-0.16 SD). A majority (75%) of pursuit neurons discharged appropriately up to 500 ms after target blanking even though eye velocity decreased sharply, suggesting a dissociation of the activity of those pursuit neurons and eye velocity. To examine whether pursuit cell responses contain a predictive component that anticipates visual input, the monkeys were required to fixate a stationary target while a second test laser spot was moved sinusoidally. A majority (68%) of pursuit cells tested responded to the second target motion. When the second spot moved abruptly along the preferred direction, the response delays clearly seen at the onset of sinusoidal target motion were compensated in succeeding cycles. Blanking (400-600 ms) was also applied during sinusoidal motion at 1 Hz before the test spot changed its direction and before pursuit neurons normally increased their activity. Preferred directions were similar to those calculated for target motion (normalized mean gain=0.72). Similar responses were also evoked even if the second spot was flashed as it moved. Since the monkeys fixated the stationary spot well, such flashed stimuli should not induce significant retinal slip. These results taken together suggest that the prediction-related activity of periarcuate pursuit neurons contains extracted visual components that reflect direction and speed of the reconstructed target image, signals sufficient for estimating target motion. We suggest that many periarcuate pursuit neurons convey this information to generate appropriate smooth pursuit eye movements.     

Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion

Success of motor behavior often depends on the ability to predict the path of moving objects. Here we asked whether tracking a visual object with smooth pursuit eye movements helps to predict its motion direction. We developed a paradigm, "eye soccer," in which observers had to either track or fixate a visual target (ball) and judge whether it would have hit or missed a stationary vertical line segment (goal). Ball and goal were presented briefly for 100-500 ms and disappeared from the screen together before the perceptual judgment was prompted. In pursuit conditions, the ball moved towards the goal; in fixation conditions, the goal moved towards the stationary ball, resulting in similar retinal stimulation during pursuit and fixation. We also tested the condition in which the goal was fixated and the ball moved. Motion direction prediction was significantly better in pursuit than in fixation trials, regardless of whether ball or goal served as fixation target. In both fixation and pursuit trials, prediction performance was better when eye movements were accurate. Performance also increased with shorter ball-goal distance and longer presentation duration. A longer trajectory did not affect performance. During pursuit, an efference copy signal might provide additional motion information, leading to the advantage in motion prediction.     

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.     

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)     

Doing without learning: stimulation of the frontal eye fields and floccular complex does not instruct motor learning in smooth pursuit eye movements

Under natural conditions, motor learning is instructed by sensory feedback. We have asked whether sensory signals that indicate motor errors are necessary to instruct learning or if the motor signals related to movements normally driven by sensory error signals would be sufficient. We measured eye movements in trained rhesus monkeys while employing electrical microstimulation of the floccular complex of the cerebellum and the smooth eye movement region of the frontal eye fields to alter ongoing pursuit eye movements. Repeated electrical stimulation at fixed times after the onset of target motion and pursuit failed to cause any learning that was retained beyond the time period used to instruct learning. Learning was not uncovered when the target was stabilized with respect to the moving eye to prevent competition between instructive signals created by electrical stimulation and visual image motion signals evoked when stimulation drove the eye away from the tracking target. We suggest that signals emanating from motor-related structures in the pursuit circuit do not instruct learning. Instead, instructive sensory error signals seem to be necessary.     

Pursuit responses to target steps during ongoing tracking

Brief smooth eye-velocity responses to target position steps have been reported during smooth pursuit. We investigated position-error responses in eight healthy human subjects, comparing the effects of a step-ramp change in target position when imposed on steady-state smooth pursuit, vestibuloocular reflex (VOR) slow phases, or fixation. During steady-state pursuit or VOR, the target performed a step-ramp movement in the same or in the opposite direction relative to ongoing eye movements. When the step was directed backward relative to steady-state smooth pursuit, eye velocity transiently decreased (1.3 +/- 0.4 degrees /s; average peak change in amplitude +/- SD), beginning about 100 ms after the step. The amplitude of position-error responses varied inversely with the step size. In contrast, there was little or no response in trials with forward steps during steady-state smooth pursuit, when step-ramps were imposed on VOR or when smooth pursuit began from fixation. We hypothesize that during ongoing smooth tracking when a sudden shift in target position is detected the pursuit system compares the direction of ongoing eye velocity with the relative positional error on the retina. In the case of different relative directions between ongoing tracking and a new target eccentricity, a position-error response toward the new target is initiated. Such a mechanism might help the smooth pursuit system to respond better to changes in target direction. These experimental findings were simulated by a mathematical model of smooth pursuit by implementing direction-dependent behavior with a position-error gating mechanism.     

Centripetal bias on preparation for smooth pursuit eye movements based on the anticipation

It has been reported that a brief perturbation of a stationary target during fixation induces larger eye movement when monkeys anticipate future smooth pursuit than when they do not. Here, we recorded eye movements in human subjects after briefly perturbing a target and the eccentricity of its initial position was changed under three conditions: (1) subjects anticipated saccades for a target that appeared before; (2) they anticipated smooth pursuit for a target that appeared before; and (3) they anticipated smooth pursuit but did not know beforehand where the target started from. We found that in condition 2 substantial eye movements were induced by the perturbation started moving toward the center. However, weak responses were observed in conditions 1 and 3. These results indicate that ocular responses to brief perturbations of the target at eccentric positions are increased with centripetal bias when human subjects prepare for future smooth pursuit.     

Adaptation of catch-up saccades during the initiation of smooth pursuit eye movements

Reduction of retinal speed and alignment of the line of sight are believed to be the respective primary functions of smooth pursuit and saccadic eye movements. As the eye muscles strength can change in the short-term, continuous adjustments of motor signals are required to achieve constant accuracy. While adaptation of saccade amplitude to systematic position errors has been extensively studied, we know less about the adaptive response to position errors during smooth pursuit initiation, when target motion has to be taken into account to program saccades, and when position errors at the saccade endpoint could also be corrected by increasing pursuit velocity. To study short-term adaptation (250 adaptation trials) of tracking eye movements, we introduced a position error during the first catch-up saccade made during the initiation of smooth pursuit—in a ramp-step-ramp paradigm. The target position was either shifted in the direction of the horizontally moving target (forward step), against it (backward step) or orthogonally to it (vertical step). Results indicate adaptation of catch-up saccade amplitude to back and forward steps. With vertical steps, saccades became oblique, by an inflexion of the early or late saccade trajectory. With a similar time course, post-saccadic pursuit velocity was increased in the step direction, adding further evidence that under some conditions pursuit and saccades can act synergistically to reduce position errors.     

Contrast and assimilation in motion perception and smooth pursuit eye movements

The analysis of visual motion serves many different functions ranging from object motion perception to the control of self-motion. The perception of visual motion and the oculomotor tracking of a moving object are known to be closely related and are assumed to be controlled by shared brain areas. We compared perceived velocity and the velocity of smooth pursuit eye movements in human observers in a paradigm that required the segmentation of target object motion from context motion. In each trial, a pursuit target and a visual context were independently perturbed simultaneously to briefly increase or decrease in speed. Observers had to accurately track the target and estimate target speed during the perturbation interval. Here we show that the same motion signals are processed in fundamentally different ways for perception and steady-state smooth pursuit eye movements. For the computation of perceived velocity, motion of the context was subtracted from target motion (motion contrast), whereas pursuit velocity was determined by the motion average (motion assimilation). We conclude that the human motion system uses these computations to optimally accomplish different functions: image segmentation for object motion perception and velocity estimation for the control of smooth pursuit eye movements.     

Extraretinal signals in MSTd neurons related to volitional smooth pursuit

Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VOR x 1) and cancellation of the VOR (VOR x 0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity < or = 0.10 spike/s/ degrees /s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.     

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.     

Involuntary cueing effects during smooth pursuit: facilitation and inhibition of return in oculocentric coordinates

Peripheral cues induce facilitation with short cue-target intervals and inhibition of return (IOR) with long cue-target intervals. Modulations of facilitation and IOR by continuous displacements of the eye or the cued stimuli are poorly understood. Previously, the retinal coordinates of the cued location were changed by saccadic or smooth pursuit eye movements during the cue-target interval. In contrast, we probed the relevant coordinates for facilitation and IOR by orthogonally varying object motion (stationary, moving) and eye movement (fixation, smooth pursuit). In the pursuit conditions, cue and target were presented during the ongoing eye movement and observers made a saccade to the target. Importantly, we found facilitation and IOR of similar size during smooth pursuit and fixation. The results suggest that involuntary orienting is possible even when attention has to be allocated to the moving target during smooth pursuit. Comparison of conditions with stabilized and moving objects suggest an oculocentric basis for facilitation as well as inhibition. Facilitation and IOR were reduced with objects that moved on the retina both with smooth pursuit and eye fixation.