Extraretinal inputs to neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements.

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.

Effects of directional expectations on motion perception and pursuit eye movements.

Expectations about future motions can influence both perceptual judgements and pursuit eye movements. However, it is not known whether these two effects are due to shared processing, or to separate mechanisms with similar properties. We have addressed this question by providing subjects with prior information about the likely direction of motion in an upcoming random-dot motion display and measuring both the perceptual judgements and pursuit eye movements elicited by the stimulus. We quantified the subjects' responses by computing oculometric curves from their pursuit eye movements and psychometric curves from their perceptual decisions. Our results show that directional cues caused similar shifts in both the oculometric and psychometric curves toward the expected motion direction, with little change in the shapes of the curves. Prior information therefore biased the outcome of both eye movement and perceptual decisions without systematically changing their thresholds. We also found that eye movement and perceptual decisions tended to be the same on a trial-by-trial basis, at a higher frequency than would be expected by chance. Furthermore, the effects of prior information were evident during pursuit initiation, as well as during pursuit maintenance, indicating that prior information likely influenced the early processing of visual motion. We conclude that, in our experiments, expectations caused similar effects on both pursuit and perception by altering the activity of visual motion detectors that are read out by both the oculomotor and perceptual systems. Applying cognitive factors such as expectations at relatively early stages of visual processing could act to coordinate the metrics of eye movements with perceptual judgements.

Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements.

The intermediate and deep layers of the monkey superior colliculus (SC) comprise a retinotopically organized map for eye movements. The rostral end of this map, corresponding to the representation of the fovea, contains neurons that have been referred to as "fixation cells" because they discharge tonically during active fixation and pause during the generation of most saccades. These neurons also possess movement fields and are most active for targets close to the fixation point. Because the parafoveal locations encoded by these neurons are also important for guiding pursuit eye movements, we studied these neurons in two monkeys as they generated smooth pursuit. We found that fixation cells exhibit the same directional preferences during pursuit as during small saccades-they increase their discharge during movements toward the contralateral side and decrease their discharge during movements toward the ipsilateral side. This pursuit-related activity could be observed during saccade-free pursuit and was not predictive of small saccades that often accompanied pursuit. When we plotted the discharge rate from individual neurons during pursuit as a function of the position error associated with the moving target, we found tuning curves with peaks within a few degrees contralateral of the fovea. We compared these pursuit-related tuning curves from each neuron to the tuning curves for a saccade task from which we separately measured the visual, delay, and peri-saccadic activity. We found the highest and most consistent correlation with the delay activity recorded while the monkey viewed parafoveal stimuli during fixation. The directional preferences exhibited during pursuit can therefore be attributed to the tuning of these neurons for contralateral locations near the fovea. These results support the idea that fixation cells are the rostral extension of the buildup neurons found in the more caudal colliculus and that their activity conveys information about the size of the mismatch between a parafoveal stimulus and the currently foveated location. Because the generation of pursuit requires a break from fixation, the pursuit-related activity indicates that these neurons are not strictly involved with maintaining fixation. Conversely, because activity during the delay period was found for many neurons even when no eye movement was made, these neurons are also not obligatorily related to the generation of a movement. Thus the tonic activity of these rostral neurons provides a potential position-error signal rather than a motor command-a principle that may be applicable to buildup neurons elsewhere in the SC.

Activation and inactivation of rostral superior colliculus neurons during smooth-pursuit eye movements in monkeys.

Neurons in the intermediate and deep layers of the rostral superior colliculus (SC) of monkeys are active during attentive fixation, small saccades, and smooth-pursuit eye movements. Alterations of SC activity have been shown to alter saccades and fixation, but similar manipulations have not been shown to influence smooth-pursuit eye movements. Therefore we both activated (electrical stimulation) and inactivated (reversible chemical injection) rostral SC neurons to establish a causal role for the activity of these neurons in smooth pursuit. First, we stimulated the rostral SC during pursuit initiation as well as pursuit maintenance. For pursuit initiation, stimulation of the rostral SC suppressed pursuit to ipsiversive moving targets primarily and had modest effects on contraversive pursuit. The effect of stimulation on pursuit varied with the location of the stimulation with the most rostral sites producing the most effective inhibition of ipsiversive pursuit. Stimulation was more effective on higher pursuit speeds than on lower and did not evoke smooth-pursuit eye movements during fixation. As with the effects on pursuit initiation, ipsiversive maintained pursuit was suppressed, whereas contraversive pursuit was less affected. The stimulation effect on smooth pursuit did not result from a generalized inhibition because the suppression of smooth pursuit was greater than the suppression of smooth eye movements evoked by head rotations (vestibular-ocular reflex). Nor was the stimulation effect due to the activation of superficial layer visual neurons rather than the intermediate layers of the SC because stimulation of the superficial layers produced effects opposite to those found with intermediate layer stimulation. Second, we inactivated the rostral SC with muscimol and found that contraversive pursuit initiation was reduced and ipsiversive pursuit was increased slightly, changes that were opposite to those resulting from stimulation. The results of both the stimulation and the muscimol injection experiments on pursuit are consistent with the effects of these activation and inactivation experiments on saccades, and the effects on pursuit are consistent with the hypothesis that the SC provides a position signal that is used by the smooth-pursuit eye-movement system.

Population coding of movement dynamics by cerebellar Purkinje cells.

In order to accomplish desired movements, the nervous system must specify the movement dynamics: it must provide a signal that compensates for the mechanical constraints encountered during movement. Here we tested whether the population activity of Purkinje cells in the cerebellum specifies the dynamics for pursuit eye movements. We first estimated the population activity by computing weighted averages of Purkinje cell firing on a millisecond time scale. We then generated predicted eye movements by transforming this pooled neural activity with a description of eye mechanics. We found that the equally weighted average of Purkinje cell outputs produced a close match between the predicted and actual eye movements. These findings demonstrate that neural circuits through the cerebellum are capable of providing the dynamic compensation necessary to achieve desired movements.

Target selection for pursuit and saccadic eye movements in humans.

Eye movements were recorded from three subjects as they initiated tracking of a small circle ("target") moving leftward or rightward, above or below the horizontal meridian, either alone or in the presence of a small square ("distractor") moving leftward or rightward on the other side of the horizontal meridian. At the start of each trial, subjects were provided with either a "form" cue (always centrally positioned and having the circular shape and color of the upcoming moving target) or a "location" cue (a small white square positioned where the upcoming target would appear). The latency of pursuit increased in the presence of an oppositely moving distractor when subjects were provided the form cues but not when they were provided the location cues. The latency of saccades showed similar, but smaller, increases when subjects were given the form cues. On many trials with the form cues, pursuit started in the direction of the distractor and then reversed to follow the target. On these trials, the initial saccade often, but not always, also followed the distractor. These results indicate that the mechanisms of target selection for pursuit and saccades are tightly coordinated but not strictly yoked. The shared effects of the distractor on the latencies of pursuit and saccades probably reflect the common role of visual attention in filtering the inputs that guide these two types of eye movements. The differences in the details of the effects on pursuit and saccades suggest that the neural mechanisms that trigger these two movements can be independently regulated.

Tracking with the mind's eye.

The two components of voluntary tracking eye-movements in primates, pursuit and saccades, are generally viewed as relatively independent oculomotor subsystems that move the eyes in different ways using independent visual information. Although saccades have long been known to be guided by visual processes related to perception and cognition, only recently have psychophysical and physiological studies provided compelling evidence that pursuit is also guided by such higher-order visual processes, rather than by the raw retinal stimulus. Pursuit and saccades also do not appear to be entirely independent anatomical systems, but involve overlapping neural mechanisms that might be important for coordinating these two types of eye movement during the tracking of a selected visual object. Given that the recovery of objects from real-world images is inherently ambiguous, guiding both pursuit and saccades with perception could represent an explicit strategy for ensuring that these two motor actions are driven by a single visual interpretation.

Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation.

We studied the eye movements evoked by applying small amounts of current (2-50 microA) within the oculomotor vermis of two monkeys. We first compared the eye movements evoked by microstimulation applied either during maintained pursuit or during fixation. Smooth, pursuitlike changes in eye velocity caused by the microstimulation were directed toward the ipsilateral side and occurred at short latencies (10-20 ms). The amplitudes of these pursuitlike changes were larger during visually guided pursuit toward the contralateral side than during either fixation or visually guided pursuit toward the ipsilateral side. At these same sites, microstimulation also often produced abrupt, saccadelike changes in eye velocity. In contrast to the smooth changes in eye velocity, these saccadelike effects were more prevalent during fixation and during pursuit toward the ipsilateral side. The amplitude and type of evoked eye movements could also be manipulated at single sites by changing the frequency of microstimulation. Increasing the frequency of microstimulation produced increases in the amplitude of pursuitlike changes, but only up to a certain point. Beyond this point, the value of which depended on the site and whether the monkey was fixating or pursuing, further increases in stimulation frequency produced saccadelike changes of increasing amplitude. To quantify these effects, we introduced a novel method for classifying eye movements as pursuitlike or saccadelike. The results of this analysis showed that the eye movements evoked by microstimulation exhibit a distinct transition point between pursuit and saccadelike effects and that the amplitude of eye movement that corresponds to this transition point depends on the eye movement behavior of the monkey. These results are consistent with accumulating evidence that the oculomotor vermis and its associated deep cerebellar nucleus, the caudal fastigial, are involved in the control of both pursuit and saccadic eye movements. We suggest that the oculomotor vermis might accomplish this role by altering the amplitude of a motor error signal that is common to both saccades and pursuit.

Shared motor error for multiple eye movements.

Most natural actions are accomplished with a seamless combination of individual movements. Such coordination poses a problem: How does the motor system orchestrate multiple movements to produce a single goal-directed action? The results from current experiments suggest one possible solution. Oculomotor neurons in the superior colliculus of a primate responded to mismatches between eye and target positions, even when the animal made two different types of eye movements. This neuronal activity therefore does not appear to convey a command for a specific type of eye movement but instead encodes an error signal that could be used by multiple movements. The use of shared inputs is one possible strategy for ensuring that different movements share a common goal.

Initiation of saccades during fixation or pursuit: evidence in humans for a single mechanism.

1. In four human subjects, we measured the latency of saccadic eye movements made to a second, eccentric target after an initial, foveated target was extinguished. In separate interleaved trails, the targets were either both stationary ("fixation") or both moving with the same velocity ("pursuit"). For both fixation and pursuit trials, we extinguished the first target at randomized times during maintained fixation or pursuit and varied the time interval ("gap duration") before the appearance of the second target. 2. During both fixation and pursuit, the presence of a 200-ms gap reduced the latencies of saccades, compared with those obtained with no gap. For two subjects, we imposed additional, intermediate gap durations and found that saccade latencies varied as a function of gap duration. Furthermore, the latencies of saccades elicited during pursuit displayed the same dependence on gap duration as those elicited during fixation. 3. Our results demonstrate that the "gap effect" observed for saccades made during fixation also occurs for saccades made during pursuit. To the extent that the gap effect on saccade latency reflects a mechanism underlying the release of fixation, our results suggest that the same mechanism is invoked for saccades made during pursuit. From the viewpoint of initiating saccades, the existence of separate fixation and pursuit systems may be irrelevant.

Release of fixation for pursuit and saccades in humans: evidence for shared inputs acting on different neural substrates.

1. In three human subjects, we measured the latency of pursuit and saccadic eye movements made to an eccentric target after a fixated central target was extinguished. In one set of experiments, we varied the time interval between the extinction of the central target and the appearance of the eccentric target ("gap duration"). In a second set of experiments, we varied the eccentricity at which the second target appeared. 2. Varying the gap duration produced similar changes in the latencies of pursuit and saccades. Gaps as short as 30 ms caused significant decreases in latency; progressively longer gaps produced shorter latencies, reaching a minimum for gaps of 150-200 ms. Over the range of gap durations used, the latencies of pursuit and saccades displayed the same dependence on gap duration. 3. Varying the eccentricity of the second target produced different effects on the latencies of pursuit and saccades. Saccade latencies increased when the eccentricity of the second target was decreased from 4 degrees to 0.5 degree, whereas pursuit latencies were not consistently altered. Despite these differences in the dependence on retinal eccentricity between pursuit and saccades, imposing a 200-ms gap between the extinction of the fixation point and appearance of the second target still reduced the latency of both. 4. Our results are consistent with the idea that the mechanisms underlying the release of fixation for pursuit and saccades have shared inputs but a different neural substrate. The common dependence on gap duration may indicate that a single preparatory input coordinates both types of movements. The different dependence on retinal eccentricity indicates that there are differences in the spatial organization of the premotor circuits that trigger the onset of the two types of movements.

Transitions between pursuit eye movements and fixation in the monkey: dependence on context.

1. We compared the visuomotor processing underlying the onset and offset of pursuit by recording the eye movements of three monkeys as they smoothly tracked a target that was initially at rest, started to move suddenly at a constant velocity along the horizontal meridian, and then stopped. We presented this sequence of target motions in two different contexts. In the first context the target sometimes stopped after 500 ms, but on other interleaved trials the target either continued moving at a constant velocity, slowed down, speeded up, or reversed direction. In the second context the target always stopped, but the duration of the preceding constant velocity was randomized from 500 to 700 ms. 2. The dynamics of the eye velocity during the offset of pursuit were markedly different in the two experiments. When the target stopped only sometimes, the decrease in eye velocity at the offset of pursuit often overshot zero, producing a brief, small reversal in the direction of pursuit before eye speed settled to zero. When the target always stopped, the decrease in eye velocity at the offset of pursuit followed a more gradual transition toward zero with no overshoot. Thus the eye velocity profiles obtained in the first experiment contradict, whereas those obtained in the second experiment confirm, previous characterizations of the offset of pursuit as an exponential decay toward zero eye speed. 3. To investigate the basis of the different eye velocity profiles obtained in the two experiments, we probed the state of transmission along the visuomotor pathways for pursuit with the use of small perturbations in the motion of the target. We used perturbations consisting of 1 degree step changes in target position superimposed on the constant velocity motion of the target, on the basis of previous findings that such perturbations elicit saccades during fixation but smooth changes in eye speed during maintained pursuit. Single perturbations were imposed at regularly spaced intervals on separate interleaved trials during the onset, maintenance, and offset of pursuit. 4. Perturbations imposed during the onset and maintenance of pursuit had similar effects regardless of whether the target stopped only sometimes or always. In both experiments, perturbations that stepped the target in the direction opposite to the constant velocity of the target produced decreases in eye speed; perturbations in the same direction produced negligible or inconsistent changes in eye speed. The changes in eye speed caused by perturbations were largest for those perturbations introduced within the first 100 ms after the start of target motion, before the onset of the smooth eye movement, and became progressively smaller as target motion continued. The largest changes in eye speed were therefore caused by those perturbations imposed during periods of large retinal slip and by those perturbations whose direction opposed that slip. 5. Perturbations imposed during the offset of pursuit had different effects depending on whether the target stopped only sometimes or always. When the target stopped only sometimes, forward perturbations produced large increases in eye speed, whereas backward perturbations produced negligible or inconsistent changes in eye speed. Thus the visuomotor processing underlying the offset of pursuit in this experiment strongly resembled that underlying the onset of pursuit: in both cases, those perturbations in the direction opposing large retinal slip produced the largest effects. In contrast, when the target always stopped, neither forward nor backward perturbations imposed during the offset of pursuit produced large changes in eye speed. This indicates that the visuomotor processing underlying the offset of pursuit in this experiment was different from the processing underlying the onset of pursuit. 6. Perturbations also produced changes in the frequency of saccades, although these effects were less consistent than the changes in pursuit eye speed

Decreases in the latency of smooth pursuit and saccadic eye movements produced by the "gap paradigm" in the monkey.

The initiation of both pursuit and saccades was affected by the presence of a temporal gap between the disappearance of a fixated visual target and the appearance of a second, eccentric, target. For pursuit, the gap paradigm produced a modest (20 msec) decrease in latency. For saccades, the gap paradigm produced a similar modest decrease in the latency of some saccades, but also revealed a population of very short latency "express" saccades. The modest changes in the latency of pursuit and regular saccades displayed a similar dependence on gap duration, with the largest decreases produced by gaps of 200-300 msec. The gap paradigm did not produce "express" pursuit, even though express saccades could be elicited on interleaved trials.

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

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

Short-latency disparity vergence responses and their dependence on a prior saccadic eye movement.

1. A dichoptic viewing arrangement was used to study the initial vergence eye movements elicited by brief horizontal disparity steps applied to large textured patterns in three rhesus monkeys. Disconjugate steps (range, 0.2-10.9 degrees) were applied to the patterns at selected times (range, 13-303 ms) after 10 degrees leftward saccades into the center of the pattern. The horizontal and vertical positions of both eyes were recorded with the electromagnetic search coil technique. 2. Without training or reinforcement, disparity steps of suitable amplitude consistently elicited vergence responses at short latencies. For example, with 1.8 degrees crossed-disparity steps applied 26 ms after the centering saccade, the mean latency of onset of convergence for each of the three monkeys was 52.2 +/- 3.8 (SD) ms, 52.3 +/- 5.2 ms, and 53.4 +/- 4.1 ms. 3. Experiments in which the disparity step was confined to only one eye indicated that each eye was not simply tracking the apparent motion that is saw. For example, when crossed-disparity steps were confined to the right eye (which saw leftward steps), the result was (binocular) convergence in which the left eye moved to the right even though that eye had seen only a stationary scene. This movement of the left eye cannot have resulted from independent monocular tracking and indicates that the vergences here derived from the binocular misalignment of the two retinal images. 4. The initial vergence responses to crossed-disparity steps had the following main features. 1) They were always in the correct (i.e., convergent) direction over the full range of stimuli tested, the initial vergence acceleration increasing progressively with increases in disparity until reaching a peak with steps of 1.4-2.4 degrees and declining thereafter to a nonzero asymptote as steps exceeded 5-7 degrees. 2) They showed transient postsaccadic enhancement whereby steps applied in the immediate wake of a saccadic eye movement resulted in much higher initial vergence accelerations than the same steps applied some time later. The response decline in the wake of a saccade was roughly exponential with time constants of 67 +/- 5 (SD) ms, 35 +/- 2 ms, and 54 +/- 4 ms for the three animals. 3) That the postsaccadic enhancement might have resulted in part from the visual stimulation associated with the prior saccade was suggested by the finding that enhancement could also be observed when the disparity steps were applied in the wake of (conjugate) saccadelike shifts of the textured pattern. However, this visual enhancement did not reach a peak unit 17-37 ms after the end of the "simulated" saccade, and the peak enhancement averaged only 45% of that after a "real" saccade. 4) Qualitatively similar transient enhancements in the wake of real and simulated saccades have also been reported for initial ocular following responses elicited by conjugate drifts of the visual scene. We replicated the enhancement effects on ocular following to allow a direct comparison with the enhancement effects on disparity vergence using the same animals and visual stimulus patterns and, despite some clear quantitative differences, we suggest that the enhancement effects share a similar etiology. 5. Initial vergence responses to uncrossed-disparity steps had the following main features. 1) They were in the correct (i.e., divergent) direction only for very small steps (< 1.5-2.5 degrees), and then only when postsaccadic delays were small; when the magnitude of the steps was increased beyond these levels, responses declined to zero and thereafter reversed direction, eventually reaching a nonzero (convergent) asymptote similar to that seen with large crossed-disparity steps; convergent responses were also seen with larger vertical disparity steps, suggesting that they represent default responses to any disparity exceeding a few degrees. 2) As the postsaccadic delay was increased, responses to small steps (1.8 degrees) declined to zero and thereafter re

A model of visually-guided smooth pursuit eye movements based on behavioral observations.

We report a model that reproduces many of the behavioral properties of smooth pursuit eye movements. The model is a negative-feedback system that uses three parallel visual motion pathways to drive pursuit. The three visual pathways process image motion, defined as target motion with respect to the moving eye, and provide signals related to image velocity, image acceleration, and a transient that occurs at the onset of target motion. The three visual motion signals are summed and integrated to produce the eye velocity output of the model. The model reproduces the average eye velocity evoked by steps of target velocity in monkeys and humans and accounts for the variation among individual responses and subjects. When its motor pathways are expanded to include positive feedback of eye velocity and a "switch", the model reproduces the exponential decay in eye velocity observed when a moving target stops. Manipulation of this expanded model can mimic the effects of stimulation and lesions in the arcuate pursuit area, the middle temporal visual area (MT), and the medial superior temporal visual area (MST).

Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during the onset and offset of pursuit eye movements.

1. We recorded the simple spike firing rate of gaze velocity Purkinje cells (GVP-cells) in the flocculus/ventral paraflocculus of two monkeys during the smooth pursuit eye movements evoked by a target that was initially at rest, started suddenly, moved at a constant velocity, and then stopped. 2. For target motion in the preferred direction, GVP-cells showed a large transient increase in firing rate at the onset of pursuit, a smaller but sustained increase during the maintenance of pursuit, and a smooth return to baseline firing with little undershoot at the offset of pursuit. For target motion in the nonpreferred direction, GVP-cells showed a small decrease in firing rate at the onset of pursuit, a similar sustained decrease during the maintenance of pursuit, but a large transient increase in firing rate at the offset of pursuit before returning to baseline firing. 3. We pooled the data in our sample of horizontal GVP-cells by subtracting the population average of firing rate recorded during pursuit in the nonpreferred direction from the population average recorded during pursuit in the preferred direction. We transformed this net population average by passing it through a model of the brain stem final common pathway and the oculomotor plant. This yielded a signal that closely matched the observed trajectory of eye velocity during pursuit. We conclude that the transient overshoots exhibited in the firing rate of GVP-cells can provide appropriate compensation for the lagging dynamics of the oculomotor plant.

Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys.

1. Our goal was to assess whether visual motion signals related to changes in image velocity contribute to pursuit eye movements. We recorded the smooth eye movements evoked by ramp target motion at constant speed. In two different kinds of stimuli, the onset of target motion provided either an abrupt, step change in target velocity or a smooth target acceleration that lasted 125 ms followed by prolonged target motion at constant velocity. We measured the eye acceleration in the first 100 ms of pursuit. Because of the 100-ms latency from the onset of visual stimuli to the onset of smooth eye movement, the eye acceleration in this 100-ms interval provides an estimate of the open-loop response of the visuomotor pathways that drive pursuit. 2. For steps of target velocity, eye acceleration in the first 100 ms of pursuit depended on the "motion onset delay," defined as the interval between the appearance of the target and the onset of motion. If the motion onset delay was > 100 ms, then the initial eye movement consisted of separable early and late phases of eye acceleration. The early phase dominated eye acceleration in the interval from 0 to 40 ms after pursuit onset and was relatively insensitive to image speed. The late phase dominated eye acceleration in the interval 40-100 ms after the onset of pursuit and had an amplitude that was proportional to image speed. If there was no delay between the appearance of the target and the onset of its motion, then the early component was not seen, and eye acceleration was related to target speed throughout the first 100 ms of pursuit. 3. For step changes of target velocity, the relationship between eye acceleration in the first 40 ms of pursuit and target velocity saturated at target speeds > 10 degrees /s. In contrast, the relationship was nearly linear when eye acceleration was measured in the interval 40-100 ms after the onset of pursuit. We suggest that the first 40 ms of pursuit are driven by a transient visual motion input that is related to the onset of target motion (motion onset transient component) and that the next 60 ms are driven by a sustained visual motion input (image velocity component). 4. When the target accelerated smoothly for 125 ms before moving at constant speed, the initiation of pursuit resembled that evoked by steps of target velocity. However, the latency of pursuit was consistently longer for smooth target accelerations than for steps of target velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys.

1. Our goal was to discriminate between two classes of models for pursuit eye movements. The monkey's pursuit system and both classes of model exhibit oscillations around target velocity during tracking of ramp target motion. However, the mechanisms that determine the frequency of oscillations differ in the two classes of model. In "internal feedback" models, oscillations are controlled by internal feedback loops, and the frequency of oscillation does not depend strongly on the delay in visual feedback. In "image motion" models, oscillations are controlled by visual feedback, and the frequency of oscillation does depend on the delay in visual feedback. 2. We measured the frequency of oscillation during pursuit of ramp target motion as a function of the total delay for visual feedback. For the shortest feedback delays of approximately 70 ms, the frequency of oscillation was between 6 and 7 Hz. Increases in feedback delay caused decreases in the frequency of oscillation. The effect of increasing feedback delay was similar, whether the increases were produced naturally by dimming and decreasing the size of the tracking target or artificially with the computer. We conclude that the oscillations in eye velocity during pursuit of ramp target motion are controlled by visual inputs, as suggested by the image motion class of models. 3. Previous experiments had suggested that the visuomotor pathways for pursuit are unable to respond well to frequencies as high as the 6-7 Hz at which eye velocity oscillates in monkeys. We therefore tested the response to target vibration at an amplitude of +/- 8 degrees/s and frequencies as high as 15 Hz. For target vibration at 6 Hz, the gain of pursuit, defined as the amplitude of eye velocity divided by the amplitude of target velocity, was as high as 0.65. We conclude that the visuomotor pathways for pursuit are capable of processing image motion at high temporal frequencies. 4. The gain of pursuit was much larger when the target vibrated around a constant speed of 15 degrees/s than when it vibrated around a stationary position. This suggests that the pursuit pathways contain a switch that must be closed to allow the visuomotor pathways for pursuit to operate at their full gain. The switch apparently remains open for target vibration around a stationary position. 5. The responses to target vibration revealed a frequency at which eye velocity lagged target velocity by 180 degrees and at which one monkey showed a local peak in the gain of pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual motion commands for pursuit eye movements in the cerebellum.

Eye movements that follow a target (pursuit eye movements) facilitate high acuity visual perception of moving targets by transforming visual motion inputs into motor commands that match eye motion to target motion. The performance of pursuit eye movements requires the cerebellar flocculus, which processes both visual motion and oculomotor signals. Electrophysiological recordings from floccular Purkinje cells have allowed the identification of their firing patterns during generation of the image velocity and image acceleration signals used for pursuit. Analysis with a method based on a behavioral model converted the time-varying spike trains of floccular Purkinje cells into a description of the firing rate contributed by three visual motion signals and one oculomotor input. The flocculus encodes all the signals needed to guide pursuit.