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.     

Saccades to stationary and moving targets differ in the monkey

Saccade characteristics in response to moving and stationary targets were studied in three monkeys (Macaca mulatta) that had been trained to look at a target, which after an initial jump either remained in place or moved forward or backward with constant velocity (10°/s). Eye movements were recorded using a search coil. The contribution of smooth pursuit to the saccade amplitude was small (<0.25°). Saccades having the same amplitude (5.67–6.83° for different monkeys) to forward and backward moving targets were compared. Peak velocity was higher (37–42°/s on average for different monkeys) and saccade duration was shorter (8–10 ms on average) for backward saccades than for forward saccades These differences were highly significant (t-test: P<0.001). Thus, forward and backward saccades are not on the same main sequence. This suggests that saccade dynamics are affected not only by the retinal position error but also by target motion. Further analysis revealed that saccade peak velocity mainly depends on the retinal position error, but saccade amplitude also depends on a stimulus-related velocity factor, which affects the saccade mainly during deceleration. This velocity factor could be retinal slip or target velocity, which was the same under our conditions. Our results experimentally support recent models that propose that the saccade acceleration in response to moving targets might be controlled by the superior colliculus, whereas the deceleration changes are fine-tuned by the cerebellum. This prediction must still be tested on a neuronal level.Both Yanfang Guan and Thomas Eggert contributed equally     

Velocity prediction in corrective saccades during smooth-pursuit eye movements in monkey

Summary It has been noted in a variety of studies in both humans and monkeys that saccades made during smooth pursuit eye movements are usually quite accurate. Since saccades are known to be planned on the basis of neuronal information existing at some interval of time before the actual onset of the movement, it is generally accepted that some sort of prediction or use of visual motion velocity is combined with static position error in the execution of these saccades to moving targets. However, statistical treatment of this response in humans has provided evidence for alternative mechanisms, including a strategy of saccading ahead in the direction of target motion without any incorporation of actual speed information about target motion in the response. We reinvestigated this question quantitatively in the monkey on a large data base of saccades. We found evidence that supports the hypothesis that information about target speed per se is used in this species in the production of saccades to moving targets. Multiple linear regression analysis supported the hypothesis that information about the position error and the target velocity that exists at about 100 ms prior to the saccade onset are both required to provide a statistical explanation of saccade size during pursuit eye movements under the conditions of our experiments.     

A quantitative analysis of the correlations between eye movements and neural activity in the pretectum

The study of the saccadic system has focused mainly on neurons active before the beginning of saccades, in order to determine their contribution in movement planning and execution. However, most oculomotor structures contain also neurons whose activity starts only after the onset of saccades, the maximum of their activity sometimes occurring near saccade end. Their characteristics are still largely unknown. We investigated pretectal neurons with saccade-related activity in the alert cat during eye movements towards a moving target. They emitted a high-frequency burst of action potentials after the onset of saccades, irrespective of their direction, and will be referred to as "pretectal saccade-related neurons". The delay between saccade onset and cell activity varied from 17 to 66 ms on average. We found that burst parameters were correlated with the parameters of saccades; the peak eye velocity was correlated with the peak of the spike density function, the saccade amplitude with the number of spikes in the burst, and burst duration increased with saccade duration. The activity of six pretectal saccade-related neurons was studied during smooth pursuit at different velocities. A correlation was found between smooth pursuit velocity and mean firing rate. A minority of these neurons (2/6) were also visually responsive. Their visual activity was proportional to the difference between eye and target velocity during smooth pursuit (retinal slip). These results indicate that the activity of pretectal saccade-related neurons is correlated with the characteristics of eye movements. This finding is in agreement with the known anatomical projections from premotor regions of the saccadic system to the pretectum.     

Predictive elements in ocular interception and tracking of a moving target by untrained cats

We presented a mechanical target moving at constant velocity to awake, nontrained, head-restrained cats, in order to study how naive animals pursue objects moving at a high speed with their gaze. Eye movements were recorded while the target was moving in different directions at a constant velocity (20–80°/s) through the center of the visual field. We observed two oculomotor strategies: cats either made an interception saccade (IS) toward the target but opposite to its motion, or tracked it in the direction of motion. They used the interception strategy more frequently when the gaze position error at the onset of target motion was large, and the tracking strategy when it was small. Interception was always achieved by single saccades, which were faster than tracking saccades (TS). During tracking, cats generated sequences of two to six saccades separated by "smooth" eye movements. Tracking quality varied considerably from trial to trial. When the level of motivation was high, cats would track the target at 80°/s over up to 75% of the oculomotor range, with relatively small position errors. We compared ISs and TSs with respect to their metric properties and timing. The amplitudes of ISs positively correlated with position error existing 100 ms before saccade onset, but saccade vectors were directed to a point ahead of the target along the target's track. We conclude that, in programming the ISs, target motion is used to predict the future target position so as to assure a spatial lead of the gaze at the saccade end, instead of attempting a precise capture of the target. The amplitude of TSs did not depend on preceding position errors. TSs were usually small at the onset of the first saccade, as if cats would wait till the target arrived near the line of sight. A majority of primary TSs were initiated before the target arrived near the direction of gaze. Thus they had a direction, opposite to the position error sampled 100 ms before the saccade, but the same as the direction of target motion. Prediction of the future target position from its velocity vector should therefore contribute to the programming of TSs. In addition, we observed that TSs were faster when they were initiated with a spatial lag relative to the target and they were slower if there was a spatial lead or target velocity was reduced. Such a modulation appears to be analogous to the predictive correction of the saccade amplitude during smooth pursuit in primates. Considering strong visual motion sensitivity and motor properties of output neurons of the superior colliculus, it is likely that, in cats, the colliculus makes a major contribution to the integration of eye movement-related and target motion-related signals. Electronic Publication     

Eye-head coordination in cats

Gaze is the position of the visual axis in space and is the sum of the eye movement relative to the head plus head movement relative to space. In monkeys, a gaze shift is programmed with a single saccade that will, by itself, take the eye to a target, irrespective of whether the head moves. If the head turns simultaneously, the saccade is correctly reduced in size (to prevent gaze overshoot) by the vestibuloocular reflex (VOR). Cats have an oculomotor range (OMR) of only about +/- 25 degrees, but their field of view extends to about +/- 70 degrees. The use of the monkey's motor strategy to acquire targets lying beyond +/- 25 degrees requires the programming of saccades that cannot be physically made. We have studied, in cats, rapid horizontal gaze shifts to visual targets within and beyond the OMR. Heads were either totally unrestrained or attached to an apparatus that permitted short unexpected perturbations of the head trajectory. Qualitatively, similar rapid gaze shifts of all sizes up to at least 70 degrees could be accomplished with the classic single-eye saccade and a saccade-like head movement. For gaze shifts greater than 30 degrees, this classic pattern frequently was not observed, and gaze shifts were accomplished with a series of rapid eye movements whose time separation decreased, frequently until they blended into each other, as head velocity increased. Between discrete rapid eye movements, gaze continued in constant velocity ramps, controlled by signals added to the VOR-induced compensatory phase that followed a saccade. When the head was braked just prior to its onset in a 10 degrees gaze shift, the eye attained the target. This motor strategy is the same as that reported for monkeys. However, for larger target eccentricities (e.g., 50 degrees), the gaze shift was interrupted by the brake and the average saccade amplitude was 12-15 degrees, well short of the target and the OMR. Gaze shifts were completed by vestibularly driven eye movements when the head was released. Braking the head during either quick phases driven by passive head displacements or visually triggered saccades resulted in an acceleration of the eye, thereby implying interaction between the VOR and these rapid-eye-movement signals. Head movements possessed a characteristic but task-dependent relationship between maximum velocity and amplitude. Head movements terminated with the head on target. The eye saccade usually lagged the head displacement.(ABSTRACT TRUNCATED AT 400 WORDS)     

Accuracies of saccades to moving targets during pursuit initiation and maintenance

The overall goals of the studies presented here were to compare (1) the accuracies of saccades to moving targets with either a novel or a known target motion, and (2) the relationships between the measures of target motion and saccadic amplitude during pursuit initiation and maintenance. Since resampling of position error just prior to saccade initiation can confound the interpretation of results, the target ramp was masked during the planning and execution of the saccade. The results suggest that saccades to moving targets were significantly more accurate if the target motion was known from the early part of the trial (e.g., during pursuit maintenance) than in the case of novel target motion (e.g., during pursuit initiation); both these types of saccades were more accuate than those when target motion information was not available. Using target velocity in space as a rough estimate of the magnitude of the extra-retinal signal during pursuit maintenance, the saccadic amplitude was significantly associated with the extra-retinal target motion information after accounting for the position error. In most subjects, this association was stronger than the one between retinal slip velocity and saccadic amplitude during pursuit initiation. The results were similar even when the smooth eye motion prior to the saccade was controlled. These results suggest that different sources of target motion information (retinal image velocity vs internal representation of previous target motion in space) are used in planning saccades during different stages of pursuit. The association between retinal slip velocity and saccadic amplitude is weak during initiation, thus explaining poor saccadic accuracy during this stage of pursuit.     

Eye position and memory saccade related responses in substantia nigra pars reticulata

The substantia nigra pars reticulata (SNr), a major output nucleus of the basal ganglia, has been implicated anatomically, pharmacologically and physiologically in the generation of saccadic eye movements. However, the unique contribution of the SNr to saccade generation remains elusive. We studied the activity of SNr neurons while rhesus monkeys made saccades from different initial orbital positions, to determine what effects, if any, eye position had on SNr neuronal activity. We found that there was no effect of eye position on SNr neuronal responses. We also examined the responses of SNr neurons during memory-guided saccades to determine whether SNr discharges were affected by whether the target of the upcoming saccade was visible. We found that there was no change in response properties during memory saccade trials as compared to otherwise identical visually guided trials. SNr neurons appear to carry no information about either eye position or whether a movement is guided by a visible or remembered target. These results suggest that nigral signals are encoded in the same coordinate frame as those in the SC and FEF, but that unlike neuronal responses in these areas, SNr activity is not influenced by whether the saccade target remains visible until the movement is executed.     

Adaptive modifications of human postsaccadic pursuit eye movements induced by a step-ramp-ramp paradigm

 The main purpose of the present study was to investigate adaptive properties in human smooth-pursuit eye movements generated by a peripheral moving target. In adaptation trials, a target appeared in the peripheral visual field and immediately moved away at a constant speed, and a subject made a saccade and postsaccadic pursuit responses to track it. The target speed was, however, changed to a higher or lower constant speed (step-ramp-ramp target motion) at the termination of the saccade. This adaptation paradigm induced adaptive modifications in postsaccadic pursuit responses and our results revealed the following properties of the pursuit adaptation system. Topographic modification: Modification of the initial pursuit velocity depends on the position of a moving target. Pursuit gain change: Pursuit velocity is modified not by the addition of a constant bias to the pre-adaptation pursuit velocity, but by a change in the pursuit gain (pursuit velocity/target velocity). Lack of influence on saccade properties: Pursuit adaptation does not change the amplitude and latency of saccades either to a moving target or to a stationary target. Received: 31 May 1996 / Accepted: 28 January 1997     

Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range

Gaze, the direction of the visual axis in space, is the sum of the eye position relative to the head (E) plus head position relative to space (H). In the old explanation, which we call the oculocentric motor strategy, of how a rapid orienting gaze shift is controlled, it is assumed that 1) a saccadic eye movement is programmed with an amplitude equal to the target's offset angle, 2) this eye movement is programmed without reference to whether a head movement is planned, 3) if the head turns simultaneously the saccade is reduced in size by an amount equal to the head's contribution, and 4) the saccade is attenuated by the vestibuloocular reflex (VOR) slow phase. Humans have an oculomotor range (OMR) of about +/- 55 degrees. The use of the oculocentric motor strategy to acquire targets lying beyond the OMR requires programming saccades that cannot be made physically. We have studied in normal human subjects rapid horizontal gaze shifts to visible and remembered targets situated within and beyond the OMR at offsets ranging from 30 to 160 degrees. Heads were attached to an apparatus that permitted short unexpected perturbations of the head trajectory. The acceleration and deceleration phases of the head perturbation could be timed to occur at different points in the eye movement. 4. Single-step rapid gaze shifts of all sizes up to at least 160 degrees (the limit studied) could be accomplished with the classic single-eye saccade and an accompanying saccadelike head movement. In gaze shifts less than approximately 45 degrees, when head motion was prevented totally by the brake, the eye attained the target. For larger target eccentricities the gaze shift was interrupted by the brake and the average eye saccade amplitude was approximately 45 degrees, well short of the OMR. Thus saccadic eye movement amplitude was neurally, not mechanically, limited. When the head's motion was not perturbed by the brake, the eye saccade amplitude was a function of head velocity: for a given target offset, the faster the head the smaller the saccade. For gaze shifts to targets beyond the OMR and when head velocity was low, the eye frequently attained the 45 degrees position limit and remained there, immobile, until gaze attained the target.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of voluntary blinks on saccades,vergence eye movements,and saccade-vergence interactions in humans

Blinks are known to change the kinematic properties of horizontal saccades, probably by influencing the saccadic premotor circuit. The neuronal basis of this effect could be explained by changes in the activity of omnipause neurons in the nucleus raphe interpositus or in the saccade-related burst neurons of the superior colliculus. Omnipause neurons cease discharge during both saccades and vergence movements. Because eyelid blinks can influence both sets of neurons, we hypothesized that blinks would influence the kinematic parameters of saccades in all directions, vergence, and saccade-vergence interactions. To test this hypothesis, we investigated binocular eye and lid movements in five normal healthy subjects with the magnetic search coil technique. The subjects performed conjugate horizontal and vertical saccades from gaze straight ahead to targets at 20 degrees up, down, right, or left while either attempting not to blink or voluntarily blinking. While following the same blink instruction, subjects made horizontal vergence eye movements of 7 degrees and combined saccade-vergence movements with a version amplitude of 20 degrees. The movements were performed back and forth from two targets simultaneously presented nearby (38 cm) and more distant (145 cm). Small vertical saccades accompanied most vergence movements. These results show that blinks change the kinematics (saccade duration, peak velocity, peak acceleration, peak deceleration) of not only horizontal but also of vertical saccades, of horizontal vergence eye movements, and of combined saccade-vergence eye movements. Peak velocity, acceleration, and deceleration of eye movements were decreased on the average by 30%, and their duration increased by 43% on the average when they were accompanied by blinks. The blink effect was time dependent with respect to saccade and vergence onset: the greatest effect occurred 100 ms prior to saccade onset, whereas there was no effect when the blink started after saccade onset. The effects of blinks on saccades and vergence, which are tightly coupled to latency, support the hypothesis that blinks cause profound spatiotemporal perturbations of the eye movements by interfering with the normal saccade/vergence premotor circuits. However, the measured effect may to a certain degree but not exclusively be explained by mechanical interference.     

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

Recent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighing factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.     

The assessment of position of stationary targets perceived during saccadic eye movement

Summary The experiment was performed to establish the accuracy with which visual targets perceived during saccadic eye movement are localised. Subjects were presented with the task of executing saccades of 30° plus amplitude, passing through primary gaze, about the time of peak velocity a 5 ms red flash was presented at some random position (up to 30° left or right of centre) on a horizontal visual display. Subjects were required to indicate the direction in which they thought the flash was localised by fixating in that direction. Observations were made under conditions of prolonged total darkness and in the presence of a contrasting background. Measurement was made of saccade velocity and eye displacement as an index of target positions. Eye displacement was linearly scaled with respect to true target direction. Targets were localised with an average error of 5°–6° although the variance was high. No systematic differences were found between conditions or subjects. Error was unrelated to saccade velocity. It is concluded that during saccadic eye movements the appreciation of target position is maintained with an acceptable degree of accuracy.     

The initiation of smooth pursuit eye movements and saccades in normal subjects and in “express-saccade makers”

A vast knowledge exists about saccadic reaction times (RT) and their bi- or multimodal distributions with very fast (express) and regular RT. Recently, there has been some evidence that the smooth pursuit system may show a similar RT behavior. Since moving targets usually evoke a combined pursuit/saccade response, we asked which processes influence the initiation of pursuit and saccadic eye movements. Furthermore, we investigated whether and how the pursuit and saccadic system interact during the initiation of eye movements to moving targets. We measured the RT of the initial smooth pursuit (iSP) response and of the first corrective saccade and compared the RT behavior of both. Furthermore we compared the behavior of the corrective saccades to moving targets to that of saccades to stationary targets, known from the literature. The stimulus consisted of a target that moved suddenly at constant velocity (ramp). In addition, prior to the movement, a temporal gap, a position step or a combination of both could occur (gap-ramp, step-ramp, gap-step-ramp, respectively). Differently from most previous studies, we chose step and ramp with the same direction to provoke competition between the pursuit and saccade system. For the first time we investigated pursuit initiation in "express-saccade makers" (ES makers), a subject group known to produce an abnormally high percentage of short-latency saccades in saccade tasks. We compared their results with subject groups who were either naive or trained with respect to saccade tasks. The iSP started at approximately 100 ms, which corresponds to express saccade latencies. These short iSP-RT occurred reflex-like and almost independent of the experimental task. A bimodal frequency distribution of RT with a second peak of longer iSP-RT occurred exclusively in the ramp paradigm. The RT of the first corrective saccades in a pursuit task were comparable with that in a saccade task and depended on the stimulus. The ability of ES makers to produce a high number of express saccades was transferred to corrective saccades in the pursuit task, but not to pursuit initiation. In summary, short-latency pursuit responses differ from express saccades with respect to their independence of experiment and subject group. Therefore, a simple analogy to express saccades cannot be drawn, although some mechanisms seem to act similarly on both the pursuit and the saccade system (such as disengagement of attention with the gap effect). Furthermore, we found evidence that the initial pursuit response and the first corrective saccade are processed independently of each other. The first corrective saccades to moving targets behave like saccades to stationary targets. Normal pursuit but abnormal saccade RT of ES makers can be explained by recent theories of superior colliculus (SC) function in terms of retinal error handling.     

Processing of retinal and extraretinal signals for memory-guided saccades during smooth pursuit

It is an essential feature for the visual system to keep track of self-motion to maintain space constancy. Therefore the saccadic system uses extraretinal information about previous saccades to update the internal representation of memorized targets, an ability that has been identified in behavioral and electrophysiological studies. However, a smooth eye movement induced in the latency period of a memory-guided saccade yielded contradictory results. Indeed some studies described spatially accurate saccades, whereas others reported retinal coding of saccades. Today, it is still unclear how the saccadic system keeps track of smooth eye movements in the absence of vision. Here, we developed an original two-dimensional behavioral paradigm to further investigate how smooth eye displacements could be compensated to ensure space constancy. Human subjects were required to pursue a moving target and to orient their eyes toward the memorized position of a briefly presented second target (flash) once it appeared. The analysis of the first orientation saccade revealed a bimodal latency distribution related to two different saccade programming strategies. Short-latency (<175 ms) saccades were coded using the only available retinal information, i.e., position error. In addition to position error, longer-latency (>175 ms) saccades used extraretinal information about the smooth eye displacement during the latency period to program spatially more accurate saccades. Sensory parameters at the moment of the flash (retinal position error and eye velocity) influenced the choice between both strategies. We hypothesize that this tradeoff between speed and accuracy of the saccadic response reveals the presence of two coupled neural pathways for saccadic programming. A fast striatal-collicular pathway might only use retinal information about the flash location to program the first saccade. The slower pathway could involve the posterior parietal cortex to update the internal representation of the flash once extraretinal smooth eye displacement information becomes available to the system.     

Sensorimotor integration in the primate superior colliculus. I. Motor convergence

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.     

Predictive strategies in interception tasks: differences between eye and hand movements

To investigate how the sensorimotor systems of eye and hand use position, velocity, and timing information of moving targets, we conducted a series of three experiments. Subjects performed combined eye-hand catch-up movements toward visual targets that moved with step-ramp-like velocity profiles. Visual feedback of the hand was prevented by blanking the target at the onset of the hand movement. A multiple regression was used to determine the effects of position, velocity, and timing accessed before each movement on the movement amplitudes of eye and hand. The following results were obtained: 1.The predictive strategy of eye movements could be modeled by a linear regression on the basis of the position error and the target velocity. This was not the case for hand movements, for which there was a significant partial correlation between the movement amplitude and the product of target velocity and movement duration. This correlation was not observed for eye movements suggesting that the predictive strategy of hand movements takes movement duration into account, in contrast to the strategy used in eye movements. 2.To determine whether the movement amplitudes of eye and hand depend on a categorical classification between a discrete number of movement types, we compared an experiment in which target position and velocity were distributed continuously with an experiment using only four different combinations of target position and velocity. No systematic differences between these experiments were observed. This shows that the system output is a function of continuous, interval-scaled variables rather than a function of discrete categorical variables. 3.We also analyzed the component of the movement amplitudes not explained by the regression, i.e., the residual error. The residual errors between subsequent trials were correlated more strongly for eye than for hand movements, suggesting that short-term temporal fluctuations of the predictive strategy were stronger for the eye than for the hand.     

Direct evidence for a position input to the smooth pursuit system

When objects move in our environment, the orientation of the visual axis in space requires the coordination of two types of eye movements: saccades and smooth pursuit. The principal input to the saccadic system is position error, whereas it is velocity error for the smooth pursuit system. Recently, it has been shown that catch-up saccades to moving targets are triggered and programmed by using velocity error in addition to position error. Here, we show that, when a visual target is flashed during ongoing smooth pursuit, it evokes a smooth eye movement toward the flash. The velocity of this evoked smooth movement is proportional to the position error of the flash; it is neither influenced by the velocity of the ongoing smooth pursuit eye movement nor by the occurrence of a saccade, but the effect is absent if the flash is ignored by the subject. Furthermore, the response started around 85 ms after the flash presentation and decayed with an average time constant of 276 ms. Thus this is the first direct evidence of a position input to the smooth pursuit system. This study shows further evidence for a coupling between saccadic and smooth pursuit systems. It also suggests that there is an interaction between position and velocity error signals in the control of more complex movements.     

Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target

Because smooth-pursuit eye movements (SPEM) can be executed only in the presence of a moving target, it has been difficult to attribute the neuronal activity observed during the execution of these eye movements to either sensory processing or to motor preparation or execution. Previously, we showed that rhesus monkeys can be trained to perform SPEM directed toward an "imaginary" target defined by visual cues confined to the periphery of the visual field. The pursuit of an "imaginary" target provides the opportunity to elicit SPEM without stimulating visual receptive fields confined to the center of the visual field. Here, we report that a subset of neurons [85 "imaginary" visual tracking (iVT)-neurons] in area MST of 3 rhesus monkeys were identically activated during pursuit of a conventional, foveal dot target and the "imaginary" target. Because iVT-neurons did not respond to the presentation of a moving "imaginary" target during fixation of a stationary dot, we are able to exclude that responses to pursuit of the "imaginary" target were artifacts of stimulation of the visual field periphery. Neurons recorded from the representation of the central parts of the visual field in neighboring area MT, usually vigorously discharging during pursuit of foveal targets, in no case responded to pursuit of the "imaginary" target. This dissociation between MT and MST neurons supports the view that pursuit responses of MT neurons are the result of target image motion, whereas those of iVT-neurons in area MST reflect an eye movement-related signal that is nonretinal in origin. iVT-neurons fell into two groups, depending on the properties of the eye movement-related signal. Whereas most of them (71%) encoded eye velocity, a minority showed responses determined by eye position, irrespective of whether eye position was changed by smooth pursuit or by saccades. Only the former group exhibited responses that led the eye movement, which is a prerequisite for a causal role in the generation of SPEM.     

Quantitative analysis of catch-up saccades during sustained pursuit

During visual tracking of a moving stimulus, primates orient their visual axis by combining two very different types of eye movements, smooth pursuit and saccades. The purpose of this paper was to investigate quantitatively the catch-up saccades occurring during sustained pursuit. We used a ramp-step-ramp paradigm to evoke catch-up saccades during sustained pursuit. In general, catch-up saccades followed the unexpected steps in position and velocity of the target. We observed catch-up saccades in the same direction as the smooth eye movement (forward saccades) as well as in the opposite direction (reverse saccades). We made a comparison of the main sequences of forward saccades, reverse saccades, and control saccades made to stationary targets. They were all three significantly different from each other and were fully compatible with the hypothesis that the smooth pursuit component is added to the saccadic component during catch-up saccades. A multiple linear regression analysis was performed on the saccadic component to find the parameters determining the amplitude of catch-up saccades. We found that both position error and retinal slip are taken into account in catch-up saccade programming to predict the future trajectory of the moving target. We also demonstrated that the saccadic system needs a minimum period of approximately 90 ms for taking into account changes in target trajectory. Finally, we reported a saturation (above 15 degrees /s) in the contribution of retinal slip to the amplitude of catch-up saccades.