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Expected surprise, defined as the anticipation of uncertainty associated with the occurrence of a future event, plays a major role in gaze shifting and spatial attention. In the present study, we analyzed its impact on oculomotor behavior. We hypothesized that the occurrence of anticipatory saccades could decrease with increasing expected surprise and that its influence on visually-guided responses could be different given the presence of sensory information and perhaps competitive attentional effects. This hypothesis was tested in humans using a saccadic reaction time task in which a cue indicated the future stimulus position. In the ‘no expected surprise’ condition, the visual target could appear only at one previously cued location. In other conditions, more likely future positions were cued with increasing expected surprise. Anticipation was more frequent and pupil size was larger in the ‘no expected surprise’ condition compared with all other conditions, probably due to increased arousal. The latency of visually-guided saccades increased linearly with the logarithm of surprise (following Hick’s law) but their maximum velocity repeated the arousal-related pattern. Therefore, expected surprise affects anticipatory and visually-guided responses differently. Moreover, these observations suggest a causal chain linking surprise, attention and saccades that could be disrupted in attentional or impulse control disorders.

Patient suffering of Major Depressive Disorder (MDD) often complain that subjective time seems to ‘drag’ with respect to physical time. This may point towards a generalized dysfunction of temporal processing in MDD. In the present study, we investigated temporal preparation in MDD. “Temporal preparation” refers to an increased readiness to act before an expected event; consequently, reaction time should be reduced. MDD patients and age-matched controls were required to make a saccadic eye movement between a central and an eccentric visual target after a variable duration preparatory period. We found that MDD patients produced a larger number of premature saccades, saccades initiated prior to the appearance of the expected stimulus. These saccades were not temporally controlled; instead, they seemed to reflect increased oculomotor impulsivity. In contrast, the latency of visually-guided saccades was strongly influenced by temporal preparation in controls; significantly less so, in MDD patients. This observed reduced temporal preparation in MDD was associated with a faster decay of short-term temporal memory. Moreover, in patients producing a lot of premature responses, temporal preparation to early imperative stimuli was increased. A reduction in premature saccades, however, was associated with reduced temporal preparation to late imperative stimuli.In conclusion, reduced temporal preparation and short-term temporal memory in the oculomotor domain supports the hypothesis that temporal processing was altered in MDD patients. These observed deficits could reflect other underlying aspects of abnormal time experience in MDD.

International audience; In a rapidly changing environment, we often know when to do something before we have to do it. This preparation in the temporal domain is based on a ‘perception’ of elapsed time and short-term memory of previous stimulation in a similar context. These functions could be perturbed in Parkinson’s disease. Therefore, we investigated their role in eye movement preparation in sporadic Parkinson’s disease and in a very infrequent variant affecting the Parkin gene. We used a simple oculomotor task where subjects had to orient to a visual target and movement latency was measured. We found that in spite of an increased average reaction time, the influence of elapsed time on movement preparation was similar in controls and the two groups of PD patients. However, short-term temporal memory of previous stimulation was severely affected in sporadic PD patients either ON or OFF dopaminergic therapy. We conclude that the two different contributions to temporal preparation could be dissociated. Moreover, a short-term temporal memory deficit might underlie temporal cognition deficits previously observed in PD.

Causality is a unique feature of human perception. We present here a behavioral investigation of the influence of physical causality during visual pursuit of object collisions. Pursuit and saccadic eye movements of human subjects were recorded during ocular pursuit of two concurrently launched targets, one that moved according to the laws of Newtonian mechanics (the causal target) and the other one that moved in a physically implausible direction (the non-causal target). We found that anticipation of collision evoked early smooth pursuit decelerations. Saccades to non-causal targets were hypermetric and had latencies longer than saccades to causal targets. In conclusion, before and after a collision of two moving objects the oculomotor system implicitly predicts upcoming physically plausible target trajectories.

During visual pursuit of a moving target, expected changes in its trajectory often evoke anticipatory smooth pursuit responses. In the present study, we investigated characteristics of anticipatory smooth pursuit decelerations before a change or the end of a target trajectory. Healthy humans had to pursue with the eyes a target moving along a circular path that predictably or unpredictably reversed direction and then retraced its movement back to the starting position. We found that anticipatory eye decelerations were often evoked in temporal expectation of target reversal and of the end of the trajectory. The latency of anticipatory decelerations initiated before target reversal was variable, had poor temporal accuracy and depended on the history of previous trials. Anticipations of the end of the trajectory were more accurate, more precise and were not influenced by previous trials. In this case, subjects probably based their estimate of the end of the trajectory on the duration just experienced before target motion reversal. These results suggest that anticipatory eye decelerations are based on the characteristics of the current or preceding trials depending on the most reliable information available.

Expectation of upcoming events is an essential cognitive function on which anticipatory actions are based. The neuronal basis of this prospective representation is poorly understood. We trained rhesus monkeys in a smooth-pursuit task in which the direction of upcoming target motion was indicated using a color cue. Under these conditions, directional expectation frequently evoked anticipatory smooth movements. We found that the activity of a population of neurons in the supplementary eye fields encoded the expected future direction of the target. Neuronal activity increased after presentation of the cue, indicating future target motion in the preferred direction. Neuronal activity either remained unaltered or was reduced if the antipreferred direction was cued. In addition, ∼30% of these neurons were more active during trials with anticipatory pursuit in the preferred direction than during trials when monkeys did not anticipate target motion onset. This subset of recorded neurons encoded the direction of the subsequent anticipatory pursuit. We hypothesize that the neural representation of directional expectation could be conceptualized as a competitive interaction between pools of neurons representing likely future events, with the winner of this competition determining the direction of the subsequent anticipatory movement. Similar mechanisms could drive prediction before movement initiation in other motor domains.

RATIONALE: It has been shown that antagonism of the glutamatergic N-methyl-D-aspartate (NMDA) receptor with subanesthetic doses of ketamine perturbs the perception of elapsed time. Anticipatory eye movements are based on an internal representation of elapsed time. Therefore, the occurrence of anticipatory saccades could be a particularly sensitive indicator of abnormal time perception due to NMDA receptors blockade. OBJECTIVES: To determine whether the occurrence of anticipatory saccades could be selectively altered by a subanesthetic dose of ketamine. METHODS: Three Rhesus monkeys were trained in a simple visually-guided saccadic task with a variable delay. Monkeys were rewarded for making a visually-guided saccade at the end of the delay. Premature anticipatory saccades to the future position of the eccentric target initiated before the end of the delay were not rewarded. A sub-anesthetic dose of ketamine (0.25 mg/kg) or a saline solution of the same volume was injected i.m. during the task. RESULTS: We found that the injected dose of ketamine did not induce sedation or abnormal behavior. However, in ~4 minutes, ketamine induced a strong reduction of the occurrence of anticipatory saccades but did not reduce the occurrence of visually-guided saccades. CONCLUSION: This unexpected reduction of anticipatory saccade occurrence could be interpreted as resulting from an altered use of the perception of elapsed time during the delay period induced by NMDA receptors antagonism.

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.

A saccade triggered during sustained smooth pursuit is programmed using retinal information about the relative position and velocity of the target with respect to the eye. Thus the smooth pursuit and saccadic systems are coordinated by using common retinal inputs. Yet, in the absence of retinal information about the relative motion of the eye with respect to the target, the question arises whether the smooth and saccadic systems are still able to be coordinated possibly by using extraretinal information to account for the saccadic and smooth eye movements. To address this question, we flashed a target during smooth anticipatory eye movements in darkness, and the subjects were asked to orient their visual axis to the remembered location of the flash. We observed multiple orientation saccades (typically 2–3) toward the memorized location of the flash. The first orienting saccade was programmed using only the position error at the moment of the flash, and the smooth eye movement was ignored. However, subsequent saccades executed in darkness compensated gradually for the smooth eye displacement (mean compensation ≅ 70%). This behavior revealed a 400-ms delay in the time course of orientation for the compensation of the ongoing smooth eye displacement. We conclude that extraretinal information about the smooth motor command is available to the saccadic system in the absence of visual input. There is a 400-ms delay for smooth movement integration, saccade programming and execution.

The aim of the present study was to find out whether smooth eye movements (SEMs) evoked by superior colliculus (SC) stimulation are, as suggested by Breznen et al. (1996), artefactual eye movements resulting from a non-physiological response of the saccadic generator. This question was reinvestigated in head-restrained cats. Long-lasting SC stimulation was found to evoke, in a comparable proportion, either a single saccade followed by an uninterrupted SEM or a staircase of two or three saccades interleaved with SEMs. These two different patterns of eye movements could be elicited at a near-threshold current and at low stimulation frequencies. In most cases, SEM direction clearly differed from that of the preceding saccade. This difference between SEM and saccade directions varied in a systematic way as a function of the initial saccade direction. As demonstrated by computer simulation, this observation can be explained if the neural circuit controlling SEMs reaches a saturation level earlier than the saccadic burst-generator. Our results in cats were reminiscent of those reported by Breznen et al. (1996) in the monkey only in some instances, when high frequency stimulation (400-600 Hz) was applied. Indeed, in the case of near-threshold stimulation-elicited staircase saccades, increasing the stimulation frequency led to a progressive disappearance of the smaller subsequent saccades that were substituted by uninterrupted SEM-like movements. Altogether, the present results confirm the view that SEMs are genuine eye movements. These results rule out the hypothesis that SEMs result from a saturation of the saccadic generator and strengthen the hypothesis that SEMs and saccades are distinct movements. We suggest that the same collicular efferent cells carry out the motor command to saccadic and SEM circuits and that the position error originating from the SC may be distributed amongst separate downstream motor systems.

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°/s) in the contribution of retinal slip to the amplitude of catch-up saccades.

When tracking moving visual stimuli, primates orient their visual axis by combining two kinds of eye movements, smooth pursuit and saccades, that have very different dynamics. Yet, the mechanisms that govern the decision to switch from one type of eye movement to the other are still poorly understood, even though they could bring a significant contribution to the understanding of how the CNS combines different kinds of control strategies to achieve a common motor and sensory goal. In this study, we investigated the oculomotor responses to a large range of different combinations of position error and velocity error during visual tracking of moving stimuli in humans. We found that the oculomotor system uses a prediction of the time at which the eye trajectory will cross the target, defined as the “eye crossing time” ( T XE). The eye crossing time, which depends on both position error and velocity error, is the criterion used to switch between smooth and saccadic pursuit, i.e., to trigger catch-up saccades. On average, for T XEbetween 40 and 180 ms, no saccade is triggered and target tracking remains purely smooth. Conversely, when T XEbecomes smaller than 40 ms or larger than 180 ms, a saccade is triggered after a short latency (around 125 ms).

If a visual object of interest suddenly starts to move, we will try to follow it with a smooth movement of the eyes. This smooth pursuit response aims to reduce image motion on the retina that could blur visual perception. In recent years, our knowledge of the neural control of smooth pursuit initiation has sharply increased. However, stopping smooth pursuit eye movements is less well understood and will be discussed in this paper. The most straightforward way to study smooth pursuit stopping is by interrupting image motion on the retina. This causes eye velocity to decay exponentially towards zero. However, smooth pursuit stopping is not a passive response, as shown by behavioural and electrophysiological evidence. Moreover, smooth pursuit stopping is particularly influenced by active prediction of the upcoming end of the target. Here, we suggest that a particular class of inhibitory neurons of the brainstem, the omnipause neurons, could play a central role in pursuit stopping. Furthermore, the role of supplementary eye fields of the frontal cortex in smooth pursuit stopping is also discussed. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

The passage of time can be estimated either explicitly, e.g. before leaving home in the morning, or implicitly, e.g. when catching a flying ball. In the present study, the latency of saccadic eye movements was used to evaluate differences between implicit and explicit timing. Humans were required to make a saccade between a central and a peripheral position on a computer screen. The delay between the extinction of a central target and the appearance of an eccentric target was the independent variable that could take one out of four different values (400, 900, 1400 or 1900 ms). In target trials, the delay period lasted for one of the four durations randomly. At the end of the delay, a saccade was initiated by the appearance of an eccentric target. Cue&target trials were similar to target trials but the duration of the delay was visually cued. In probe trials, the duration of the upcoming delay was cued, but there was no eccentric target and subjects had to internally generate a saccade at the estimated end of the delay. In target and cue&target trials, the mean and variance of latency distributions decreased as delay duration increased. In cue&target trials latencies were shorter. In probe trials, the variance increased with increasing delay duration and scalar variability was observed. The major differences in saccadic latency distributions were observed between visually-guided (target and cue&target trials) and internally-generated saccades (probe trials). In target and cue&target trials the timing of the response was implicit. In probe trials, the timing of the response was internally-generated and explicitly based on the duration of the visual cue. Scalar timing was observed only during probe trials. This study supports the hypothesis that there is no ubiquitous timing system in the brain but independent timing processes active depending on task demands.

Anticipatory eye movements are often evoked by the temporal expectation of an upcoming event. Temporal expectation is based on implicit timing about when a future event could occur. Implicit timing emerges from observed temporal regularities in a changing stimulus without any voluntary estimate of elapsed time, unlike explicit timing. The neural bases of explicit and implicit timing are likely different. It has been shown that the basal ganglia (BG) play a central role in explicit timing. In order to determine the influence of BG in implicit timing, we investigated the influence of early Parkinson’s disease (PD) and aging on the latency of anticipatory eye movements. We hypothesized that a deficit of implicit timing should yield inadequate temporal expectations, and consequently abnormally timed anticipatory eye movements compared with age-matched controls. To test this hypothesis, we used an oculomotor paradigm where anticipation of a salient target event plays a central role. Participants pursued a visual target that moved along a circular path at a constant velocity. After a randomly short (1200 ms) or long (2400 ms) forward path, the target reversed direction, returned to its starting position and stopped. Target motion reversal caused an abrupt "slip" of the pursued target image on the retina and was a particularly salient event evoking anticipatory eye movements. Anticipatory eye movements were less frequent in PD patients. However, the timing of anticipation of target motion reversal was statistically similar in PD patients and control subjects. Other eye movements showed statistically significant differences between PD and controls, but these differences could be attributed to other factors. We conclude that all anticipatory eye movements are not similarly impaired in PD and that implicit timing of salient events seems largely unaffected by this disease. The results support the hypothesis that implicit and explicit timing are differently affected by BG dysfunction.

When two objects such as billiard balls collide, observers perceive that the action of one caused the motion of the other. We have previously shown (Badler, Lefèvre, & Missal, 2010) that this extends to the oculomotor domain: subjects make more predictive movements in the expected direction of causal motion than in a noncausal direction. However, predictive oculomotor and reactive psychophysical responses have never been directly compared. They should be correlated if they tap into the same mental processes. To test this, we recorded oculomotor responses to launching stimuli, then asked subjects to manually classify those stimuli as causal or noncausal. Overall the psychophysical classifications matched the oculomotor biases, although correlations across subjects were mostly absent. In subsequent experiments, 50% of the trials had a 300-millisecond delay after the collision to impede the perception of causality. Subjects maintained their causal oculomotor bias but used different classification strategies, usually grouping the stimuli either by delay or by direction. In addition, there was no evidence that the two response types were correlated on a trial-by-trial basis. The results suggest divergent processes underlying oculomotor responses to and judgments of causal stimuli.

Recent experimental results show evidence for the corrective role of postsaccadic drifts. This paper addresses the modeling of these slow correcting gaze movements (SCMs). Classical arguments to explain drifts are presented, both in the head fixed condition (pulse-step mismatch) and in the head free condition (vestibulo-ocular reflex (VOR)). The most significant behavioral and electrophysiological experimental data related to SCMs are then briefly reported, with the conclusion that SCMs have a clear corrective role, incompatible with classical explanations of drifts. Based on these experimental data, existing models of the saccadic system are then compared. A theoretical comparison of the classical Robinson model with an alternative model is proposed. Two possible (slow and fast) pathways involved in the control of SCMs are examined, and simulation results are presented. Finally, the discussion addresses the observed species differences in SCMs. The link between natural SCMs and electrical SC stimulations, and the interactions between saccades, VOR, and SCMs are also discussed.

Feeling the beat and meter is fundamental to the experience of music. However, how these periodicities are represented in the brain remains largely unknown. Here, we test whether this function emerges from the entrainment of neurons resonating to the beat and meter. We recorded the electroencephalogram while participants listened to a musical beat and imagined a binary or a ternary meter on this beat (i.e., a march or a waltz). We found that the beat elicits a sustained periodic EEG response tuned to the beat frequency. Most importantly, we found that meter imagery elicits an additional frequency tuned to the corresponding metric interpretation of this beat. These results provide compelling evidence that neural entrainment to beat and meter can be captured directly in the electroencephalogram. More generally, our results suggest that music constitutes a unique context to explore entrainment phenomena in dynamic cognitive processing at the level of neural networks.

When viewing one object move after being struck by another, humans perceive that the action of the first object “caused” the motion of the second, not that the two events occurred independently. Although established as a perceptual and linguistic concept, it is not yet known whether the notion of causality exists as a fundamental, preattentional “Gestalt” that can influence predictive motor processes. Therefore, eye movements of human observers were measured while viewing a display in which a launcher impacted a tool to trigger the motion of a second “reaction” target. The reaction target could move either in the direction predicted by transfer of momentum after the collision (“causal”) or in a different direction (“noncausal”), with equal probability. Control trials were also performed with identical target motion, either with a 100 ms time delay between the collision and reactive motion, or without the interposed tool. Subjects made significantly more predictive movements (smooth pursuit and saccades) in the causal direction during standard trials, and smooth pursuit latencies were also shorter overall. These trends were reduced or absent in control trials. In addition, pursuit latencies in the noncausal direction were longer during standard trials than during control trials. The results show that causal context has a strong influence on predictive movements.

Visually guided catch-up saccades during the pursuit of a moving target are highly influenced by smooth pursuit performance. For example, the decision to execute a saccade and its amplitude is driven by the difference in velocity between the eye and the target. In previous studies, we have demonstrated that the predictive saccades that occur during the blanking of the moving target compensate for the variability of the smooth pursuit response. Therefore, we wondered whether the predictive smooth pursuit response during target blanking influenced the occurrence of predictive saccades, which is the case for visually guided catch-up saccades. To answer this question, we asked subjects to track visually a target moving along a circular path. From time to time, the target was unexpectedly blanked for some randomized durations and disappeared from the screen. Surprisingly, we did not find any differences in smooth pursuit performance between the blanks that did and those that did not contain predictive saccades. In addition, during the blanks, the differences in smooth pursuit performance across the sessions or across the subjects did not correlate with the differences in the number of predictive saccades. Therefore, this study demonstrates that smooth pursuit performance does not influence the occurrence of predictive saccades. We interpret these results in light of the possible minimization of position error at target reappearance, which heavily depends on the saccadic amplitudes but not on their timing. ispartof: Journal of Vision vol:9 issue:11 pages:7- ispartof: location:United States status: published

The ability to predict upcoming events is important to compensate for relatively long sensory-motor delays. When stimuli are temporally regular, their prediction depends on a representation of elapsed time. However, it is well known that the allocation of attention to the timing of an upcoming event alters this representation. The role of attention on the temporal processing component of prediction was investigated in a visual smooth pursuit task that was performed either in isolation or concurrently with a manual response task. Subjects used smooth pursuit eye movements to accurately track a moving target after a constant-duration delay interval. In the manual response task, subjects had to estimate the instant of target motion onset by pressing a button. The onset of anticipatory pursuit eye movements was used to quantify the subject's estimate of elapsed time. We found that onset times were delayed significantly in the presence of the concurrent manual task relative to the pursuit task in isolation. There was also a correlation between the oculomotor and manual response latencies. In the framework of Scalar Timing Theory, the results are consistent with a centralized attentional gating mechanism that allocates clock resources between smooth pursuit preparation and the parallel timing task.

The timing of an upcoming event depends on two factors: its temporal position, proximal or distal with respect to the present moment, and the unavoidable stochastic variability around this temporal position. We searched for a general mechanism that could describe how these two factors influence the anticipation of an upcoming event in an oculomotor task. Monkeys were trained to pursue a moving target with their eyes. During a delay period inserted before target motion onset, anticipatory pursuit responses were frequently observed. We found that anticipatory movements were altered by the temporal position of the target. Increasing the timing uncertainty associated with the stimulus resulted in an increase in the width of the latency distribution of anticipatory pursuit. These results show that monkeys relied on an estimation of the changing probability of target motion onset as time elapsed during the delay to decide when to initiate an anticipatory smooth eye movement.

To organise behaviors, the brain makes predictions from past experience. Addicted subjects, who persist in consuming despite negative consequences, may be unable to learn from past experience. Anticipatory oculomotor movements can be accurately studied in with eye tracking techniques and may serve as an index of procedural learning processes. …

A classic paradigm to study anticipatory pursuit consists in training monkeys to look at a target that appears in the center of a visual display, disappears during a short “gap” period, then reappears and immediately starts to move. To determine the role of prior directional information on anticipatory pursuit eye movements, we trained rhesus monkeys to associate the color of a centrally presented visual cue with the direction of an upcoming target motion. In a first experiment, a gap period occurred randomly in 50% of the trials. Consequently, two possible choices of timing of target motion onset were given to subjects to guide their anticipatory responses. In a second experiment, a gap period occurred during each trial and only a single choice of timing of target motion onset was given to subjects. We found that monkeys used the learned association between the color of the cue and the direction of future target motion to voluntarily initiate anticipatory pursuit movements in the appropriate direction. Anticipatory movements could be classified in two distinct populations: early and late movements. Early movements were most frequent when prior directional information was provided and when two choices of timing of target motion onset were given. The latency of visual pursuit was shortened and its velocity was larger when prior directional information was provided. We conclude that cognitive expectation of future target motion plays a dominant role in determining characteristics of anticipatory pursuit in the monkey.

The influence of position and motion signals on saccades was studied in two dimensions (2D) using a double step-ramp paradigm. We showed the presence of a predictive component in 2D catch-up saccade programming that is based on motion signals and influences both saccade amplitude and orientation. Interestingly, a significant proportion of catch-up saccades was characterized by a large curvature or a sudden change of direction in midflight for large values of retinal slip. For these saccades, a quantitative analysis showed that their trajectory could be explained by an asynchrony between position and motion signals in saccade programming. When the saccade trajectory was not straight, position error was always available first and influenced the initial orientation of the saccade, whereas retinal slip determined the final orientation. This new paradigm could be used in electrophysiological experiments, where it should prove to be very useful to study position and motion pathways separately in catch-up saccades.

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 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.

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.

A long-standing belief holds that the saccadic and smooth-pursuit eye movement systems are composed of largely separate premotor circuits, at least in the brainstem. One crucial prediction predicated on this belief is that the tonic discharge of omnipause neurons (OPNs), which are thought to be part of only the saccadic system, should not be modulated during pursuit eye movements. This report shows that the discharge of OPNs, in contradiction, is modulated downward during pursuit movements. In contrast to their behavior during saccades, where they pause completely for the duration of the movement, the downward modulation during pursuit did not totally silence OPNs. The depth of the downward modulation was correlated with the speed of the ongoing pursuit movement. Another type of cell, which we have named saccade/pursuit neurons, was recorded in the paramedian pontine reticular formation near the location of OPNs. This subpopulation of burst cells discharged a cascade of spikes for saccades in a preferred direction. They also displayed a lower-frequency sustained discharge of spikes for the duration of pursuit in the same preferred direction. These data suggest a new type of combined model for the organization of the brainstem saccade/pursuit system. In this new combined model, the OPNs form a common inhibitory mechanism for both types of movements, and the saccade/pursuit neurons participate in the eye-velocity modulation of OPN discharge or membrane polarization during either type of movement.

Briefly flashed visual stimuli presented during smooth object- or self-motion are systematically mislocalized. This phenomenon is called the "flash-lag effect" (Nijhawan, 1994). All previous studies had one common characteristic, the subject's sense of motion. Here we asked whether motion perception is a necessary condition for the flash-lag effect to occur. In our first experiment, we briefly flashed a target during smooth anticipatory eye movements in darkness and subjects had to orient their gaze toward the perceived flash position. Subjects reported to have no sense of eye motion during anticipatory movements. In our second experiment, subjects had to adjust a cursor on the perceived position of the flash. As a result, we show that gaze orientation reflects the actual perceived flash position. Furthermore, a flash-lag effect is present despite the absence of motion perception. Moreover, the time course of gaze orientation shows that the flash-lag effect appeared immediately after the egocentric to allocentric reference frame transformation.

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.

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 ∼20%. At most sites, the threshold for a significant facilitation was 50 μA 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.

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

Differences between gaze shifts evoked by collicular electrical stimulation and those triggered by the presentation of a visual stimulus were studied in head-free cats by increasing the head moment of inertia. This maneuver modified the dynamics of these two types of gaze shifts by slowing down head movements. Such an increase in the head moment of inertia did not affect the metrics of visually evoked gaze saccades because their duration was precisely adjusted to compensate for these changes in movement dynamics. In contrast, the duration of electrically evoked gaze shifts remained constant irrespective of the head moment of inertia, and therefore their amplitude was significantly reduced. These results suggest that visually and electrically evoked gaze saccades are controlled by different mechanisms. Whereas the accuracy of visually evoked saccades is likely to be assured by on-line feedback information, the absence of duration adjustment in electrically evoked gaze shifts suggests that feedback information necessary to maintain their metrics is not accessible or is corrupted during collicular stimulation. This is of great importance when these two types of movements are compared to infer the role of the superior colliculus in the control of orienting gaze shifts.

Missal et al. observed that the responses of inferior temporal (IT) neurons to a shape were reduced markedly when this shape partially overlapped a larger second shape, suggesting that shape interactions determine IT responses. In the present study, we compared the responses of IT neurons with combinations of two shapes which did or did not overlap and studied the effect of the relative and absolute positions of the two shapes. In a first test, a preferred shape (figure) was presented at the fixation point while a second, nonpreferred, shape was displayed either in the background of the figure (overlap) or at one of four peripheral positions (nonoverlap). Controls consisted of presentations of either shape in isolation at each of the five positions. The stimuli were presented during a fixation task. The responses to these combinations of two shapes were, on average, reduced compared with those elicited by the preferred shape presented in isolation. This suppression occurred whether or not the two shapes overlapped, but the degree of suppression in the overlap and nonoverlap conditions did not correlate. These interactions were stronger when the interacting stimulus was located in the contralateral compared with the ipsilateral hemifield. The position of the interacting stimulus within a hemifield significantly affected the suppression associated with combined shapes in some neurons. The strength of the interactions of the two nonoverlapping shapes depended on the shape of the interacting stimulus in half of the neurons. In a second test, the preferred shape and interacting stimulus could appear either at the fixation point or at one eccentric position. Here we found that the suppression was, on average, strongest when the interacting stimulus, rather than the preferred shape, was presented at the fixation position. Also, in 40% of the neurons, the response reduction was similar in overlap and nonoverlap conditions if effects of stimulus position were taken into account. In both tests, we also measured the responses to combinations of a nonpreferred shape and the interacting stimulus and showed that the response to a combination of two nonpreferred shapes was, in general, smaller than the response to a combination of the preferred and nonpreferred shape. Overall the results indicate that stimulus interactions in the receptive fields of IT neurons can be position and shape selective; this can contribute to the coding for the relationships between object parts.

We tested whether macaque inferior temporal neurons can signal the presence of their preferred shape independently of other shapes simultaneously present, by comparing the responses and selectivity of TE neurons to shapes (figures), either presented in isolation or overlapping another shape (background). The two overlapping shapes differed in color or texture and thus were easily segmentable. We found that the response and selectivity of TE neurons to the figure can be dramatically altered, most commonly reduced, when the figure is overlapping the background. This reduction in response was also present when the monkey was required to actively discriminate the figures from varying backgrounds during recording. The level of suppression depended on the shape of the background and on whether or not figure and background can be discriminated. These results indicate that responses of TE cells are not only determined by the properties of the figures but also are influenced by the properties of stimuli in the background.

Head-fixed gaze shifts were evoked by electrical stimulation of the deeper layers of the cat superior colliculus (SC). After a short latency, saccades were triggered with kinematics similar to those of visually guided saccades. When electrical stimulation was maintained for more than 150-200 ms, postsaccadic smooth eye movements (SEMs) were observed. These movements were characterized by a period of approximately constant velocity following the evoked saccade. Depending on electrode position, a single saccade followed by a slow displacement or a "staircase" of saccades interspersed by SEMs were evoked. Mean velocity decreased with increasing deviation of the eye in the orbit in the direction of the movement. In the situation where a single evoked saccade was followed by a smooth movement, the duration of the latter depended on the duration of the stimulation train. In the situation where evoked saccades converged towards a restricted region of the visual field ("goal"-directed or craniocentric saccades), the SEMs were directed towards the centre of this region and their mean velocity decreased as the eye approached the goal. The direction of induced SEMs depended on the site of stimulation, as is the case for saccadic eye movements, and was not modified by stimulation parameters ("place" code). On the other hand, mean velocity of the movements depended on the site of stimulation and on the frequency and intensity of the current ("rate" code), as reported for saccades in the cat. The kinematics of these postsaccadic SEMs are similar to the kinematics of slow, postsaccadic correction observed during visually triggered gaze shifts of the alert cat. These results support the hypothesis that the SC is not exclusively implicated in the control of fast refixation of gaze but also in controlling postsaccadic conjugate slow eye movements in the cat.

The orientation of the line of sight (gaze) is necessary for the exploration of the visual environment. Classically, eye movements are divided into two broad categories: movements that orient gaze, and movements that stabilise gaze. Stabilisation of gaze is accomplished by the combined actions of the vestibulo-ocular and the optokinetic reflexes. Orientation is performed by saccades, smooth pursuit and vergence. In each of these categories, eye movements can be subdivided into fast (typically quick phases or saccades) or slow (typically slow phases or smooth pursuit) movements. Neurophysiologically, the control of fast and slow eye movements is considered to be performed by different structures.