Anticipatory Smooth Pursuit Eye Movements Research Articles

The role of knowledge of Newtonian mechanics in anticipatory smooth pursuit eye movements

The role of knowledge of Newtonian mechanics in anticipatory smooth pursuit eye movements

Reinforcement effects in anticipatory smooth eye movements.

When predictive information about target motion is available, anticipatory smooth pursuit eye movements (aSPEM) are consistently generated before target appearance, thereby reducing the typical sensorimotor delay between target motion onset and foveation. By manipulating the probability for target motion direction, we were able to bias the direction and mean velocity of aSPEM. This suggests that motion-direction expectancy has a strong effect on the initiation of anticipatory movements. To further understand the nature of anticipatory smooth eye movements, we investigated different effects of reinforcement on aSPEM. In a first experiment, the reinforcement was contingent to a particular anticipatory behavior. A monetary reward was associated to a criterion-matching anticipatory velocity as estimated online during the gap before target motion onset. Our results showed a small but significant effect of behavior-contingent monetary reward on aSPEM. In a second experiment, the proportion of rewarded trials was manipulated across motion directions (right vs. left) independently from participants' behavior. Our results indicate that a bias in expected reward does not systematically affect anticipatory eye movements. Overall, these findings strengthen the notion that anticipatory eye movements can be considered as an operant behavior (similar to visually guided ones), whereas the expectancy for a noncontingent reward cannot efficiently bias them.

Anticipatory smooth pursuit eye movements evoked by probabilistic cues.

Anticipatory smooth eye movements (ASEM; smooth eye movements in the direction of anticipated target motion) are elicited by cues that signal the direction of future target motion with high levels of certainty. Natural cues, however, rarely convey information with perfect certainty, and responses to uncertainty provide insights about how predictive behaviors are generated. Subjects smoothly pursued targets that moved to the right or left with varying cued probabilities. ASEM strength in a given direction increased with the probability level. The type of cue also played a role. ASEM elicited by symbolic visual cues tended to underweight low probabilities and overweight high probabilities. Cues based on memory (varying the proportion of trials with left or right motion) produced the opposite pattern, overweighting low probabilities and underweighting high probabilities. Finally, cues whose perceptual structure depicted the motion path produced a bias in ASEM in the depicted direction that was maintained across levels of cue congruency. The results show that the smooth pursuit system relies on a combination of signals, including memory for recent target motions, interpretation of cues, and prior beliefs about the relationship between the perceptual configuration and the motion path to determine the anticipatory response in the presence of uncertainty.

Operant reinforcement versus reward expectancy: effects on anticipatory eye movements

When an object is moving in the visual field, we are able to accurately track it with a combination of saccades and smooth eye movements. These movements allow us to align and stabilize the object on the fovea, thus enabling visual analysis with high acuity. Importantly, when predictive information is available about the target motion, anticipatory smooth pursuit eye movements (aSPEM) are efficiently generated before target appearance, which reduces the typical sensorimotor delay between target motion onset and foveation. By manipulating the probability for target motion direction we were able to bias the direction and mean velocity of aSPEM (baseline condition). This suggests that probabilistic information may be used to inform the internal representation of motion prediction for the initiation of anticipatory movements. To further understand the nature of this process, we investigate the effects of reinforcement on aSPEM with two distinct experiments. First, it has been previously shown that several properties of eye movements can be modulated by reinforcement paradigms based on monetary reward (Madelain et al. 2011). We adapted and extended this framework to prediction-based aSPEM, by associating a monetary reward to a criterion-matching anticipatory velocity, in the gap before the target onset. Second, it has also been reported that accurate perception per se can play the role of an efficient ecological reinforcer for visually guided saccades (Montagnini & Chelazzi, 2005). With a gaze-contingent procedure, we manipulated the discriminability of a perceptual target (Appearing at the end of a pursuit trial and followed by a discrimination task). The difficulty level of this task has been matched depending on the velocity of aSPEM. This experiment taps on the very reason to produce anticipatory tracking movement, that is to grant a quicker high-acuity vision of the moving target. We compare predictive anticipatory eye movements across these conditions. Meeting abstract presented at VSS 2015.

Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

To compute spatially correct smooth pursuit eye movements, the brain uses both retinal motion and extraretinal signals about the eyes and head in space (Blohm and Lefèvre 2010). However, when smooth eye movements rely solely on memorized target velocity, such as during anticipatory pursuit, it is unknown if this velocity memory also accounts for extraretinal information, such as head roll and ocular torsion. To answer this question, we used a novel behavioral updating paradigm in which participants pursued a repetitive, spatially constant fixation-gap-ramp stimulus in series of five trials. During the first four trials, participants' heads were rolled toward one shoulder, inducing ocular counterroll (OCR). With each repetition, participants increased their anticipatory pursuit gain, indicating a robust encoding of velocity memory. On the fifth trial, they rolled their heads to the opposite shoulder before pursuit, also inducing changes in ocular torsion. Consequently, for spatially accurate anticipatory pursuit, the velocity memory had to be updated across changes in head roll and ocular torsion. We tested how the velocity memory accounted for head roll and OCR by observing the effects of changes to these signals on anticipatory trajectories of the memory decoding (fifth) trials. We found that anticipatory pursuit was updated for changes in head roll; however, we observed no evidence of compensation for OCR, representing the absence of ocular torsion signals within the velocity memory. This indicated that the directional component of the memory must be coded retinally and updated to account for changes in head roll, but not OCR.

Anticipatory smooth pursuit eye movements in response to global motion

Anticipatory smooth pursuit eye movements in response to global motion

Scaling of anticipatory smooth pursuit eye movements with target speed probability

References Direction randomization Anticipatory smooth pursuit permits tracking of expected target trajectories with little delay. It can be a mirror of cognitive expectations, but It is still unclear how these expectations are built. Pursuit anticipation scales with several target parameters in an adaptive way [1]. This is compatible, for instance, with a switch between expectation states after one or several wrong guesses [2].Alternatively, the underlying mechanism could rely on a global subjective probability estimation.

Anticipating uncertain events: estimates of probability driving anticipatory eye movements

Introduction Animal and human sensorimotor behavior is influenced by expecting that a particular event will occur. Such expectancy is likely to rely on an internal estimation of the probability of occurrence of different events. Furthermore, expectancy can affect several aspects of the behavioral response, like reaction times [1], visuomotor gain [2] and anticipatory motor responses [3]. In this study, we analyze anticipatory smooth pursuit eye movements as a function of the relative probability of occurrence of different target motion types. Smooth pursuit eye movements (SPEM) permit the stabilization of the image of moving targets on the retina. In humans, visually guided SPEM start typically with a 100 ms latency with respect to target motion onset, leading to an initial lag of the eye relative to the target position (retinal error) and speed (retinal slip). Anticipatory SPEM (aSPEM) can be initiated some hundreds of milliseconds before target onset when the motion characteristics are totally or partially predictable and they might help reduce retinal error and slip.

Active linear head motion improves dynamic visual acuity in pursuing a high-speed moving object

We usually move both our eyes and our head when pursuing a high-speed moving object. However, the vestibulo-ocular reflex (VOR), evoked by head motion, seems to disturb smooth pursuit eye movement because the VOR stabilizes the gaze against head motion. To determine whether head motion is advantageous for pursuing a high-speed moving object, we examined dynamic visual acuity (DVA) for a high-speed (80 degrees /s) rightward moving object with and without active linear rightward head motion (HM) at a maximum of 50 cm/s in nine healthy subjects. Furthermore, we analyzed eye and head movements to investigate the contribution of linear VOR (LVOR) and smooth eye movement under these conditions. In most subjects, active linear head motion improved DVA for a high-speed moving object. Subjects with higher DVA scores under HM had robust rightward gaze (eye + head) velocities (>60 cm/s), i.e., rightward smooth eye movements (>10 degrees /s). With the head stationary (HS), faster smooth eye movements (>40 degrees /s) were generated when the subjects pursued a high-speed moving object. They also showed anticipatory smooth eye movements under conditions HM and HS. However, the level of suppression of their LVOR abilities was equal to that of the others. These results suggest that the ability to generate anticipatory smooth pursuit eye movements for following a high-speed moving object against the LVOR is a determining factor for improvement of DVA under HM.

Anticipatory smooth-pursuit eye movements in man and monkey

A fundamental problem in the generation of goal-directed behaviour is caused by the inevitable latency of biological sensory systems. Behaviour which is fully synchronised with the triggering sensory event can only be executed if the occurrence of this event can be predicted based on prior information. Smooth-pursuit eye movements are a classical and well-established example of goal-directed behaviour. The execution of these eye movements is thought to be very closely linked to the processing of visual motion signals. Here, we show that healthy human subjects as well as trained rhesus monkeys are able to initiate smooth-pursuit eye movements in anticipation of a moving target. These anticipatory pursuit eye movements are scaled to the velocity of the expected target. Furthermore, we can exclude the possibility that anticipatory pursuit is simply an after-pursuit of the previous trial. Visually-guided pursuit is only marginally affected by the presence of a structured background. However, the presence of a structured background severely impedes the ability to perform anticipatory pursuit. More generally, our data provide additional evidence that the cognitive oculomotor repertoires of human and monkeys are similar, at least with respect of smooth-pursuit in the prediction of an appearing target.

Visual-tracking neurons in area MST are activated during anticipatory pursuit eye movements.

Here, I report that rhesus monkeys are able to generate anticipatory smooth pursuit eye movements in the transient absence of a moving target, if this target moves periodically. The eye velocity before target reappearance was significantly larger if the target trajectory was predictable compared with the control condition consisting of unpredictable target trajectory. Parallel to the registration of the eye movements, single-unit activity was recorded from neurons in the middle superior temporal (MST) area of the two monkeys. The neuronal activity of visual-tracking neurons resembled the observed eye movements, i.e. these neurons increased their activity earlier if the movement of the target was predictable compared with the unpredictable control. These results provide further evidence for the existence of extra-retinal signals in the activity of visual-tracking neurons located in area MST.

Sequence learning in human ocular smooth pursuit

It has been established that repeated presentation of a transient target motion stimulus such as a constant-velocity ramp leads to the build up of steady state (SS), anticipatory smooth pursuit eye movements after two or three presentations. Each SS response is then composed of the anticipatory component of nonvisual origin, a visual component associated with the stimulus presentation and another nonvisual component that represents the decay of the response after extinction of the stimulus. Here we investigated the interactions that occur when each motion stimulus was itself a sequence containing more than one ramp component. Ramp components had a velocity of 15 degrees /s or 30 degrees /s to left or right and were separated by gaps of 200 ms duration. In an initial experiment, responses to 2-ramp stimuli were examined and compared with responses to the single-ramp stimuli from which they were constituted. We present evidence that the anticipatory, nonvisual components of the double-ramp response result from the linear summation of the nonvisual components of the responses to the constituent single-ramp components. In a 2nd experiment, we examined responses to a wide variety of 4-ramp sequences and again found evidence that, in the SS, the responses were formed from the linear summation of the constituent single-ramp components. Regression analysis performed on the velocity at onset of each ramp component indicated that this nonvisual part of the response was predictive of the upcoming ramp component. To confirm this, unexpected changes were introduced into single ramp components of the 4-ramp sequence after at least five prior presentations of the sequence had allowed a SS response to be established. Subjects continued to initiate a response to the modified component that was appropriate in velocity and direction for the corresponding part of the previous sequence and inappropriate for the newly modified stimulus. This preprogrammed response persisted unmodified for more than 170 ms after onset of the modified ramp component. In contrast, in the second presentation of the new sequence, the anticipatory component of the response was highly correlated with the SS response of the new sequence, but not with that of the prior sequence, showing that the preprogrammed response had been modified very rapidly. Similar behaviour was observed whichever of the 4-ramp components was modified, indicating that the velocity and direction of the anticipatory response to each component had been preprogrammed. The results suggest that velocity information related to at least four elements of a sequence can be temporarily stored and subsequently released with appropriate temporal order to form an anticipatory response throughout the whole sequence.

Volitional selection of direction in the generation of anticipatory ocular smooth pursuit in humans

Anticipatory smooth pursuit eye movements cannot normally be generated in the absence of a moving target. However, repeated presentation of identical target motion stimuli, preceded by warning cues, leads to the build up of anticipatory smooth pursuit prior to target onset. These anticipatory responses arguably depend more on motor habit than cognitive expectations. Here, we show that directional cues, concomitant with a timing cue, may be used to initiate predictive (velocity scaled) movements in response to target stimuli of random direction. Furthermore, we show stored velocity and timing information may be directionally transferred, thus allowing predictive movements in a novel direction. This demonstrates the internal origin of these movements and their volitional as opposed to reflexive nature.