Anticipatory Smooth Eye Movements Research Articles

The eyes anticipate where objects will move based on their shape

Imagine staring into a clear river, starving, desperately searching for a fish to spear and cook. You see a dark shape lurking beneath the surface. It doesn't resemble any sort of fish you've encountered before - but you're hungry. To catch it, you need to anticipate which way it will move when you lunge for it, to compensate for your own sensory and motor processing delays1,2,3. Yet you know nothing about the behaviour of this creature, and do not know in which direction it will try to escape. What cues do you then use to drive such anticipatory responses? Fortunately, many species4, including humans, have the remarkable ability to predict the directionality of objects based on their shape - even if they are unfamiliar and so we cannot rely on semantic knowledge about their movements5. While it is known that such directional inferences can guide attention5, we do not yet fully understand how such causal inferences are made, or the extent to which they enable anticipatory behaviours. Does the oculomotor system, which moves our eyes to optimise visual input, use directional inferences from shape to anticipate upcoming motion direction? Such anticipation is necessary to stabilise the moving object on the high-resolution fovea of the retina while tracking the shape, a primary goal of the oculomotor system6, and to guide any future interactions7,8. Here, we leveraged a well-known behaviour of the oculomotor system: anticipatory smooth eye movements (ASEM), where an increase in eye velocity is observed in the direction of a stimulus' expected motion, before the stimulus actually moves3, to show that the oculomotor system extracts directional information from shape, and uses this inference to predict and anticipate upcoming motion.

Predictability of visual motion speed and acceleration for anticipatory smooth eye movements

Predictability of visual motion speed and acceleration for anticipatory smooth eye movements

Changes in visual speed perception induced by anticipatory smooth eye movements.

Expectations about forthcoming visual motion shaped by observers' experiences are known to induce anticipatory smooth eye movements (ASEMs) and changes in visual perception. Previous studies have demonstrated discrete effects of expectations on the control of ASEM and perception. However, the tasks designed in those studies were not able to segregate the effects of expectations and execution of ASEM itself on perception. In the present study, we attempted to directly examine the effect of ASEM itself on visual speed perception with a two-alternative forced-choice (2AFC) task, in which observers were asked to track a pair of sequentially presented visual motion stimuli with their eyes and to judge whether the second stimulus (test stimulus) was faster or slower than the first (reference stimulus). Our results showed that observers' visual speed perception, quantified by a psychometric function, shifted according to ASEM velocity. This was the case even though there was no difference in the steady-state eye velocity. Further analyses revealed that the observers' perceptual decisions could be explained by a difference in the magnitude of retinal slip velocity in the initial phase of ocular tracking when the reference and test stimuli were presented, rather than in the steady-state phase. Our results provide psychophysical evidence of the importance of initial ocular tracking in visual speed perception and the strong impact of ASEM.NEW & NOTEWORTHY We provide psychophysical evidence that the execution of anticipatory smooth eye movement (ASEM) leads to underestimation of visual speed perception, that is, observers perceive the object motion velocity as slower than when ASEM is not induced, even though the performance of subsequent ocular tracking is comparable. Moreover, our results showed that such perceptual decisions regarding object motion velocity were derived from the ASEM-induced decrease in retinal slip velocity during the initial phase of ocular tracking.

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

Anticipatory smooth eye movements adapt to higher-order probabilistic structure of the environment

Anticipatory smooth eye movements adapt to higher-order probabilistic structure of the environment

Predictive Smooth Pursuit Eye Movements.

Smooth pursuit eye movements maintain the line of sight on smoothly moving targets. Although often studied as a response to sensory motion, pursuit anticipates changes in motion trajectories, thus reducing harmful consequences due to sensorimotor processing delays. Evidence for predictive pursuit includes (a) anticipatory smooth eye movements (ASEM) in the direction of expected future target motion that can be evoked by perceptual cues or by memory for recent motion, (b) pursuit during periods of target occlusion, and (c) improved accuracy of pursuit with self-generated or biologically realistic target motions. Predictive pursuit has been linked to neural activity in the frontal cortex and in sensory motion areas. As behavioral and neural evidence for predictive pursuit grows and statistically based models augment or replace linear systems approaches, pursuit is being regarded less as a reaction to immediate sensory motion and more as a predictive response, with retinal motion serving as one of a number of contributing cues.

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.

Dynamic modulation of volatility by reward contingencies: effects on anticipatory smooth eye movement

Dynamic modulation of volatility by reward contingencies: effects on anticipatory smooth eye movement

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.

Anticipatory smooth eye movements and reinforcement

Anticipatory smooth eye movements and reinforcement

Anticipatory smooth eye movements evoked by motor intentions

Anticipatory smooth eye movements evoked by motor intentions

Anticipatory smooth eye movements elicited by symbolic cues

Anticipatory smooth eye movements elicited by symbolic cues

Davida Teller Award Lecture 2013: the importance of prediction and anticipation in the control of smooth pursuit eye movements.

The ability of smooth pursuit eye movements to anticipate the future motion of targets has been known since the pioneering work of Dodge, Travis, and Fox (1930) and Westheimer (1954). This article reviews aspects of anticipatory smooth eye movements, focusing on the roles of the different internal or external cues that initiate anticipatory pursuit.We present new results showing that the anticipatory smooth eye movements evoked by different cues differ substantially, even when the cues are equivalent in the information conveyed about the direction of future target motion. Cues that convey an easily interpretable visualization of the motion path produce faster anticipatory smooth eye movements than the other cues tested, including symbols associated arbitrarily with the path, and the same target motion tested repeatedly over a block of trials. The differences among the cues may be understood within a common predictive framework in which the cues differ in the level of subjective certainty they provide about the future path. Pursuit may be driven by a combined signal in which immediate sensory motion, and the predictions about future motion generated by sets of cues, are weighted according to their respective levels of certainty. Anticipatory smooth eye movements, an overt indicator of expectations and predictions, may not be operating in isolation, but may be part of a global process in which the brain analyzes available cues, formulates predictions, and uses them to control perceptual, motor, and cognitive processes.

Anticipatory smooth eye movements in autism spectrum disorder.

Smooth pursuit eye movements are important for vision because they maintain the line of sight on targets that move smoothly within the visual field. Smooth pursuit is driven by neural representations of motion, including a surprisingly strong influence of high-level signals representing expected motion. We studied anticipatory smooth eye movements (defined as smooth eye movements in the direction of expected future motion) produced by salient visual cues in a group of high-functioning observers with Autism Spectrum Disorder (ASD), a condition that has been associated with difficulties in either generating predictions, or translating predictions into effective motor commands. Eye movements were recorded while participants pursued the motion of a disc that moved within an outline drawing of an inverted Y-shaped tube. The cue to the motion path was a visual barrier that blocked the untraveled branch (right or left) of the tube. ASD participants showed strong anticipatory smooth eye movements whose velocity was the same as that of a group of neurotypical participants. Anticipatory smooth eye movements appeared on the very first cued trial, indicating that trial-by-trial learning was not responsible for the responses. These results are significant because they show that anticipatory capacities are intact in high-functioning ASD in cases where the cue to the motion path is highly salient and unambiguous. Once the ability to generate anticipatory pursuit is demonstrated, the study of the anticipatory responses with a variety of types of cues provides a window into the perceptual or cognitive processes that underlie the interpretation of events in natural environments or social situations.

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 eye movements with random-dot kinematograms

Anticipatory smooth eye movements were studied in response to expectations of motion of random-dot kinematograms (RDKs). Dot lifetime was limited (52-208 ms) to prevent selection and tracking of the motion of local elements and to disrupt the perception of an object moving across space. Anticipatory smooth eye movements were found in response to cues signaling the future direction of global RDK motion, either prior to the onset of the RDK or prior to a change in its direction of motion. Cues signaling the lifetime of the dots were not effective. These results show that anticipatory smooth eye movements can be produced by expectations of global motion and do not require a sustained representation of an object or set of objects moving across space. At the same time, certain properties of global motion (direction) were more sensitive to cues than others (dot lifetime), suggesting that the rules by which prediction operates to influence pursuit may go beyond simple associations between cues and the upcoming motion of targets.

Anticipatory smooth eye movements with passive and actively-controlled target motions

Anticipatory smooth eye movements with passive and actively-controlled target motions

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.