Saccadic initiation biased by fixational activity.

Both the gap and overlap paradigm may reveal the interaction between fixating and moving the eyes, but the effects of the overlap paradigm have not been fully characterized yet. Here we present a series of experiments probing how an overlap paradigm, combined with the manipulation of stimuli durations, saliency and transient changes might modulate saccadic reaction time distributions. We recorded saccadic reaction time in four participants in six experiments in which a saccade-target appeared at a pseudo-random amplitude after a fixation period. First, we parametrically manipulated the duration of the overlap using a range of intervals (from 0 to 200 ms). In a second experiment we probed the interaction of various foreperiod intervals (i.e. the duration of the fixation period prior to saccade-target onset) and overlap using two overlap intervals (20 or 140 ms). In two additional experiments we manipulated either the stimuli sizes or their contrast ratio in overlap paradigms (20 or 140 ms). Lastly, we introduced a visual transient during the overlap interval via two manipulations (both with a range of SOA): either a distractor ring appeared around the fixation-target, or a dynamic random noise patch replaced the fixation-target. Results show reliable modifications in the latency distributions depending on the overlap interval as well as idiosyncratic differences. Additional experimental manipulations also affected the latency distributions revealing strong interacting inhibitory processes. We conclude that the effects of overlap intervals may combine with the influence of other stimuli properties affecting decision process.

Perception of saccadic reaction time.

That saccadic reaction times (SRTs) may depend on reinforcement contingencies has been repeatedly demonstrated. It follows that one must be able to discriminate one's latencies to adequately assign credit to one's actions, which is to connect behaviour to its consequence. To quantify the ability to perceive one's SRT, we used an adaptive procedure to train sixteen participants in a stepping visual target saccade paradigm. Subsequently, we measured their RTs perceptual threshold at 75% in a conventional constant stimuli procedure. For each trial, observers had to saccade to a stepping target. Then, in a 2-AFC task, they had to choose one value representing the actual SRT, while the other value proportionally differed from the actual SRT. The relative difference between the two alternatives was computed by either adding or subtracting from the actual SRT a percent-difference value randomly chosen among a fixed set. Feedback signalling the correct choice was provided after each response. Overall, our results showed that the 75% SRT perceptual threshold averaged 23% (about 40 ms). The ability to discriminate small SRT differences provides support for the possibility that the credit assignment problem may be solved even for short reaction times.

Irrelevant auditory and tactile signals, but not visual signals, interact with the target onset and modulate saccade latencies.

Saccadic eye movements bring events of interest to the center of the retina, enabling detailed visual analysis. This study explored whether irrelevant auditory (experiments A, B & F), visual (C & D) or tactile signals (E & F) delivered around the onset of a visual target modulates saccade latency. Participants were instructed to execute a quick saccade toward a target stepping left or right from a fixation position. We observed an interaction between auditory beeps or tactile vibrations and the oculomotor reaction that included two components: a warning effect resulting in faster saccades when the signal and the target were presented simultaneously; and a modulation effect with shorter-or longer-latencies when auditory and tactile signals were delivered before-or after-the target onset. Combining both modalities only increased the modulation effect to a limited extent, pointing to a saturation of the multisensory interaction with the motor control. Interestingly, irrelevant visual stimuli (black background or isoluminant noise strips in peripheral vision, flashed for 10 ms) increased saccade latency whether they were presented just before or after target onset. The lack of latency reduction with visual signals suggests that the modulation observed in the auditory and tactile experiments was not related to priming effects but rather to low-level audio- and tactile-visual integration. The increase in saccade latency observed with irrelevant visual stimuli is discussed in relation to saccadic inhibition. Our results demonstrate that signals conveying no information regarding where and when a visual target would appear modulate saccadic reactivity, much like in multisensory temporal binding, but only when these signals come from a different modality.

Prediction and final temporal errors are used for trial-to-trial motor corrections.

Many daily life situations (e.g. dodging an approaching object or hitting a moving target) require people to correct planning of future movements based on previous temporal errors. However, the actual temporal error can be difficult to perceive: imagine a baseball batter that swings and misses a fastball. Here we show that in such situations people can use an internal error signal to make corrections in the next trial. This signal is based on the discrepancy between the actual and the planned action onset time: the prediction error. In this study, we used three interception tasks: reaching movements, saccadic eye movements and a button press that released a cursor moving ballistically for a fixed time. We found that action onset depended on the previous temporal error in the arm movement experiment only and not in the saccadic and button press experiments. However, this dependency was modulated by the movement time: faster arm movements depended less on the previous actual temporal error. An analysis using a Kalman filter confirmed that people used the prediction error rather than the previous temporal error for trial-by-trial corrections in fast arm movements, saccades and button press.

Inter-individual variability and consistency of saccade adaptation in oblique saccades: Amplitude increase and decrease in the horizontal or vertical saccade component.

Despite changes in the physical structures controlling the eyes, saccades, the rapid eye movements used to explore the visual environment, remain accurate throughout the lifetime. The process underlying this sensorimotor adaptation is studied using a double step paradigm: an intra-saccadic target displacement introduces a systematic position error which triggers changes in saccadic amplitude or direction across trials. Numerous researches on this saccade adaptation have been conducted, but the level of inter-individual variability and consistency in saccade gain change and how it relates to increase- or decrease-amplitude paradigms is not fully described. We conducted experiments in four groups of 25 participants with 800 trials per participant, including 200 baseline trials and 200 recovery trials. We used four distinct double-step paradigms that differed by the intra-saccadic target-step leading to either a horizontal (Backward or Forward) or vertical (Upward or Downward) gain modulation. Across experiments 95% of the participants exhibited adaptation, revealing the consistency of this phenomenon. We observed strong inter-individual differences, both in the extent and rate of adaptation, which were not correlated with the individual baseline saccades characteristics. As previously reported, the rates of adaptation were higher for gain decrease than for gain increase experiments but the final extent of adaptation were similar. Our results also support the view that adaptation of oblique saccades occurs where the saccade command is represented as a vector. Finally, at the individual level, we did not observe systematic changes in the saccade metrics in relation to adaptation.

Reinforcement reduces the size-latency phenomenon: A cost-benefit evaluation of saccade triggering.

Saccadic latencies are known to change as a function of target eccentricity and size. Recently, it has been shown that latencies consistently change according to the amplitude of the step in proportion to the size of the target (Madelain, Krauzlis, & Wallman, 2005; Harwood, Madelain, Krauzlis, & Wallman, 2008; De Vries, Azadi, & Harwood, 2016). This effect, called the size-latency phenomenon, might be seen as a function of a cost-benefit relationship: Longer latencies might be explained by the lower benefit of making a saccade while the target mostly remains within the attentional field. Here, we probe this hypothesis by manipulating the cost-benefit relationship using a reinforcement procedure. Participants tracked a target stepping horizontally with varying amplitudes and sizes such that the step-to-size ratio was equal to either 0.3 or 1.5. We used a dynamic-reinforcement criterion in the blocked conditions. In the 0.3-ratio condition, any latency shorter than the criterion was reinforced. In the 1.5-ratio condition, any latency longer than the criterion was reinforced. During baseline, we observed the size-latency effect with large differences in latencies depending on the ratio in force (229 and 161 ms, respectively, for 0.3 and 1.5). After learning, distributions shifted toward the shorter or longer value (198 and 236 ms, respectively, for 0.3 and 1.5). On average, latencies decreased by 31 ms and increased by 75 ms according to the ongoing reinforcement contingencies. Our results indicate that reinforcement contingencies can considerably affect saccadic-latency distributions, and support the idea of a cost-benefit evaluation of saccade triggering.

Discriminative control of saccade latencies.

Recent studies have demonstrated that saccadic reaction times (SRTs) are influenced by the temporal regularities of dynamic environments (Vullings & Madelain, 2018). Here, we ask whether discriminative control (i.e., the possibility to use external stimuli signaling the future state of the environment) of latencies in a search task might be established using reinforcement contingencies. Eight participants made saccades within 80-750 ms toward a target displayed among distractors. We constructed two latency classes, "short" and "long," using the first and last quartiles of the individual baseline distributions. We then used a latency-contingent display paradigm in which finding the visual target among other items was made contingent upon specific SRTs. For a first group, the postsaccadic target was displayed only following short latencies with leftward saccades, and following long latencies with rightward saccades. The opposite was true for a second group. When short- and long-latency saccades were reinforced (i.e., the target was displayed) depending on the saccade direction, median latencies differed by 74 ms on average (all outside the 98% null hypothesis confidence intervals). Posttraining, in the absence of reinforcement, we still observed strong differences in latency distributions, averaging 64 ms for leftward versus rightward saccades. Our results demonstrate the discriminative control of SRTs, further supporting the effects of reinforcement learning for saccade. This study reveals that saccade triggering is finely controlled by learned temporal and spatial properties of the environment using predictive mechanisms.

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.

Control of saccadic latency in a dynamic environment: allocation of saccades in time follows the matching law.

When exploring the visual environment, one uses saccades to shift gaze and fixation to gather spatially and temporally localized information. We propose that the temporal structure of our environment should constrain the temporal allocation of saccades. Here we probe the possibility of learning to control saccadic latencies in a choice paradigm. Six participants made saccades within 80-300 ms following a target horizontally stepping by 10° between two fixed locations. For each participant we constructed two classes of latencies, "short" and "long," using the first and last quartiles of the individual baseline distribution (e.g., [80;152] ms and [185;300] ms, respectively). We then concurrently reinforced each class in three blocked conditions across ~60 experimental sessions per participant, using different reinforcement probabilities such that the relative ratio of reinforcement rates for short vs. long latencies was 9/1, 1/9, or 1/1. Latency distributions followed the reinforcement conditions: distributions shifted toward the shorter or longer values or became strongly bimodal. Moreover, the relative rates of short over long latencies matched the relative rates of reinforcers earned for the corresponding latencies (slope up to 0.95), which reveals the ability to choose when to saccade. Our results reveal that learned contingencies considerably affect the allocation of saccades in time and are in line with recent studies on the temporal adjustment of behavior to dynamic environments. This study provides strong evidence for fine operant control of saccadic latency, supporting the hypothesis of a cost-benefit control of saccade latencies. NEW & NOTEWORTHY Saccades may be regarded as an information-foraging behavior mostly concerned with the spatial localization of objects, yet our world is dynamic and environmental temporal regularities should also affect saccade decisions. We present behavioral data from a choice task establishing that humans can learn to choose their saccadic latencies depending on the reinforcement contingencies. This suggests a cost-benefit-based policy that takes into account the learned temporal properties of the environmental contingencies for controlling saccade triggering.

Eye tracking a self-moved target with complex hand-target dynamics.

Previous work has shown that the ability to track with the eye a moving target is substantially improved when the target is self-moved by the subject's hand compared with when being externally moved. Here, we explored a situation in which the mapping between hand movement and target motion was perturbed by simulating an elastic relationship between the hand and target. Our objective was to determine whether the predictive mechanisms driving eye-hand coordination could be updated to accommodate this complex hand-target dynamics. To fully appreciate the behavioral effects of this perturbation, we compared eye tracking performance when self-moving a target with a rigid mapping (simple) and a spring mapping as well as when the subject tracked target trajectories that he/she had previously generated when using the rigid or spring mapping. Concerning the rigid mapping, our results confirmed that smooth pursuit was more accurate when the target was self-moved than externally moved. In contrast, with the spring mapping, eye tracking had initially similar low spatial accuracy (though shorter temporal lag) in the self versus externally moved conditions. However, within ∼5 min of practice, smooth pursuit improved in the self-moved spring condition, up to a level similar to the self-moved rigid condition. Subsequently, when the mapping unexpectedly switched from spring to rigid, the eye initially followed the expected target trajectory and not the real one, thereby suggesting that subjects used an internal representation of the new hand-target dynamics. Overall, these results emphasize the stunning adaptability of smooth pursuit when self-maneuvering objects with complex dynamics.

Reinforcing saccadic amplitude variability in a visual search task.

Human observers often adopt rigid scanning strategies in visual search tasks, even though this may lead to suboptimal performance. Here we ask whether specific levels of saccadic amplitude variability may be induced in a visual search task using reinforcement learning. We designed a new gaze-contingent visual foraging task in which finding a target among distractors was made contingent upon specific saccadic amplitudes. When saccades of rare amplitudes led to displaying the target, the U values (measuring uncertainty) increased by 54.89% on average. They decreased by 41.21% when reinforcing frequent amplitudes. In a noncontingent control group no consistent change in variability occurred. A second experiment revealed that this learning transferred to conventional visual search trials. These results provide experimental support for the importance of reinforcement learning for saccadic amplitude variability in visual search.

Saccade adaptation as a model of flexible and general motor learning.

The rapid point-to-point movements of the eyes called saccades are the most commonly made movement by humans, yet differ from nearly every other type of motor output in that they are completed too quickly to be adjusted during their execution by visual feedback. Saccadic accuracy remains quite high over a lifetime despite inevitable changes to the physical structures controlling the eyes, indicating that the oculomotor system actively monitors and adjusts motor commands to achieve consistent behavioral production. Indeed, it seems that beyond the ability to compensate for slow, age-related bodily changes, saccades can be modified following traumatic injury or pathology that affects their production, or in response to more short-term systematic alterations to post-saccadic visual feedback in a laboratory setting. These forms of plasticity rely on the visual detection of accuracy errors by a unified set of mechanisms that support the process known as saccade adaptation. Saccade adaptation has been mostly studied as a phenomenon in its own right, outside of motor learning in general. Here, we highlight the commonalities between eye and arm movement adaptation by reviewing the literature across these fields wherever there are compelling overlapping theories or data. Recent exciting findings are challenging previous interpretations of the underlying mechanisms of saccade adaptation with the incorporation of concepts including prediction, reinforcement and contextual learning. We review the emerging ideas and evidence with particular emphasis on the important contributions made by Josh Wallman in this sphere over the past 15 years.

Saccade adaptation goes for the goal.

The oculomotor system maintains saccade accuracy by adjusting saccades that are consistently inaccurate. Four experiments were performed to determine the relative contribution of background and target postsaccadic displacement. Unlike typical saccade adaptation experiments, we used natural image scenes and masked target and background displacements during the saccade to exclude motion signals from allowing detection of the displacements. We found that the background had no effect on saccade gain while the target drove gain changes. Only when the target was blanked after the saccade did we observe some adaptation in the direction of the background displacement. We conclude that target selection is critical to saccade adaptation, and operates effectively against natural image backgrounds.

Reinforcing saccadic amplitude variability.

Saccadic endpoint variability is often viewed as the outcome of neural noise occurring during sensorimotor processing. However, part of this variability might result from operant learning. We tested this hypothesis by reinforcing dispersions of saccadic amplitude distributions, while maintaining constant their medians. In a first experiment we reinforced the least frequent saccadic amplitudes to increase variability, and then reinforced the central part of the amplitude distributions to reduce variability. The target was placed at a constant distance from the fovea after the saccade to maintain the postsaccadic visual signal constant and an auditory reinforcement was delivered depending on saccadic amplitude. The second experiment tested the effects of the contingency. We reinforced high levels of variability in 4 participants, whereas 4 other participants were assigned to a yoked control group. On average, saccadic amplitude standard deviations were doubled while the medians remained mostly unchanged in the experimental participants in both experiments, and variability returned to baseline level when low variability was reinforced. In the control group no consistent changes in amplitude distributions were observed. These results, showing that variability can be reinforced, challenge the idea of a stochastic neural noise. We instead propose that selection processes constrain saccadic amplitude distributions.

Modification of saccadic gain by reinforcement.

Control of saccadic gain is often viewed as a simple compensatory process in which gain is adjusted over many trials by the postsaccadic retinal error, thereby maintaining saccadic accuracy. Here, we propose that gain might also be changed by a reinforcement process not requiring a visual error. To test this hypothesis, we used experimental paradigms in which retinal error was removed by extinguishing the target at the start of each saccade and either an auditory tone or the vision of the target on the fovea was provided as reinforcement after those saccades that met an amplitude criterion. These reinforcement procedures caused a progressive change in saccade amplitude in nearly all subjects, although the rate of adaptation differed greatly among subjects. When we reversed the contingencies and reinforced those saccades landing closer to the original target location, saccade gain changed back toward normal gain in most subjects. When subjects had saccades adapted first by reinforcement and a week later by conventional intrasaccadic step adaptation, both paradigms yielded similar degrees of gain changes and similar transfer to new amplitudes and to new starting positions of the target step as well as comparable rates of recovery. We interpret these changes in saccadic gain in the absence of postsaccadic retinal error as showing that saccade adaptation is not controlled by a single error signal. More generally, our findings suggest that normal saccade adaptation might involve general learning mechanisms rather than only specialized mechanisms for motor calibration.

Operant control of human eye movements.

Saccade and smooth pursuit are the eye movements used by primates to shift gaze. In this article we review evidence for the effects of reinforcement on several dimensions of these responses such as their latencies, velocities or amplitudes. We propose that these responses are operant behaviours controlled by their consequences on performance of visually guided tasks. Studying the conditions under which particular eye movement patterns might emerge from the cumulative effects of reinforcement provides critical insights about how motor responses are attuned to environmental exigencies.

Saccade adaptation is unhampered by distractors.

Saccade adaptation has been extensively studied using a paradigm in which a target is displaced during the saccade, inducing an adjustment in saccade amplitude or direction. These changes in saccade amplitude are widely considered to be controlled by the post-saccadic position of the target relative to the fovea. However, because such experiments generally employ only a single target on an otherwise blank screen, the question remains whether the same adaptation could occur if both the target and a similar distractor were present when the saccade landed. To investigate this issue, three experiments were conducted, in which the post-saccadic locations of the target and distractor were varied. Results showed that decreased amplitude adaptation, increased amplitude adaptation, and recovery from adaptation were controlled by the post-saccadic position of the target rather than the distractor. These results imply that target selection is critical to saccade adaptation.

The spatial scale of attention strongly modulates saccade latencies.

We have previously shown that when a stimulus consisting of two concentric rings moves, saccade latencies are much longer (by 150 ms) when attention is directed to the larger ring than to the smaller ring. Here, we investigated whether this effect can be explained by a deferral of the "cost" of making a saccade while the target remains inside the attentional field, or by purely visual factors (eccentricity or contrast). We found 1) latencies were shorter when attention was directed to small features irrespective of retinal eccentricity; 2) saccade latency distributions were systematically determined by the ratio between the amplitude of the stimulus step and the diameter of the attended ring: stimulus steps that were larger than the attended ring resulted in short latencies, whereas steps smaller than the attended ring resulted in proportionally longer and more variable latencies; 3) this effect was not seen in manual reaction times to the same target movement; and 4) suprathreshold changes in the contrast of targets, mimicking possible attentional effects on perceived contrast and saliency, had little effect on latency. We argue that the spatial scale of attention determines the urgency of saccade motor preparation processes by changing the rate and rate variability of the underlying decision signal, to defer the cost of saccades that result in little visual benefit.

Control of sensorimotor variability by consequences.

Studies of reaction-time distributions provide a useful quantitative approach to understand decision processes at the neural level and at the behavioral level. A strong relationship between the spread of latencies and the median is generally accepted even though there has been no attempt to disentangle experimentally these two parameters. Here we test the ability to independently control the median and the variability in reaction times. Reaction times were measured in human subjects instructed to make a discrimination between a target and a distractor in a 2AFC task. In a first experiment, saccadic latencies were measured. In a second experiment, we used manual response reaction times. Subjects were trained to produce four different reaction-time distributions. A reinforcing feedback was given depending on both the variability and the median of the latency distributions. When low variability was reinforced, the standard deviation (SD) of reaction-time distributions were reduced by a factor of two and when high variability was reinforced, the SD returned to baseline level. Our procedure independently affected the spread and the median of the distribution patterns. By fitting the latency distributions using the Reddi and Carpenter LATER model, we found that these effects could be simulated by changing the distribution of the noise affecting the decision process. Our results demonstrate that learned contingencies can affect reaction time variability and support the view that the so-called noise level in decision processes can undergo long-term changes.