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Psychophysical, motor control, and modeling studies have revealed that sensorimotor reference frame transformations (RFTs) add variability to transformed signals. For perceptual decision-making, this phenomenon could decrease the fidelity of a decision signal's representation or alternatively improve its processing through stochastic facilitation. We investigated these two hypotheses under various sensorimotor RFT constraints. Participants performed a time-limited, forced-choice motion discrimination task under eight combinations of head roll and/or stimulus rotation while responding either with a saccade or button press. This paradigm, together with the use of a decision model, allowed us to parameterize and correlate perceptual decision behavior with eye-, head-, and shoulder-centered sensory and motor reference frames. Misalignments between sensory and motor reference frames produced systematic changes in reaction time and response accuracy. For some conditions, these changes were consistent with a degradation of motion evidence commensurate with a decrease in stimulus strength in our model framework. Differences in participant performance were explained by a continuum of eye-head-shoulder representations of accumulated motion evidence, with an eye-centered bias during saccades and a shoulder-centered bias during button presses. In addition, we observed evidence for stochastic facilitation during head-rolled conditions (i.e., head roll resulted in faster, more accurate decisions in oblique motion for a given stimulus-response misalignment). We show that perceptual decision-making and stochastic RFTs are inseparable within the present context. We show that by simply rolling one's head, perceptual decision-making is altered in a way that is predicted by stochastic RFTs.

A fundamental problem in motor control is the coordination of complementary movement types to achieve a common goal. As a common example, humans view moving objects through coordinated pursuit and saccadic eye movements. Pursuit is initiated and continuously controlled by retinal image velocity. During pursuit, eye position may lag behind the target. This can be compensated by the discrete execution of a catch-up saccade. The decision to trigger a saccade is influenced by both position and velocity errors, and the timing of saccades can be highly variable. The observed distributions of saccade frequency and trigger time remain poorly understood, and this decision process remains imprecisely quantified. Here, we propose a predictive, probabilistic model explaining the decision to trigger saccades during pursuit to foveate moving targets. In this model, expected position error and its associated uncertainty are predicted through Bayesian inference across noisy, delayed sensory observations (Kalman filtering). This probabilistic prediction is used to estimate the confidence that a saccade is needed (quantified through log-probability ratio), triggering a saccade upon accumulating to a fixed threshold. The model qualitatively explains behavioral observations on the frequency and trigger time distributions of saccades during pursuit over a range of target motion trajectories. Furthermore, this model makes novel predictions that saccade decisions are highly sensitive to uncertainty for small predicted position errors, but this influence diminishes as the magnitude of predicted position error increases. We suggest that this predictive, confidence-based decision-making strategy represents a fundamental principle for the probabilistic neural control of coordinated movements. NEW & NOTEWORTHY This is the first stochastic dynamical systems model of pursuit-saccade coordination accounting for noise and delays in the sensorimotor system. The model uses Bayesian inference to predictively estimate visual motion, triggering saccades when confidence in predicted position error accumulates to a threshold. This model explains saccade frequency and trigger time distributions across target trajectories and makes novel predictions about the influence of sensory uncertainty in saccade decisions during pursuit.

For humans, visual tracking of moving stimuli often triggers catch-up saccades during smooth pursuit. The switch between these continuous and discrete eye movements is a trade-off between tolerating sustained position error (PE) when no saccade is triggered or a transient loss of vision during the saccade due to saccadic suppression. de Brouwer et al. (2002b) demonstrated that catch-up saccades were less likely to occur when the target re-crosses the fovea within 40-180 ms. To date, there is no mechanistic explanation for how the trigger decision is made by the brain. Recently, we proposed a stochastic decision model for saccade triggering during visual tracking (Coutinho et al., 2018) that relies on a probabilistic estimate of predicted PE (PE pred ). Informed by model predictions, we hypothesized that saccade trigger time length and variability will increase when pre-saccadic predicted errors are small or visual uncertainty is high (e.g., for blurred targets). Data collected from human participants performing a double step-ramp task showed that large pre-saccadic PE pred (>10°) produced short saccade trigger times regardless of the level of uncertainty while saccade trigger times preceded by small PE pred (<10°) significantly increased in length and variability, and more so for blurred targets. Our model also predicted increased signal-dependent noise (SDN) as retinal slip (RS) increases; in our data, this resulted in longer saccade trigger times and more smooth trials without saccades. In summary, our data supports our hypothesized predicted error-based decision process for coordinating saccades during smooth pursuit., (Copyright © 2020 Nachmani et al.)

Combination of signals based on their reliability is an increasingly popular model for sensorimotor processing. However, how reliability is estimated, or how such estimation is affected by prolonged exposure to noisy inputs, is still unknown. In this study, we compare patients with unilateral functional amblyopia with control subjects tracking either a reliable target, or a blurry, unreliable target, in a task of repeated, sustained smooth pursuit. We provide evidence for a lower weight of visual information during smooth pursuit in amblyopic and control subjects tracking a blurry target, with no significant difference of prior information weight. In contrast, we found no evidence of lower visual information weight in the catch-up saccades of amblyopic subjects. We conclude that oculomotor performance in unilateral amblyopia mostly lays within the continuum between our control groups, without significant differences in the relative weights of prior and visual information. However, smooth pursuit exhibits additional deficits that might result from abnormal visual development., (© 2019 Elsevier B.V. All rights reserved.)

Oculomotor behaviors integrate sensory and prior information to overcome sensory-motor delays and noise. After much debate about this process, reliability-based integration has recently been proposed and several models of smooth pursuit now include recurrent Bayesian integration or Kalman filtering. However, there is a lack of behavioral evidence in humans supporting these theoretical predictions. Here, we independently manipulated the reliability of visual and prior information in a smooth pursuit task. Our results show that both smooth pursuit eye velocity and catch-up saccade amplitude were modulated by visual and prior information reliability. We interpret these findings as the continuous reliability-based integration of a short-term memory of target motion with visual information, which support modeling work. Furthermore, we suggest that saccadic and pursuit systems share this short-term memory. We propose that this short-term memory of target motion is quickly built and continuously updated, and constitutes a general building block present in all sensorimotor systems.

The prediction of the consequences of our own actions through internal models is an essential component of motor control. Previous studies showed improvement of anticipatory behaviors with age for grasping, drawing, and postural control. Since these actions require visual and proprioceptive feedback, these improvements might reflect both the development of internal models and the feedback control. In contrast, visual tracking of a temporarily invisible target gives specific markers of prediction and internal models for eye movements. Therefore, we recorded eye movements in 50 children (aged 5-19 yr) and in 10 adults, who were asked to pursue a visual target that is temporarily blanked. Results show that the youngest children (5-7 yr) have a general oculomotor behavior in this task, qualitatively similar to the one observed in adults. However, the overall performance of older subjects in terms of accuracy at target reappearance and variability in their behavior was much better than the youngest children. This late maturation of predictive mechanisms with age was reflected into the development of the accuracy of the internal models governing the synergy between the saccadic and pursuit systems with age. Altogether, we hypothesize that the maturation of the interaction between smooth pursuit and saccades that relies on internal models of the eye and target displacement is related to the continuous maturation of the cerebellum., (Copyright © 2016 the American Physiological Society.)

Coordinating the movements of different body parts is a challenging process for the central nervous system because of several problems. Four of these main difficulties are: first, moving one part can move others; second, the parts can have different dynamics; third, some parts can have different motor goals; and fourth, some parts may be perturbed by outside forces. Here, we propose a novel approach for the control of linked systems with feedback loops for each part. The proximal parts have separate goals, but critically the most distal part has only the common goal. We apply this new control policy to eye-head coordination in two-dimensions, specifically head-unrestrained gaze saccades. Paradoxically, the hierarchical structure has controllers for the gaze and the head, but not for the eye (the most distal part). Our simulations demonstrate that the proposed control structure reproduces much of the published empirical data about gaze movements, e.g., it compensates for perturbations, accurately reaches goals for gaze and head from arbitrary initial positions, simulates the nine relationships of the head-unrestrained main sequence, and reproduces observations from lesion and single-unit recording experiments. We conclude by showing how our model can be easily extended to control structures with more linked segments, such as the control of coordinated eye on head on trunk movements.

Motor skills improve with age from childhood into adulthood, and this improvement is reflected in the performance of smooth pursuit eye movements. In contrast, the saccadic system becomes mature earlier than the smooth pursuit system. Therefore, the present study investigates whether the early mature saccadic system compensates for the lower pursuit performance during childhood. To answer this question, horizontal eye movements were recorded in 58 children (ages 5-16 yr) and 16 adults (ages 23-36 yr) in a task that required the combination of smooth pursuit and saccadic eye movements. Smooth pursuit performance improved with age. However, children had larger average position error during target tracking compared with adults, but they did not execute more saccades to compensate for their low pursuit performance despite the early maturity of their saccadic system. This absence of error correction suggests that children have a lower sensitivity to visual errors compared with adults. This reduced sensitivity might stem from poor internal models and longer processing time in young children.

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.

Disconjugate oculomotor adaptation is driven by the need to maintain binocular vision. Since binocular vision in Duane Retraction Syndrome (DRS) patients is normal in half of their horizontal field of gaze (i.e., sound-side of gaze), we wondered whether oculomotor adaptive capabilities are efficient despite such a severe impairment of eye motility towards the other half of the horizontal field of gaze (i.e., affected-side gaze). We compared properties of horizontal saccades of patients with congenital unilateral Duane Retraction Syndrome type I in binocular viewing and monocular viewing conditions by simultaneously recording both eyes with the search coil technique. Our results show a mismatch between the pulse and the step signal of the innervation for saccades. When tested in the affected eye viewing condition (sound eye covered), the eyes showed not only similarly-directed increases of the saccadic gain (pulse signal) in the two eyes but also disjunctive post-saccadic drifts (step signal). This behavior suggests that visuomotor errors presented only to the affected eye were transferred to the sound eye, producing conjugate changes of the saccadic command. The post-saccadic command remained unchanged, however, and controlled the final position of each eye separately. This suggests that monocular adaptation is possible only for the step of innervation (i.e., controlling the final eye position) but not for the pulse of innervation (i.e., controlling the saccadic gain), even though the peculiarity of unilateral DRS type I offers a clear advantage for separate pathways of control for the two eyes.

Saccades and smooth pursuit eye movements are two different modes of oculomotor control. Saccades are primarily directed toward stationary targets whereas smooth pursuit is elicited to track moving targets. In recent years, behavioural and neurophysiological data demonstrated that both types of eye movements work in synergy for visual tracking. This suggests that saccades and pursuit are two outcomes of a single sensorimotor process that aims at orienting the visual axis.

Given sufficient exposure to stimulus presentation, the oculomotor system generates a representation of the stimulus characteristics, which is then used to predict the upcoming target motion. In addition to compensating for the perceptual-motor delay, these predictive processes perpetuate eye motion during a transient occlusion and compensate for the loss of visual input. At present, however, it is not well understood whether and how the oculomotor system extracts and represents target acceleration for subsequent predictive control. To this end, we used a target occlusion paradigm where both position and velocity of the target during the occlusion and at reappearance could not be predicted without extracting target acceleration before target disappearance. We found that the oculomotor response during the blanking period was not influenced by target acceleration when the initial exposure was 200 ms. However, smooth and saccadic eye movements did discriminate between the different levels of acceleration after an initial 500- or 800-ms exposure. In the event that the smooth response during the occlusion did not match well the target trajectory and thus eliminate a developing displacement error, there was an increased saccadic displacement. Still, the combined response during the blanking period did not eliminate retinal slip and position error at target reappearance. These results indicate that information on target acceleration can be extracted on-line, during pursuit of a visible ramp, and then used to drive a predictive oculomotor response in the absence of visual input.

Past results have reported conflicting findings on the oculomotor system's ability to keep track of smooth eye movements in darkness. Whereas some results indicate that saccades cannot compensate for smooth eye displacements, others report that memory-guided saccades during smooth pursuit are spatially correct. Recently, it was shown that the amount of time before the saccade made a difference: short-latency saccades were retinotopically coded, whereas long-latency saccades were spatially coded. Here, we propose a model of the saccadic system that can explain the available experimental data. The novel part of this model consists of a delayed integration of efferent smooth eye velocity commands. Two alternative physiologically realistic neural mechanisms for this integration stage are proposed. Model simulations accurately reproduced prior findings. Thus, this model reconciles the earlier contradictory reports from the literature about compensation for smooth eye movements before saccades because it involves a slow integration process.

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.

Visual tracking of moving objects requires prediction to compensate for visual delays and minimize mismatches between eye and target position and velocity. In everyday life, objects often disappear behind an occluder, and prediction is required to align eye and target at reappearance. Earlier studies investigating eye motion during target blanking showed that eye velocity first decayed after disappearance but was sustained or often recovered in a predictive way. Furthermore, saccades were directed toward the unseen target trajectory and therefore appeared to correct for position errors resulting from eye velocity decay. To investigate the synergy between smooth and saccadic eye movements, this study used a target blanking paradigm where both position and velocity of the target at reappearance could vary independently but were presented repeatedly to facilitate prediction. We found that eye velocity at target reappearance was only influenced by expected target velocity, whereas saccades responded to the expected change of target position at reappearance. Moreover, subjects exhibited on-line adaptation, on a trial-by-trial basis, between smooth and saccadic components; i.e., saccades compensated for variability of smooth eye displacement during the blanking period such that gaze at target reappearance was independent of the level of smooth eye displacement. We suggest these results indicate that information arising from efference copies of saccadic and smooth pursuit systems are combined with the goal of adjusting eye position at target reappearance. Based on prior experimental evidence, we hypothesize that this spatial remapping is carried out through interactions between a number of identified neurophysiological structures.

Purpose: To improve understanding of the binocular control of saccades by making high-resolution eye movement recordings in patients with unilateral Duane retraction syndrome (DRS) type I (marked by congenital absence of the sixth cranial nerve)., Methods: Binocular eye movements were recorded in four patients in binocular viewing conditions during a saccade task., Results: Affected-side gaze showed normal saccades of the sound eye and undershooting saccades of the affected eye-evidence of intact interneurons, but deficient motoneurons, in the sixth-nerve nucleus on the affected side. Postsaccadic smooth onward drift followed undershooting saccades of the affected eye. Sound-side gaze, in the centripetal direction, showed relatively accurate saccades despite large offsets in initial position between the two eyes. In the centrifugal direction, there was a consistent undershoot of the affected eye. The sound eye showed unexpected overshoot. Postsaccadic drifts in opposite directions in the two eyes brought both eyes onto the target in an optimal time course., Conclusions: Studying the characteristics of the saccadic system in this oculomotor disorder gives new insight into binocular control of saccades and adaptation. In these patients, the oculomotor system was not capable of adapting the pulse command to the two eyes separately, even though DRS offers clear advantages of independent control. In contrast, independent adaptation of the saccadic step command was sent to the two eyes. This supports the idea that the rapid part of the saccadic command is common to both eyes.

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.

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

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.

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 congruent with 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.

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

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(XE) between 40 and 180 ms, no saccade is triggered and target tracking remains purely smooth. Conversely, when T(XE) becomes smaller than 40 ms or larger than 180 ms, a saccade is triggered after a short latency (around 125 ms).

Abstract: In view of all the reported evidence by electromyography in the 1970s, by histology in the 1980s, and by cerebral imagery since the 2000s, Duane retraction syndrome (DRS) has been described as the consequence of a congenital anomaly of the 6th cranial nerve nuclei with aberrant innervations by supply from the 3rd cranial nerve. Both genetic and environmental factors are likely to play a role when the cranial nerves and ocular muscles are developing between the 4th and the 8th week of gestation. New data from eye movement recordings contributed to better understanding the binocular control of saccades. Modeling of saccades in DRS seems promising for the quantification of the innervational deficit and the mechanical properties of the eye plant. The usual clinical classification of DRS needs to be updated in order to match more accurately the underlying dysinnervation of the extra ocular muscles and to illustrate the continuum that exists between the various forms. This review aims to summarize the major findings about DRS and to guide the clinician in the surgical management of this particular form of strabismus. [Copyright &y& Elsevier]

Autism has been considered as a deficit in prediction of the upcoming event or of the sensory consequences of our own movements. To test this hypothesis, we recorded eye movements from high-functioning autistic adolescents and from age-matched controls during a blanking paradigm. In this paradigm, adolescents were instructed to follow a moving target with their eyes even during its transient disappearance. Given the absence of visual information during the blanking period, eye movements during this period are solely controlled on the basis of the prediction of the ongoing target motion. Typical markers of predictive eye movements such as the number and accuracy of predictive saccades and the predictive reacceleration before target reappearance were identical in the two populations. In addition, the synergy of predictive saccades and smooth pursuit observed during the blanking periods, which is a marker for the quality of internal models about target/eye motions, was comparable between these two populations. These results suggest that, in our large population of high-functioning autistic adolescent, both predictive abilities and internal models are left intact in Autism, at least for low-level sensorimotor transformations. [ABSTRACT FROM AUTHOR]