Saccade Kinematics Research Articles

Contrasting speed-accuracy tradeoffs for eye and hand movements reveal the optimal nature of saccade kinematics.

In contrast to hand movements, the existence of a neural representation of saccade kinematics is unclear. Saccade kinematics is typically thought to be specified by motor error/desired displacement and generated by brain stem circuits that are not penetrable to voluntary control. We studied the influence of instructed hand movement velocity on the kinematics of saccades executed without explicit instructions. When the hand movement was slow the saccade velocity decreased, independent of saccade amplitude. We leveraged this modulation of saccade velocity to study the optimality of saccades (in terms of velocity and endpoint accuracy) in relation to the well-known speed-accuracy tradeoff that governs voluntary movements (Fitts' law). In contrast to hand movements that obeyed Fitts' law, normometric saccades exhibited the greatest endpoint accuracy and lower reaction times, relative to saccades accompanying slow and fast hand movements. In the slow condition, where saccade endpoint accuracy suffered, we observed that targets were more likely to be foveated by two saccades resulting in step-saccades. Interestingly, the endpoint accuracy was higher in two-saccade trials, compared with one-saccade trials in both the slow and fast conditions. This indicates that step-saccades are a part of the kinematic plan for optimal control of endpoint accuracy. Taken together, these findings suggest normometric saccades are already optimized to maximize endpoint accuracy and the modulation of saccade velocity by hand velocity is likely to reflect the sharing of kinematic plans between the two effectors.NEW & NOTEWORTHY The optimality of saccade kinematics has been suggested by modeling studies but experimental evidence is lacking. However, we observed that, when subjects voluntarily modulated their hand velocity, the velocity of saccades accompanying these hand movements was also modulated, suggesting a shared kinematic plan for eye and hand movements. We leveraged this modulation to show that saccades had less endpoint accuracy when their velocity decreased, illustrating that normometric saccades have optimal speed and accuracy.

A spiking neural network model of the midbrain superior colliculus that generates saccadic motor commands

Single-unit recordings suggest that the midbrain superior colliculus (SC) acts as an optimal controller for saccadic gaze shifts. The SC is proposed to be the site within the visuomotor system where the nonlinear spatial-to-temporal transformation is carried out: the population encodes the intended saccade vector by its location in the motor map (spatial), and its trajectory and velocity by the distribution of firing rates (temporal). The neurons’ burst profiles vary systematically with their anatomical positions and intended saccade vectors, to account for the nonlinear main-sequence kinematics of saccades. Yet, the underlying collicular mechanisms that could result in these firing patterns are inaccessible to current neurobiological techniques. Here, we propose a simple spiking neural network model that reproduces the spike trains of saccade-related cells in the intermediate and deep SC layers during saccades. The model assumes that SC neurons have distinct biophysical properties for spike generation that depend on their anatomical position in combination with a center–surround lateral connectivity. Both factors are needed to account for the observed firing patterns. Our model offers a basis for neuronal algorithms for spatiotemporal transformations and bio-inspired optimal controllers.

The same oculomotor vermal Purkinje cells encode the different kinematics of saccades and of smooth pursuit eye movements

Saccades and smooth pursuit eye movements (SPEM) are two types of goal-directed eye movements whose kinematics differ profoundly, a fact that may have contributed to the notion that the underlying cerebellar substrates are separated. However, it is suggested that some Purkinje cells (PCs) in the oculomotor vermis (OMV) of monkey cerebellum may be involved in both saccades and SPEM, a puzzling finding in view of the different kinematic demands of the two types of eye movements. Such ‘dual’ OMV PCs might be oddities with little if any functional relevance. On the other hand, they might be representatives of a generic mechanism serving as common ground for saccades and SPEM. In our present study, we found that both saccade- and SPEM-related responses of individual PCs could be predicted well by linear combinations of eye acceleration, velocity and position. The relative weights of the contributions that these three kinematic parameters made depended on the type of eye movement. Whereas in the case of saccades eye position was the most important independent variable, it was velocity in the case of SPEM. This dissociation is in accordance with standard models of saccades and SPEM control which emphasize eye position and velocity respectively as the relevant controlled state variables.

Cognitive Control of Saccadic Eye Movements in Children with Developmental Coordination Disorder.

The ability to use advance information to prepare and execute a movement requires cognitive control of behaviour (e.g., anticipation and inhibition). Our aim was to explore the integrity of saccadic eye movement control in developmental coordination disorder (DCD) and typically developing (TD) children (8–12 years) and assess how these children plan and inhibit saccadic responses, the principal mechanisms within visual attention control. Eye movements and touch responses were measured (separately and concurrently) in Cued and Non-Cued conditions. We found that children with DCD had similar saccade kinematics to the TD group during saccade initiation. Advance information decreased hand movement duration in both groups during Cued trials, but decrements in accuracy were significantly worse in the DCD group. In addition, children with DCD exhibited greater inhibitory errors and inaccurate fixation during the Cued trials. Thus, children with DCD were reasonably proficient in executing saccades during reflexive (Non-Cued) conditions, but showed deficits in more complex control processes involving prediction and inhibition. These findings have implications for our understanding of motor control in children with DCD.

Fitts’ Theorem in Oculomotor Control: Dissociable Movement Times for Amplitude and Width Manipulations

ABSTRACTThe authors examined whether movement times (MT) for discrete saccades are constant given equivalent index of difficulty (ID) values (i.e., unitary nature of Fitts’ theorem). To that end, we contrasted ID/MT relations for saccades equated for ID but differing with respect to their target amplitudes and widths. Results showed that MT increased with increasing ID within amplitude and width conditions; however, the ID/MT slope was markedly steeper in the former condition. Thus, the amplitude condition imposed greater information processing demands than the width condition—a result indicating that the constituent elements of Fitts’ theorem are dissociable (i.e., nonunitary). Further, examination of saccade kinematics demonstrated that the optimal MT for a given target amplitude was largely independent of target width.

Meaningful images produce stronger saccadic adaptation

Saccades are made to scan interesting objects in the environment with foveal vision. In the lab, however, they are usually studied with meaningless point targets. Recent experiments showed that vision of a meaningful target affects saccade kinematics, accuracy, and latency. We investigated whether saccadic adaptation, a gradual change of amplitude when the target is shifted during the saccade, is affected by the content of the target. We expected that the motivation to land accurately on a target may be stronger if the target was not a point but a meaningful picture. Thirty-four subjects (27 female) participated in a scanning outward adaptation experiment in which 4 targets (1.8°x2.8°) in rectangular arrangement had to be viewed successively. One of the targets was a small image of a human figure. A control target contained random noise matched for luminance and spatial frequency. The stimulus set shifted in saccade direction during each horizontal saccade by 33% of the initial target distance (12°). In different conditions, stimuli either remained visible throughout the experiment, or were masked after saccade onset, or 200 ms later. Adaptation was quantified by computing the Gain Change (GC) ((amplitudelate-amplitudepre)/initial target distance) for each subject, which was then averaged according to experimental condition. The results showed that saccadic adaptation was greater for saccades directed towards meaningful pictures than towards noise (GChuman 14.14 %, GCnoise 10.83 %). This was also true when the images were masked 200ms after saccade onset such that only a brief glimpse could be obtained (GChuman 13.13%, GCnoise 09.68 %). When images were masked at saccade onset, no significant difference in adaptation was observed (GChuman 10.48%, GCnoise 10.76 %). We conclude that the post-saccadic view of a meaningful image at the saccade landing position facilitates saccadic adaptation. Meeting abstract presented at VSS 2015

Micro and regular saccades across the lifespan during a visual search of “Where’s Waldo” puzzles

Despite the fact that different aspects of visual-motor control mature at different rates and aging is associated with declines in both sensory and motor function, little is known about the relationship between microsaccades and either development or aging. Using a sample of 343 individuals ranging in age from 4 to 66 and a task that has been shown to elicit a high frequency of microsaccades (solving Where’s Waldo puzzles), we explored microsaccade frequency and kinematics (main sequence curves) as a function of age. Taking advantage of the large size of our dataset (183,893 saccades), we also address (a) the saccade amplitude limit at which video eye trackers are able to accurately measure microsaccades and (b) the degree and consistency of saccade kinematics at varying amplitudes and directions. Using a modification of the Engbert–Mergenthaler saccade detector, we found that even the smallest amplitude movements (0.25–0.5°) demonstrate basic saccade kinematics. With regard to development and aging, both microsaccade and regular saccade frequency exhibited a very small increase across the life span. Visual search ability, as per many other aspects of visual performance, exhibited a U-shaped function over the lifespan. Finally, both large horizontal and moderate vertical directional biases were detected for all saccade sizes.

The kinematics of far-near re-fixation saccades.

We have analyzed the three-dimensional spatiotemporal characteristics of saccadic refixations between far and near targets in three behaviorally trained rhesus monkeys. The kinematics underlying these rapid eye movements can be accurately described by rotations of the eyes in four different planes, namely, first disconjugate rotations in the horizontal plane of regard converging the eyes toward the near target, followed by rotations in each eye's vertical direction plane, and finally, disconjugate rotations in a common frontoparallel plane. This compounded rotation of the eye was underlying an initially fast-rising variable torsion that typically overshot the final torsion, which the eyes attained at the time of target acquisition. The torsion consisted of a coarse, widely varying component of opposite polarity in the two eyes, which contained a more robust, much smaller modulation that sharply increased toward the end of saccades. The reorientation of the eyes in torsion depended on each eye's azimuth, elevation, and target distance. We conclude that refixation saccades are generated by motor commands that control ocular torsion in concert with the saccade generator, which operates in Donders-Listing kinematics underlying Listing's law.

Effect of mechanic stimulation of foot support zones during seven-day dry immersion on the immersion-induced changes in ocular saccade kinematics

The purpose of the study was to determine how daily sessions of mechanic stimulation (MS) of foot support zones intended for mitigating the effect of the lack of support on the postural muscles influence ocular saccades during prolonged support deprivation. Four control subjects and four subjects receiving MS of foot support zones (experimental group) performed the test of rapid blanking of a light target appearing at the visual field periphery. The test was carried out before and immediately after seven-day dry immersion. Eye movements were traced using their infrared images recorded at a frequency of 200 Hz. Analysis of normalized and pooled data showed that MS of foot support zones during seven-day dry immersion significantly moderated the changes in ocular saccade kinematics resulting from support load deprivation. This confirms the involvement of support afferent input in the sensory contribution to the mechanisms of ocular saccade generation.

Saccade detection using a particle filter.

When healthy subjects track a moving target, "catch-up" saccades are triggered to compensate for the non-perfect tracking gain. The evaluation of the pursuit and/or saccade kinematics requires that saccade and pursuit components be separated from the eye movement trace. A similar situation occurs when analyzes eye movements of patients that could contain eye drifts between saccades. This task is especially difficult, because the range of saccadic amplitudes goes from microsaccades (less than 1°) to large exploratory saccades (40°). In this paper we proposed a new algorithm to detect saccades based on a particle filter. The new method suppresses the baseline velocity component linked to smooth pursuit (or to eye drifts) and thus permits a constant threshold during a trial despite the smooth pursuit behavior. It also accounts for a wide range of saccade amplitudes. The new method is validated with five different paradigms, microsaccades, microsaccades plus saccades with drift, linear target motion, non-linear target motion and free viewing. The sensitivity of the method to signal noise is analyzed. Traditional saccade detection algorithms using a velocity (or acceleration or jerk) threshold can be inadequate because of the baseline velocity component linked to the smooth pursuit (especially if the target motion is non-linear, i.e. not constant velocity) or to eye drifts between saccades. The new method detects saccades in challenging situations involving eye movements between saccades (smooth pursuit and/or eye drifts) and unfiltered recordings.

Saccadic inhibition is accompanied by large and complex amplitude modulations when induced by visual backward masking

Saccadic inhibition refers to the strong temporary decrease in saccadic initiation observed when a visual distractor appears shortly after the onset of a saccadic target. Here, to gain a better understanding of this phenomenon, we assessed whether saccade amplitude changes could accompany these modulations of latency distributions. As previous studies on the saccadic system using visual backward masking--a protocol in which the mask appears shortly after the target--showed latency increases and amplitude changes, we suspected that this could be a condition in which amplitude changes would accompany saccadic inhibition. We show here that visual backward masking produces a strong saccadic inhibition. In addition, this saccadic inhibition was accompanied by large and complex amplitude changes: a first phase of gain decrease occurred before the saccadic inhibition; when saccades reappeared after the inhibition, they were accurate before rapidly entering into a second phase of gain decrease. We observed changes in saccade kinematics that were consistent with the possibility of saccades being interrupted during these two phases of gain decrease. These results show that the onset of a large stimulus shortly after a first one induces the previously reported saccadic inhibition, but also induces a complex pattern of amplitude changes resulting from a dual amplitude perturbation mechanism with fast and slow components.

Optimal Control of Saccades by Spatial-Temporal Activity Patterns in the Monkey Superior Colliculus

A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-dependent noise in the neural control signals. Here we argue that the midbrain superior colliculus (SC), a key sensorimotor interface that contains a topographically-organized map of saccade vectors, is in an ideal position to implement such an optimization principle. Most models attribute the nonlinear saccade kinematics to saturation in the brainstem pulse generator downstream from the SC. However, there is little data to support this assumption. We now present new neurophysiological evidence for an alternative scheme, which proposes that these properties reside in the spatial-temporal dynamics of SC activity. As predicted by this scheme, we found a remarkably systematic organization in the burst properties of saccade-related neurons along the rostral-to-caudal (i.e., amplitude-coding) dimension of the SC motor map: peak firing-rates systematically decrease for cells encoding larger saccades, while burst durations and skewness increase, suggesting that this spatial gradient underlies the increase in duration and skewness of the eye velocity profiles with amplitude. We also show that all neurons in the recruited population synchronize their burst profiles, indicating that the burst-timing of each cell is determined by the planned saccade vector in which it participates, rather than by its anatomical location. Together with the observation that saccade-related SC cells indeed show signal-dependent noise, this precisely tuned organization of SC burst activity strongly supports the notion of an optimal motor-control principle embedded in the SC motor map as it fully accounts for the straight trajectories and kinematic nonlinearity of saccades.

LINEAR VISUOMOTOR TRANSFORMATIONS IN MIDBRAIN SUPERIOR COLLICULUS CONTROL SACCADIC EYE-MOVEMENTS

It is well established that a localized population of neurons in the motor map of the midbrain superior colliculus (SC) drives a saccadic eye-head gaze shift. However, there is controversy as to how the brainstem saccade burst generators decode the SC activity. We focus on eye-movement generation by comparing two competing schemes from the recent literature that are both supported by neurophysiological evidence: the vector-averaging scheme versus the vector summation model. Whereas the former contains at least four nonlinearities to explain visuomotor planning and saccade execution, the latter relies predominantly on linear operations. We have demonstrated that the summation model accounts for the nonlinear main sequence of saccade kinematics, and predicted that this results from a spatial gradient in temporal burst profiles of SC cells: rostral cells have higher peak-firing rates and shorter burst durations than caudal cells. Yet, the number of spikes in their saccade-related bursts is identical. In contrast, the averaging model does not predict such activity profiles. We now also show that by incorporating the concept of predictive remapping in the spatial updating of saccade sequences, the phenomenon of target averaging in double-stimulation experiments, and the occurrence of goal-directed, but highly curved saccades in the double-step paradigm, can all be explained by the same linear summation mechanism. We argue that the linear model is more in line with neurophysiological data, while relying on fewer ad-hoc assumptions than the nonlinear vector-averaging scheme.

The time course of online trajectory corrections in memory-guided saccades

Recent investigations have revealed the kinematics of horizontal saccades are less variable near the end of the trajectory than during the course of execution. Converging evidence indicates that oculomotor networks use online sensorimotor feedback to correct for initial trajectory errors. It is also known that oculomotor networks express saccadic corrections with decreased efficiency when responses are made toward memorized locations. The present research investigated whether repetitive motor timekeeping influences online feedback-based corrections in predictive saccades. Predictive saccades are a subclass of memory-guided saccades and are observed when one makes series of timed saccades. We hypothesized that cueing predictive saccades in a sequence would facilitate the expression of trajectory corrections. Seven participants produced a number of single unpaced, visually guided saccades, and also sequences of timed predictive saccades. Kinematic and trajectory variability were used to measure the expression of online saccadic corrections at a number of time indices in saccade trajectories. In particular, we estimated the minimum time required to implement feedback-based corrections, which was consistently 37ms. Our observations demonstrate that motor commands in predictive memory-guided saccades can be parameterized by spatial working memory and retain the accuracy of online trajectory corrections typically associated with visually guided behavior. In contrast, untimed memory-guided saccades exhibited diminished kinematic evidence for online corrections. We conclude that motor timekeeping and sequencing contributed to efficient saccadic corrections. These results contribute to an evolving view of the interactions between motor planning and spatial working memory, as they relate to oculomotor control.

Changes in the ocular saccade kinematics after a seven-day dry immersion

To assess the effects of long-term support unload on gaze control, five subjects were tested for the successful touch of a light target unpredictably emerging in the peripheral field of vision before and immediately after a seven-day dry immersion. The test did not set time requirements on gaze fixation on the target or motor task implementation. Ocular movements were recorded with an infrared eye image analyzer at 100 Hz. Modification of the dependences of the maximum velocity and duration of a saccade towards a homolateral target at the amplitude following immersion pointed to the speeding-up of the saccadic eye movements.

Temporal Discounting of Reward and the Cost of Time in Motor Control

Why do movements take a characteristic amount of time, and why do diseases that affect the reward system alter control of movements? Suppose that the purpose of any movement is to position our body in a more rewarding state. People and other animals discount future reward as a hyperbolic function of time. Here, we show that across populations of people and monkeys there is a correlation between discounting of reward and control of movements. We consider saccadic eye movements and hypothesize that duration of a movement is equivalent to a delay of reward. The hyperbolic cost of this delay not only accounts for kinematics of saccades in adults, it also accounts for the faster saccades of children, who temporally discount reward more steeply. Our theory explains why saccade velocities increase when reward is elevated, and why disorders in the encoding of reward, for example in Parkinson's disease and schizophrenia, produce changes in saccade. We show that delay of reward elevates the cost of saccades, reducing velocities. Finally, we consider coordinated movements that include motion of eyes and head and find that their kinematics is also consistent with a hyperbolic, reward-dependent cost of time. Therefore, each voluntary movement carries a cost because its duration delays acquisition of reward. The cost depends on the value that the brain assigns to stimuli, and the rate at which it discounts this value in time. The motor commands that move our eyes reflect this cost of time.

Differential Effects of Reflex Blinks on Saccade Perturbations in Humans

Studies in both humans and monkeys have indicated that blinks affect the central programming of saccades. In this study, we compared the influence of two types of reflex blinks on the trajectories and kinematics of memory-guided saccades in human subjects. We found that electrical stimulation of the supraorbital nerve shortly before or during a saccade briefly halts or decelerates the eye in midflight. After this short interruption, the eye always resumed its course and reached the target location in the absence of visual feedback. Air puff stimuli produced significant decreases in mean eye velocity too, but in addition to these changes in saccade kinematics, they produced much larger and more variable perturbations of the two-dimensional saccade trajectories. Even so, the endpoints of blink-perturbed saccades obtained under both test conditions remained as accurate and as precise as those observed in the control condition. We hypothesize that the reduction in mean eye velocity is not caused by a trigeminal reactivation of brain stem omnipause neurons but could instead arise from a trigeminal transient inhibition of saccade-related activity in the midbrain superior colliculus (SC). These findings support the theory that blink-perturbed saccades are programmed as slow, but straight, saccades onto which blink-related eye movements are superimposed. This linear superposition occurs downstream from the SC.

Aerodynamic damping during rapid flight maneuvers in the fruit fly Drosophila

We systematically investigated the effect of body rotation on the aerodynamic torque generation on flapping wings during fast turning maneuvers (body saccades) in the fruit fly Drosophila. A quasi-steady aerodynamic simulation of turning maneuvers with symmetrically flapping wings showed that body rotation causes a substantial aerodynamic counter-torque, known as flapping counter-torque (FCT), which acts in the opposite direction to turning. Simulation results further indicate that FCTs are linearly dependent on the rotational velocity and the flapping frequency regardless of the kinematics of wing motion. We estimated the damping coefficients for the principal rotation axes - roll, pitch, yaw - in the stroke plane frame. FCT-induced passive damping exists about all the rotation axes examined, suggesting that the effects of body rotation cannot be ignored in the analysis of free-flight dynamics. Force measurements on a dynamically scaled robotic wing undergoing realistic saccade kinematics showed that although passive aerodynamic damping due to FCT can account for a large part of the deceleration during saccades, active yaw torque from asymmetric wing motion is required to terminate body rotation. In addition, we calculated the mean value of the damping coefficient at 21.00 x10(-12) N m s based on free-flight data of saccades, which is somewhat lower than that estimated by the simulation results (26.84 x 10(-12) N m s).

Changes in Dynamic and Kinematic Properties of Saccades in Ocular Myasthenia following Intravenous Immunoglobulin Treatment

The dynamics and kinematics of saccades in a patient with severe ocular myasthenia were studied before and after treatment with intravenous immunoglobulin (IVIG). Before therapy, horizontal saccades were hypometric, but faster than similar-sized saccades made by normal subjects. During a 5-minute test period, saccades decreased in size (fatigue effect), but remained faster than those of controls. Listing's plane of the eye with greater ophthalmoplegia was increased in thickness. After IVIG treatment, the range of eye movements improved, but saccades remained faster than those of controls. Also, no fatigue was observed and the thickness of Listing's plane was reduced toward the normal range. Increased peak velocity, despite progressive hypometria due to fatigue, supports the hypothesis that the pale global extraocular muscle fibers are relatively spared in myasthenia. Involvement of other extraocular muscle-fiber types leads to limited range of eye movements and an increase in the thickness of Listing's plane.

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

The improvement of motor behavior, based on experience, is a form of learning that is critically dependent on the cerebellum. A well studied example of cerebellar motor learning is short-term saccadic adaptation (STSA). In STSA, information on saccadic errors is used to improve future saccades. The information optimizing saccade metrics is conveyed by Purkinje cells simple spikes (PC-SS) because they are the critical input to the premotor circuits for saccades. We recorded PC-SS of monkeys undergoing STSA to reveal the code used for improving behavior. We found that the discharge of individual PC-SS was unable to account for the behavioral changes. The PC-SS population burst (PB), however, exhibited changes that closely paralleled the qualitatively different changes of saccade kinematics associated with gain-increase and gain-decrease STSA, respectively. Gain-increase STSA, characterized by an increase in saccade duration, replicates the relationship between saccade duration and the end of the PB valid for unadapted saccades. In contrast, gain-decrease STSA, which sports normal saccade duration but reduced saccadic velocity, is characterized by a PB that ends well before the adapted saccade. This suggests that the duration of normal as well as gain-increased saccades is determined by appropriately setting the end of PB end. However, the duration of gain-decreased saccades is apparently not modified by the cerebellum because the PB signals ends too early to determine saccade end. In summary, STSA, and most probably cerebellar-dependent learning in general, is based on optimizing the shape of a PC-SS population response.