New methods for removing saccades in analysis of smooth pursuit eye movement

New computation methods for removing saccades in analysis of smooth pursuit eye movement characteristics were developed. They have removed saccades more completely than previous methods, and were very effective especially for noisy data recorded by the EOG method. The fully developed method was applicable to eye movement data in tracking of pseudo-random target movement as well as deterministic target movement. Furthermore, the methods were also useful for extracting the number and magnitudes of saccades more precisely.     

Incorporating Prediction in Models for Two-Dimensional Smooth Pursuit

A predictive component can contribute to the command signal for smooth pursuit. This is readily demonstrated by the fact that low frequency sinusoidal target motion can be tracked with zero time delay or even with a small lead. The objective of this study was to characterize the predictive contributions to pursuit tracking more precisely by developing analytical models for predictive smooth pursuit. Subjects tracked a small target moving in two dimensions. In the simplest case, the periodic target motion was composed of the sums of two sinusoidal motions (SS), along both the horizontal and the vertical axes. Motions following the same or similar paths, but having a richer spectral composition, were produced by having the target follow the same path but at a constant speed (CS), and by combining the horizontal SS velocity with the vertical CS velocity and vice versa. Several different quantitative models were evaluated. The predictive contribution to the eye tracking command signal could be modeled as a low-pass filtered target acceleration signal with a time delay. This predictive signal, when combined with retinal image velocity at the same time delay, as in classical models for the initiation of pursuit, gave a good fit to the data. The weighting of the predictive acceleration component was different in different experimental conditions, being largest when target motion was simplest, following the SS velocity profiles.     

Attention governs action in the primate frontal eye field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.     

Ultrasound tracking for intra-fractional motion compensation in radiation therapy

Modern techniques as ion beam therapy or 4D imaging require precise target position information. However, target motion particularly in the abdomen due to respiration or patient movement is still a challenge and demands methods that detect and compensate this motion. Ultrasound represents a non-invasive, dose-free and model-independent alternative to fluoroscopy, respiration belt or optical tracking of the patient surface. Thus, ultrasound based motion tracking was integrated into irradiation with actively scanned heavy ions. In a first in vitro experiment, the ultrasound tracking system was used to compensate diverse sinusoidal target motions in two dimensions. A time delay of ∼200 ms between target motion and reported position data was compensated by a prediction algorithm (artificial neural network). The irradiated films proved feasibility of the proposed method. Furthermore, a practicable and reliable calibration workflow was developed to enable the transformation of ultrasound tracking data to the coordinates of the treatment delivery or imaging system – even if the ultrasound probe moves due to respiration. A first proof of principle experiment was performed during time-resolved positron emission tomography (4DPET) to test the calibration workflow and to show the accuracy of an ultrasound based motion tracking in vitro. The results showed that optical ultrasound tracking can reach acceptable accuracies and encourage further research.     

Learned timing of motor behavior in the smooth eye movement region of the frontal eye fields

Proper timing is a critical aspect of motor learning. We report a relationship between a representation of time and an expression of learned timing in neurons in the smooth eye movement region of the frontal eye fields (FEF(SEM)). During prelearning pursuit of target motion at a constant velocity, each FEF(SEM) neuron is most active at a distinct time relative to the onset of pursuit tracking. In response to an instructive change in target direction, a neuron expresses the most learning when the instruction occurs near the time of its maximal participation in prelearning pursuit. Different neurons are most active, and undergo the most learning, at distinct times during pursuit. We suggest that the representation of time in the FEF(SEM) drives learning that is temporally linked to an instructive change in target motion, and that this may be a general function of motor areas of the cortex.     

The effect of saccades on threshold perception — A model study

The effect of saccadic eye movements on threshold perception is investigated theoretically. The proposed model considers eye movements by taking into account the shifting of the stimulus pattern on the retina during the occurrence of an eye movement. Saccades are characterized by high velocity and short duration. These motions cause overshoots in the response of linear filters to certain stimulus patterns. Therefore, the model predicts facilitation effects of saccades in the perception of low spatial frequency patterns and patterns flickering with high temporal frequencies. These results agree with experimentally obtained data presented in a subsequent paper. A simple approach is formulated which approximates the complex shifting function of a saccade by a switching of the pattern.     

Paradoxical inward rib cage motion during rapid eye movement sleep in infants and young children

In neonates, rib cage motion on inspiration during rapid eye movement sleep is almost exclusively paradoxical. We wondered whether or not duration of paradoxical inward rib cage motion on inspiration during rapid eye movement sleep decreases in infancy and early childhood. Thirteen healthy infants from 7 to 31 months of age were tested during natural afternoon naps. Electroencephalogram, electrooculogram and electromyogram were all recorded. Airflow was measured by nasal and buccal thermistors, abdominal and rib cage anteroposterior diameters by magnetometers. Transcutaneous partial pressure of O2 was monitored. Diaphragmatic electromyographic activity was recorded using surface electrodes. The average total sleep time was 138 min ranging from 107 to 186 and rapid eye movement sleep time amounted to 15% of total sleep time ranging from 6 to 25. During rapid eye movement sleep, the total duration of paradoxical inward rib cage motion was measured and expressed as a percentage of rapid eye movement sleep time. We found that duration of paradoxical inward rib cage motion during rapid eye movement sleep decreased significantly with age (r = -0.66, P less than 0.02) which may be explained by the changes in chest wall compliance and geometry of the rib cage occurring with growth. We observed no decrease in transcutaneous partial pressure in O2 during paradoxical inward rib cage motion during rapid eye movement sleep in infants in contrast to that reported in neonates.     

Sequences of predictive eye movements form a fractional Brownian series – implications for self-organized criticality in the oculomotor system

When human subjects are presented with a pair of visual targets that alternate periodically, they track the targets with rapid eye movements known as saccades. In previous work we demonstrated that at low pacing rates (<0.5 Hz), saccades have a latency of about 180 ms, and the latencies are uncorrelated from trial to trial. At high pacing rates (>0.6 Hz), latencies are much shorter: subjects make predictive saccades that anticipate target motion. The predictive latencies are correlated and appear to form a fractional Brownian motion. Here we confirm this finding by examining the rate of decay of nonlinear forecasting of predictive latencies. We further characterize the nature of predictive saccade latencies through the use of detrended fluctuation analysis and surrogate data. These results lead us to conclude that predictive saccades may exhibit a form of self-organized criticality, which enables rapid response to changes in stimulus timing. We provide an experimental demonstration of this.     

The representation of time for motor learning

We have identified factors that control precise motor timing by studying learning in smooth pursuit eye movements. Monkeys tracked a target that moved horizontally for a fixed time interval before changing direction through the addition of a vertical component of motion. After repeated presentations of the same target trajectory, infrequent probe trials of purely horizontal target motion evoked a vertical eye movement around the time when the change in target direction would have occurred. The pursuit system timed the vertical eye movement by keeping track of the duration of horizontal target motion and by measuring the distance the target traveled before changing direction, but not by learning the position in space where the target changed direction. We conclude that high temporal precision in motor output relies on multiple signals whose contributions to timing vary according to task requirements.     

Human visual search does not maximize the post-saccadic probability of identifying targets

Researchers have conjectured that eye movements during visual search are selected to minimize the number of saccades. The optimal Bayesian eye movement strategy minimizing saccades does not simply direct the eye to whichever location is judged most likely to contain the target but makes use of the entire retina as an information gathering device during each fixation. Here we show that human observers do not minimize the expected number of saccades in planning saccades in a simple visual search task composed of three tokens. In this task, the optimal eye movement strategy varied, depending on the spacing between tokens (in the first experiment) or the size of tokens (in the second experiment), and changed abruptly once the separation or size surpassed a critical value. None of our observers changed strategy as a function of separation or size. Human performance fell far short of ideal, both qualitatively and quantitatively.     

The effect of eye movement on the control of arm movement to a target

Abstract

The purpose of this study was to investigate the effect of eye movement on the control of arm movement to a target. Healthy humans flexed the elbow to a stationary target in response to a start tone. Simultaneously, the subject moved the eyes to the target (saccade eye movement), visually tracked a laser point moving with the arm (smooth pursuit eye movement), or gazed at a stationary start point at the midline of the horizontal visual angle (non-eye movement—NEM). Arm movement onset was delayed when saccade eye movement accompanied it. The onset of an electromyographic burst in the biceps muscle and the onset of saccade eye movement were almost simultaneous when both the arm and the eyes moved to the target. Arm movement duration during smooth pursuit eye movement was significantly longer than that during saccade eye movement or NEM. In spite of these findings, amplitudes of motor-evoked potential in the biceps and triceps brachii muscles were not significantly different among the eye movement conditions. These findings indicate that eye movement certainly affects the temporal control of arm movement, but may not affect corticospinal excitability in the arm muscles during arm movement.     

Implicit and Explicit Timing in Oculomotor Control

The passage of time can be estimated either explicitly, e.g. before leaving home in the morning, or implicitly, e.g. when catching a flying ball. In the present study, the latency of saccadic eye movements was used to evaluate differences between implicit and explicit timing. Humans were required to make a saccade between a central and a peripheral position on a computer screen. The delay between the extinction of a central target and the appearance of an eccentric target was the independent variable that could take one out of four different values (400, 900, 1400 or 1900 ms). In target trials, the delay period lasted for one of the four durations randomly. At the end of the delay, a saccade was initiated by the appearance of an eccentric target. Cue&target trials were similar to target trials but the duration of the delay was visually cued. In probe trials, the duration of the upcoming delay was cued, but there was no eccentric target and subjects had to internally generate a saccade at the estimated end of the delay. In target and cue&target trials, the mean and variance of latency distributions decreased as delay duration increased. In cue&target trials latencies were shorter. In probe trials, the variance increased with increasing delay duration and scalar variability was observed. The major differences in saccadic latency distributions were observed between visually-guided (target and cue&target trials) and internally-generated saccades (probe trials). In target and cue&target trials the timing of the response was implicit. In probe trials, the timing of the response was internally-generated and explicitly based on the duration of the visual cue. Scalar timing was observed only during probe trials. This study supports the hypothesis that there is no ubiquitous timing system in the brain but independent timing processes active depending on task demands.     

Postural Sway and Gaze Can Track the Complex Motion of a Visual Target

Variability is an inherent and important feature of human movement. This variability has form exhibiting a chaotic structure. Visual feedback training using regular predictive visual target motions does not take into account this essential characteristic of the human movement, and may result in task specific learning and loss of visuo-motor adaptability. In this study, we asked how well healthy young adults can track visual target cues of varying degree of complexity during whole-body swaying in the Anterior-Posterior (AP) and Medio-Lateral (ML) direction. Participants were asked to track three visual target motions: a complex (Lorenz attractor), a noise (brown) and a periodic (sine) moving target while receiving online visual feedback about their performance. Postural sway, gaze and target motion were synchronously recorded and the degree of force-target and gaze-target coupling was quantified using spectral coherence and Cross-Approximate entropy. Analysis revealed that both force-target and gaze-target coupling was sensitive to the complexity of the visual stimuli motions. Postural sway showed a higher degree of coherence with the Lorenz attractor than the brown noise or sinusoidal stimulus motion. Similarly, gaze was more synchronous with the Lorenz attractor than the brown noise and sinusoidal stimulus motion. These results were similar regardless of whether tracking was performed in the AP or ML direction. Based on the theoretical model of optimal movement variability tracking of a complex signal may provide a better stimulus to improve visuo-motor adaptation and learning in postural control.     

Cross‐scanning optical coherence tomography angiography for eye motion correction

We propose a cross‐scanning optical coherence tomography (CS‐OCT) system to correct eye motion artifacts in OCT angiography images. This system employs a dual‐illumination configuration with two orthogonally polarized beams, each of which simultaneously perform raster scanning in perpendicular direction with each other over the same area. In the reference arm, a polarization delay unit is used to acquire the two orthogonally polarized interferograms with a single photo detector by introducing different optical delay lines. The two cross‐scanned volume data are affected by the same eye motion but in two orthogonal directions. We developed a motion correction algorithm, which removes artifacts in the slow axis of each angiogram using the other and merges them through a nonrigid registration algorithm. In this manner, we obtained a motion‐corrected angiogram within a single volume scanning time without additional eye‐tracking devices.     

The effect of the visual stimulation of the leading and nonleading eye on the value of the saccadic latency period and on the peak latency of rapid presaccadic potentials]

Visual targets were presented monocularly to the leading and nonleading eyes. The complex of rapid positive and negative potentials was studied using the reverse summation from the onset of saccades. The latencies of saccades and peak latencies of the averaged presaccadic potentials were measured. The dependence of the saccade latencies and peak latencies of the complex of potentials on stimulation of the leading or nonleading eye and saccade direction was not simple and was largely determined by the individual profile of asymmetry. It is suggested that during stimulation of the leading eye the processes of attention fixation and switching as well as of the space visual processing are faster than during stimulation of the nonleading eye. Thus, the leading role of the right eye is reflected not only in fixation processes but also in movement anticipation.     

Computer simulation of overshoot in saccadic eye movements.

The human horizontal eye movement system produces quick, precise, conjugate eye movements called saccades. These are important in normal vision. For example, reading tasks exclusively utilize saccadic eye movements. The majority of saccades have dynamic overshoot. The amplitude of this overshoot is independent of saccadic amplitude, and is such that it places the image of the stimulus within the retinal region of maximum acuity within a minimum of time. A computer based model of the saccadic mechanisms was used to study the origin of this overshoot. It was discussed that dynamic overshoot cannot be attributed to biomechanism properites of the eye movement mechanism, but must instead be explained by variations in the controlling nervous activity. The form of this neural controller signal is very similar to that required for a time optimal response of an inertial system.     

Manipulating intent: evidence for a causal role of the superior colliculus in target selection

The superior colliculus (SC) is well known for its role in the motor control of saccades. Recent work has shown that it also plays a role in the selection of saccades, but a causal role in the process of target selection has not been demonstrated. We applied subthreshold microstimulation to the SC while monkeys performed a task requiring them to select a stimulus as the target for a pursuit or saccade movement. Stimulation increased the proportion of selections toward the stimulus that appeared contralateral to the site of stimulation and also decreased their latencies. For pursuit, this stimulation-induced contralateral response bias was with respect to the initial target location and not the direction of eye movement, demonstrating a causal effect on target choice distinct from any effect on motor preparation. These results show that the SC helps decide the object of the next movement, beyond its traditional responsibility of saccade production.     

A quantitative synchronization model for smooth pursuit target tracking

We propose a quantitative model for human smooth pursuit tracking of a continuously moving visual target which is based on synchronization of an internal expectancy model of the target position coupled to the retinal target signal. The model predictions are tested in a smooth circular pursuit eye tracking experiment with transient target blanking of variable duration. In subjects with a high tracking accuracy, the model accounts for smooth pursuit and repeatedly reproduces quantitatively characteristic patterns of the eye dynamics during target blanking. In its simplest form, the model has only one free parameter, a coupling constant. An extended model with a second parameter, a time delay or memory term, accounts for predictive smooth pursuit eye movements which advance the target. The model constitutes an example of synchronization of a complex biological system with perceived sensory signals. Cognitive and Neurobiological Research Consortium in Traumatic Brain Injury (CNRC-TBI).     

Oculocentric frames of reference for limb movement

We have reviewed evidence that suggests that the target for limb motion is encoded in a retinocentric frame of reference. Errors in pointing that are elicited by an illusion that distorts the perceived motion of a target are strongly correlated with errors in gaze position. The modulations in the direction and speed of ocular smooth pursuit and of the hand show remarkable similarities, even though the inertia of the arm is much larger than that of the eye. We have suggested that ocular motion is constrained so that gaze provides an appropriate target signal for the hand. Finally, ocular and manual tracking deficits in patients with cerebellar ataxia are very similar. These deficits are also consistent with the idea that a gaze signal provides the target for hand motion; in some cases limb ataxia would be a consequence of optic ataxia rather than reflecting a deficit in the control of limb motion per se. These results, as well as neurophysiological data summarized here, have led us to revise a hypothesis we have previously put forth to account for the initial stages of sensorimotor transformations underlying targeted limb motions. In the original hypothesis, target location and initial arm posture were ultimately encoded in a common frame of reference tied to somatosensation, i.e. a body-centered frame of reference, and a desired change in posture was derived from the difference between the two. In our new scheme, a movement vector is derived from the difference between variables encoded in a retinocentric frame of reference. Accordingly, gaze, with its exquisite ability to stabilize a target image even under dynamic conditions, would be used as a reference signal. Consequently, this scheme would facilitate the processing of information under conditions in which the body and the target are moving relative to each other.     

Extra-retinal adaptation of cortical motion-processing areas during pursuit eye movements

Repetitive eye movement produces a compelling motion aftereffect (MAE). One mechanism thought to contribute to the illusory movement is an extra-retinal motion signal generated after adaptation. However, extra-retinal signals are also generated during pursuit. They modulate activity within cortical motion-processing area MST, helping transform retinal motion into motion in the world during an eye movement. Given the evidence that MST plays a key role in generating MAE, it may also become indirectly adapted by prolonged pursuit. To differentiate between these two extra-retinal mechanisms we examined storage of the MAE across a period of darkness. In one condition observers were told to stare at a moving pattern, an instruction that induces a more reflexive type of eye movement. In another they were told to deliberately pursue it. We found equally long MAEs when testing immediately after adaptation but not when the test was delayed by 40 s. In the case of the reflexive eye movement the delay almost completely extinguished the MAE, whereas the illusory motion following pursuit remained intact. This suggests pursuit adapts cortical motion-processing areas whereas unintentional eye movement does not. A second experiment showed that cortical mechanisms cannot be the sole determinant of pursuit-induced MAE. Following oblique pursuit, we found MAE direction changes from oblique to vertical. Perceived MAE direction appears to be influenced by a subcortical mechanism as well, one based on the relative recovery rate of horizontal and vertical eye-movement processes recruited during oblique pursuit.