Cursive writing with smooth pursuit eye movements

The eyes never cease to move: ballistic saccades quickly turn the gaze toward peripheral targets, whereas smooth pursuit maintains moving targets on the fovea where visual acuity is best. Despite the oculomotor system being endowed with exquisite motor abilities, any attempt to generate smooth eye movements against a static background results in saccadic eye movements [1, 2]. Although exceptions to this rule have been reported [3-5], volitional control over smooth eye movements is at best rudimentary. Here, I introduce a novel, temporally modulated visual display, which, although static, sustains smooth eye movements in arbitrary directions. After brief training, participants gain volitional control over smooth pursuit eye movements and can generate digits, letters, words, or drawings at will. For persons deprived of limb movement, this offers a fast, creative, and personal means of linguistic and emotional expression.     

A model of visually-guided smooth pursuit eye movements based on behavioral observations

We report a model that reproduces many of the behavioral properties of smooth pursuit eye movements. The model is a negative-feedback system that uses three parallel visual motion pathways to drive pursuit. The three visual pathways process image motion, defined as target motion with respect to the moving eye, and provide signals related to image velocity, image acceleration, and a transient that occurs at the onset of target motion. The three visual motion signals are summed and integrated to produce the eye velocity output of the model. The model reproduces the average eye velocity evoked by steps of target velocity in monkeys and humans and accounts for the variation among individual responses and subjects. When its motor pathways are expanded to include positive feedback of eye velocity and a switch, the model reproduces the exponential decay in eye velocity observed when a moving target stops. Manipulation of this expanded model can mimic the effects of stimulation and lesions in the arcuate pursuit area, the middle temporal visual area (MT), and the medial superior temporal visual area (MST).     

Nonlinear parameter estimation applied to a model of smooth pursuit eye movements

We present a procedure that optimally adjusts specified parameters of a mathematical model to describe a set of measured data. The technique integrates a dynamic systems-simulation language with a robust algorithm for nonlinear parameter estimation, and it can be implemented on a microcomputer. Sensitivity functions are generated that indicate how the operation of the model is affected by each updated parameter. This procedure offers a greater resolution of optimal parameter values than other, less rigorous methods. To illustrate this technique we have applied it to the model of human smooth pursuit eye movements proposed by D.A. Robinson and colleagues (1986).     

Cortical mechanisms of smooth eye movements revealed by dynamic covariations of neural and behavioral responses

Neural activity in the frontal eye fields controls smooth pursuit eye movements, but the relationship between single neuron responses, cortical population responses, and eye movements is not well understood. We describe an approach to dynamically link trial-to-trial fluctuations in neural responses to parallel variations in pursuit and demonstrate that individual neurons predict eye velocity fluctuations at particular moments during the course of behavior, while the population of neurons collectively tiles the entire duration of the movement. The analysis also reveals the strength of correlations in the eye movement predictions derived from pairs of simultaneously recorded neurons and suggests a simple model of cortical processing. These findings constrain the primate cortical code for movement, suggesting that either a few neurons are sufficient to drive pursuit at any given time or that many neurons operate collectively at each moment with remarkably little variation added to motor command signals downstream from the cortex.     

A model of the smooth pursuit eye movement system

Human, horizontal, smooth-pursuit eye movements were recorded by the search coil method in response to Rashbass step-ramp stimuli of 5 to 30 deg/s. Eye velocity records were analyzed by measuring features such as the time, velocity and acceleration of the point of peak acceleration, the time and velocity of the peaks and troughs of ringing and steady-state velocity. These values were averaged and mean responses reconstructed. Three normal subjects were studied and their responses averaged. All showed a peak acceleration-velocity saturation. All had ringing frequencies near 3.8 Hz and the mean steady-state gain was 0.95.It is argued that a single, linear forward path with any transfer function G(s) and a 100 ms delay (latency) cannot simultaneously simulate the initial rise of acceleration and ring at 3.8 Hz based on a Bode analysis. Also such a simple negative feedback model cannot have a steady-state gain greater than 1.0; a situation that occurs frequently experimentally. L.R. Young's model, which employs internal positive feedback to eliminate the built-in unity negative feedback, was felt necessary to resolve this problem and a modification of that model is proposed which simulates the data base. Acceleration saturation is achieved by borrowing the idea of the local feedback model for saccades so that one nonlinearity can account for the acceleration-velocity saturation: the main sequence for pursuit. Motor plasticity or motor learning, recently demonstrated for pursuit, is also incorporated and simulated.It was noticed that the offset of pursuit did not show the ringing seen in the onset so this was quantified in one subject. Offset velocity could be characterized by a single exponential with a time constant of about 90 ms. This observation suggests that fixation is not pursuit at zero velocity and that the pursuit system is turned on when needed and off during fixation.     

Quantitative evaluation of smooth pursuit eye movements by personal computer. I) Normative data and effect of aging

We recorded the smooth pursuit eye movements (SPEM) of 52 healthy subjects by binocular electrooculographic technique. The 52 subjects were homogeneously distributed from the 2nd to the 6th decade. The target moved over 60 deg of amplitude at constant velocity (ramp); different target velocities were used ranging from 10 to 50 deg/sec. All subjects were tested with the same 58 pseudo-random ramp sequence under the control of a Personal Computer (PC). The quantitative analysis of SPEM was carried out by an interactive program implemented on the same PC. Different equations were tested by a multiple regression analysis in order to describe the relationship between SPEM gain values and target velocities; two of these equations were chosen and used in order to find out if SPEM gain was influenced by target direction (the direction effect) and/or by subject age (the age effect). The statistical analyses we performed, demonstrated that SPEM gain values were influenced by aging but not by target direction: SPEM gain decreased as age increased.     

The existence of a hypnotic state revealed by eye movements

Hypnosis has had a long and controversial history in psychology, psychiatry and neurology, but the basic nature of hypnotic phenomena still remains unclear. Different theoretical approaches disagree as to whether or not hypnosis may involve an altered mental state. So far, a hypnotic state has never been convincingly demonstrated, if the criteria for the state are that it involves some objectively measurable and replicable behavioural or physiological phenomena that cannot be faked or simulated by non-hypnotized control subjects. We present a detailed case study of a highly hypnotizable subject who reliably shows a range of changes in both automatic and volitional eye movements when given a hypnotic induction. These changes correspond well with the phenomenon referred to as the "trance stare" in the hypnosis literature. Our results show that this 'trance stare' is associated with large and objective changes in the optokinetic reflex, the pupillary reflex and programming a saccade to a single target. Control subjects could not imitate these changes voluntarily. For the majority of people, hypnotic induction brings about states resembling normal focused attention or mental imagery. Our data nevertheless highlight that in some cases hypnosis may involve a special state, which qualitatively differs from the normal state of consciousness.     

Quantitative analysis of smooth pursuit eye movements by personal computer. II. Evaluation of individual performance and clinical applicability

In a previous report on quantitative analysis of smooth pursuit eye movements (SPEM) we assessed two equations in order to describe the SPEM gain/target velocity relationship, and we demonstrated that this relationship is age-related. This report presents a method to evaluate normality of a single subject SPEM performance. Three points have been considered: 1) The control of gain asymmetries depending on target direction (leftward vs rightward SPEM) 2) The definition of age-related control values 3) The subject vs control values comparison An example to explain how our method actually works and its clinical applicability is shown. Finally, the reasons why no choice has been made between the two equations are discussed.     

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.     

Separate visual representations for perception and action revealed by saccadic eye movements

Some 30 years ago, Trevarthen [1] introduced the idea of two separate visual systems, a focal system for fine motor acts and an ambient system for gross body movements such as ambulation. More recent developments indicating anatomically and physiologically separate pathways in primate vision [2] have led to a different idea of separate visual systems, one for conscious perception and one for action [3]. It has received empirical support from several studies showing that pointing, reaching, and grasping can remain accurate while the perceived position or size of objects is subject to illusory distortion [4-6]. However, much of this evidence has been challenged on the grounds of methodological flaws, particularly failure to match perfectly the conditions for verbal and motor tasks and failure to replicate results [7-10]. Here we take advantage of the strong compression of perceived position that occurs around the time of saccadic eye movements [11, 12]. Under normal lighting conditions, stimuli flashed briefly over a wide range of spatial positions just before saccadic onset are neither seen nor reached for in their veridical positions, but are compressed toward the saccadic target. We validate the idea of separate systems by showing that, in the dark, subjects are able to point accurately to the correct target position, even though their verbal reports are still subject to compression.     

The reliability of eye movement quantitative evaluation. II. Smooth pursuit eye movements.

We adopted the estimate of the intraclass coefficient of reliability, R, to evaluate the reliability of smooth pursuit eye movement quantitative analysis. At a one-week interval, we recorded twice smooth pursuit eye movements from fifteen healthy subjects by means of the binocular electrooculographic technique. R was computed for the constant and the slope of the target velocity/gain relationships. R values were rated good for the slope and excellent for the constant. Finally, we computed for each parameter the maximum variability value according to two differing methods; on the basis of the within-subjects mean square values, we defined the normal range of biological test-retest variability for the two parameters.     

Predictive adjustment of the perceived direction of gaze during saccadic eye movements

When we look at a stationary object, the perceived direction of gaze (where we are looking) is aligned with the physical direction of eyes (where our eyes are oriented) by which the object is foveated. However, this alignment may not hold in a dynamic situation. Our experiments assessed the perceived locations of two brief stimuli (1 ms) simultaneously displayed at two different physical locations during a saccade. The first stimulus was in the instantaneous location to which the eyes were oriented and the second one was always in the same location as the initial fixation point. When the timing of these stimuli was changed intra-saccadically, their perceived locations were dissociated. The first stimuli were consistently perceived near the target that will be foveated at saccade termination. The second stimuli once perceived near the target location, shifted in the direction opposite to that of saccades, as its latency from saccades increased. These results suggested an independent adjustment of gaze orientation from the physical orientation of eyes during saccades. The spatial dissociation of two stimuli may reflect sensorimotor control of gaze during saccades.     

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.     

What kind of eye movements will goldfish show in space?

Six goldfish (1 normal, 1 with otoliths removed on both sides, 4 with otoliths removed on one side) were flown in space. The behaviors of the fish were recorded with a video camera on Mission Elapsed Time (MET) Day-00, 02, 05, 08, and 12. On MET Day-00, fish with otoliths removed on one side showed rolling behavior toward the operated side. No rolling behaviors were observed after MET Day-8. Five fish showed backward looping behaviors during the mission. After the space experiment, torsional eye movements and vertical eye movements were examined by body tilting. The experiments showed that the sensitivity of eye movements were low for head up tilting and tilting to operated side.     

A neurally plausible model of the dynamics of motion integration in smooth eye pursuit based on recursive Bayesian estimation

In this study, we describe a model of motion integration in smooth eye pursuit based on a recursive Bayesian estimation process, which displays a dynamic behaviour qualitatively similar to the dynamics of the motion integration process observed experimentally, both psychophysically in humans and monkeys, and physiologically in monkeys. By formulating the model as an approximate version of a Kalman filter algorithm, we have been able to show that it can be put into a neurally plausible, distributed recurrent form which coarsely corresponds to the recurrent circuitry of visual cortical areas V1 and MT. The model thus provides further support for the notion that the motion integration process is based on a form of Bayesian estimation, as has been suggested by many psychophysical studies, and moreover suggests that the observed dynamic properties of this process are the result of the recursive nature of the motion estimation.     

The direction of rapid eye movements as an indication of hemispheric asymmetry during REM sleep. II

The hypothesis of right hemisphere predominance in REM sleep and of an increase in left activity throughout the night have been tested by analyzing the distribution of vertical and of horizontal rapid eye movements (REMs) to the right and to the left during the first and the last REM periods in 5 right-handed subjects. Neither the expected superiority of REMs to the left nor variations along the REM periods were found. For vertical eye movements our data suggest a superiority of upward movements during REM. In waking some empirical evidences suggest a relationship between upward eye movements and right hemisphere functioning although to date no hemispheric model can explain it.     

Selection of visual information for lightness judgements by eye movements

When judging the lightness of objects, the visual system has to take into account many factors such as shading, scene geometry, occlusions or transparency. The problem then is to estimate global lightness based on a number of local samples that differ in luminance. Here, we show that eye fixations play a prominent role in this selection process. We explored a special case of transparency for which the visual system separates surface reflectance from interfering conditions to generate a layered image representation. Eye movements were recorded while the observers matched the lightness of the layered stimulus. We found that observers did focus their fixations on the target layer, and this sampling strategy affected their lightness perception. The effect of image segmentation on perceived lightness was highly correlated with the fixation strategy and was strongly affected when we manipulated it using a gaze-contingent display. Finally, we disrupted the segmentation process showing that it causally drives the selection strategy. Selection through eye fixations can so serve as a simple heuristic to estimate the target reflectance.