Steady Fixation Research Articles

Eye movements facilitate stereo-slant discrimination when horizontal disparity is noisy.

Conditions in which saccadic gaze shifts within planar surfaces facilitate stereo-slant discrimination for slant about the horizontal and vertical axis were investigated. When horizontal disparity noise was added, large gaze shifts in the direction of the slant lowered stereo-slant discrimination thresholds compared to thresholds measured with steady central fixation, whereas eye movements orthogonal to the slant orientation did not lower slant-discrimination thresholds. When no horizontal noise was added, performance was the same with and without gaze shifts. These results suggest that slant is recovered from depth differences between target edges when horizontal disparity signals are variable and that foveal fixation improves the measures of disparity. Eye movements did not lower slant thresholds by providing multiple foveal samples of slant at different target locations that were averaged to reduce disparity noise levels, because eye movements only lowered the thresholds when there was a depth difference between the fixation points. To study which signals for azimuth are used when slant is recovered from the difference in depth between target edges, vertical disparity noise was added and stimulus height was reduced. Both methods elevated slant-discrimination thresholds when horizontal disparity noise was present, suggesting that vertical disparity is used as a cue for azimuth.

Pupil responses associated with coloured afterimages are mediated by the magno-cellular pathway

Sustained fixation of a bright coloured stimulus will, on extinction of the stimulus and continued steady fixation, induce an afterimage whose colour is complementary to that of the initial stimulus; an effect thought to be caused by fatigue of cones and/or of cone-opponent processes to different colours. However, to date, very little is known about the specific pathway that causes the coloured afterimage. Using isoluminant coloured stimuli recent studies have shown that pupil constriction is induced by onset and offset of the stimulus, the latter being attributed specifically to the subsequent emergence of the coloured afterimage. The aim of the study was to investigate how the offset pupillary constriction is generated in terms of input signals from discrete functional elements of the magno- and/or parvo-cellular pathways, which are known principally to convey, respectively, luminance and colour signals. Changes in pupil size were monitored continuously by digital analysis of an infra-red image of the pupil while observers viewed isoluminant green pulsed, ramped or luminance masked stimuli presented on a computer monitor. It was found that the amplitude of the offset pupillary constriction decreases when a pulsed stimulus is replaced by a temporally ramped stimulus and is eliminated by a luminance mask. These findings indicate for the first time that pupillary constriction associated with a coloured afterimage is mediated by the magno-cellular pathway.

Altered control of visual fixation and saccadic eye movements in attention-deficit hyperactivity disorder.

Attention-deficit hyperactivity disorder (ADHD) is characterized by the overt symptoms of impulsiveness, hyperactivity, and inattention. A frontostriatal pathophysiology has been hypothesized to produce these symptoms and lead to reduced ability to inhibit unnecessary or inappropriate behavioral responses. Oculomotor tasks can be designed to probe the ability of subjects to generate or inhibit reflexive and voluntary responses. Because regions of the frontal cortex and basal ganglia have been identified in the control of voluntary responses and saccadic suppression, we hypothesized that children and adults diagnosed with ADHD may have specific difficulties in oculomotor tasks requiring the suppression of reflexive or unwanted saccadic eye movements. To test this hypothesis, we measured eye movement performance in pro- and anti-saccade tasks of 114 ADHD and 180 control participants ranging in age from 6 to 59 yr. In the pro-saccade task, participants were instructed to look from a central fixation point toward an eccentric visual target. In the anti-saccade task, stimulus presentation was identical, but participants were instructed to suppress the saccade to the stimulus and instead look from the central fixation point to the side opposite the target. The state of fixation was manipulated by presenting the target either when the central fixation point was illuminated (overlap condition) or at some time after it disappeared (gap condition). In the pro-saccade task, ADHD participants had longer reaction times, greater intra-subject variance, and their saccades had reduced peak velocities and increased durations. In the anti-saccade task, ADHD participants had greater difficulty suppressing reflexive pro-saccades toward the eccentric target, increased reaction times for correct anti-saccades, and greater intra-subject variance. In a third task requiring prolonged fixation, ADHD participants generated more intrusive saccades during periods when they were required to maintain steady fixation. The results suggest that ADHD participants have reduced ability to suppress unwanted saccades and control their fixation behavior voluntarily, a finding that is consistent with a fronto-striatal pathophysiology. The findings are discussed in the context of recent neurophysiological data from nonhuman primates that have identified important control signals for saccade suppression that emanate from frontostriatal circuits.

Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts.

The superior colliculus (SC) is important for generating coordinated eye-head gaze saccades. Its deeper layers contain a retinotopically organized motor map in which each site is thought to encode a specific gaze saccade vector. Here we show that this fundamental assumption in current models of collicular function does not hold true during horizontal multi-step gaze shifts in darkness that are directed to a goal and composed of a sequence of gaze saccades separated by periods of steady fixation. At the start of a multi-step gaze shift in cats, neural activity on the SC's map was located caudally to encode the overall amplitude of the gaze displacement, not the first saccade in the sequence. As the gaze shift progressed, the locus of activity moved to encode the error between the goal and the current gaze position. Contrary to common belief, the locus of activity never encoded gaze saccade amplitude, except for the last saccade in the sequence.

Eye movement baseline oscillation and variability of eye position during foveation in congenital nystagmus.

Despite the inability to maintain steady fixation, congenital nystagmus does not necessarily reduce visual acuity, that can be achieved during the foveation periods. The duration of the foveation period, but also the cycle-to-cycle variability of eye position and velocity during foveations play an important role. A quantitative relationship that relates visual acuity with foveation time and cycle-to-cycle variability of eye position during foveation has been previously proposed. In many infrared-oculographic and electro-oculographic eye position recordings of our database, a sinusoidal-like oscillation of the baseline was observed, on which the nystagmus waveforms lay. This oscillation may contribute to increase cycle-to-cycle variability during foveations. The aim of this work is to extract the baseline oscillation from the recordings and to verify its relationship with eye position variability during foveation. On the basis of the observations, the baseline oscillation was assumed to be sinusoidal, and was estimated (using a least mean square technique) from eye movement signals recorded during fixation intervals, at different gaze positions, from 20 patients affected by congenital nystagmus with low visual acuity. The average baseline oscillation amplitude was 1.31 degrees, while the average frequency was 0.34 Hz. Baseline oscillation amplitude was well correlated (with a coefficient of 0.66) to the standard deviations of eye-position during foveation, which in turn is connected to visual acuity.

Mechanisms underlying nystagmus

In health, there are three main control mechanisms for maintaining steady gaze—fixation; the vestibulo-ocular reflex; and a gaze-holding system (the neural integrator), which operates whenever the eyes are required to hold an eccentric gaze position1,2,3. Failure of any of these control systems will bring about a disruption of steady fixation. Two types of abnormal fixation can result—nystagmus and saccadic intrusions/oscillations. The essential difference between them lies in the initial movement that takes the line of sight off the object of regard. In the case of nystagmus, it is a slow drift or ‘slow phase’ often due to a disturbance of one of the three mechanisms for gaze stability. On the other hand, with either saccadic intrusions or saccadic oscillations, it is an inappropriate fast movement that moves the eyes off target4,5. This paper will concern itself only with the clinical aspects of nystagmus and cover the possible reasons for its presence.

Medical treatment of nystagmus and its visual consequences

For us to see clearly the details in our visual world, images must be held quite still upon the retina, especially the central part (the fovea). For reading, which concerns detection of high spatial frequencies, image motion must be less than about 5° / second1. If image drift substantially exceeds this limit, visual acuity will decline and we may experience the illusion that the world is moving (oscillopsia). In health, three main mechanisms hold the line of sight steady so that our view of the world is clear and stable2. The first is ‘fixation’, which has two distinct components—the visual system's ability to detect retinal image drift and programme corrective eye movements, and the ability to suppress unwanted eye movements that would take the eye away from the target. The second mechanism is the vestibulo-ocular reflex, by which the motion detectors of the inner ear promptly initiate eye movements to compensate for head perturbations, such as occur during locomotion. The third mechanism is the gaze-holding system, which makes it possible to hold the eyes at an eccentric position (e.g. in lateral gaze). If any of the three mechanisms that normally act to hold gaze steady malfunctions, the eyes may start to drift away from the object of regard, and corrective rapid eye movements may be made. Thus, nystagmus may be defined as repetitive to-and-fro involuntary eye movements that are initiated by slow drifts of the eye. It is important to realize that some forms of nystagmus are normal. Thus, nystagmus that occurs during rotation of the body in space acts to preserve clear vision. In pathological nystagmus, however, drifts of the eyes away from the target degrade vision. In one form, pendular nystagmus, the drifts consist of a to-and-fro sinusoidal oscillation. More commonly, nystagmus consists of alternation of unidirectional drifts away from the target and corrective fast movements (saccades) which momentarily bring the visual target back to the fovea; this is jerk nystagmus. Nystagmus should be distinguished from inappropriate saccades that disrupt steady fixation. Saccades produce high-speed movement of images upon the retina—too high for clear vision—and several physiological mechanisms exist to prevent perception of the smeared retinal signal due to the saccade. However, patients in whom inappropriate saccades repeatedly misdirect the fovea often complain of difficulty with reading. Box 1 Medical strategies for treating nystagmus and its visual consequences Methods that place the eye in a position in which nystagmus is minimized Optical and electronic methods for negating the visual consequences of the nystagmus Procedures for weakening the extraocular muscles Application of somatosensory or auditory stimuli to suppress nystagmus Drugs that suppress some forms of nystagmus. Five main approaches to treating pathological nystagmus and its visual consequences are summarized in Box 1. For a fuller discussion of the clinical features, pathogenesis and treatment of nystagmus, the reader is referred to a recent textbook on eye movements2.

Effects of voluntary attention on structured afterimages.

The effect of voluntary attention on afterimage fragmentation was explored in two experiments. The afterimage, in the form of a 30 degrees-tilted star of David, was generated after prolonged steady fixation in the first experiment, and with a brief and intense flash in the second experiment. Subjects were instructed to select various target shapes in the afterimage for attention and, at the same time, observe what was visible or invisible. Verbal reports and manual responses to afterimage changes were analyzed. Attended shapes were found to disappear from awareness Faster than unattended ones (experiment 1), and complementary shapes were found to predominate visual awareness when one of the pair was selected for attention (experiment 2). Voluntary attention was also found to affect closure (filling-in of enclosed regions) and smoothing of line figures in afterimages.

The effects of dot density and motion coherence on perceptual fading of a target in noise.

A peripherally presented target embedded in dynamic texture perceptually disappears (or 'fills-in') after around 10 s of steady fixation. This phenomenon was investigated for a target containing moving dots. The effects of manipulating the coherence of the motion within the target and the density of dots across the whole screen were explored. Coherence thresholds for the detection of a target at different dot densities were recorded for comparison. Fading occurred faster as either motion coherence or dot density was reduced. Coherence thresholds for target detection were unaffected by manipulations of dot density. There appeared to be no relationship between the stimulus exposure time needed for fading and the coherence threshold for detection of a target. The results suggest that the time taken for a target to fade is not a simple function of its motion detection threshold.

Fixation neurons in the superior colliculus encode distance between current and desired gaze positions.

A visual scene is scrutinized during sequential periods of steady fixation, connected by saccades that shift the visual axis (gaze) to new positions. During such exploratory scan paths, gaze frequently strays from and then returns to salient features. How the brain keeps track of major end-goals and intermediate subgoals is not understood. We studied the discharge of fixation neurons of the brainstem's superior colliculus during multiple-step gaze shifts composed of a sequence of saccades made in the dark and separated by short periods of steady fixation. Cells were initially silent. As sequential gaze saccades approached the goal, firing began; its frequency increased progressively and peaked when gaze was on the remembered target location. We conclude that these fixation neurons encode the error between desired and actual gaze positions, irrespective of trajectory characteristics.

The scintillating grid illusion during smooth pursuit, stimulus motion, and brief exposure in humans

The Scintillating Grid Illusion occurs when small white disks are superimposed onto the intersections of a grey-on-black Hermann grid. As a result illusory dark spots are seen at numerous crossings, flashing with each flick of the eye and changing their location and distribution with each saccade. The illusion is absent with steady fixation. The present study shows that saccadic eye movements are not necessary to produce the illusion. Rather, the illusion was also found to occur (i) during smooth pursuit movements when the grid was stationary, (ii) during smooth displacement of the grid with the gaze kept steady, and (iii) during brief exposures of the stationary grid. It is concluded that, while transient stimulation is essential for generating the illusion, reduction in effective luminance contrast resulting from brief exposure and high stimulus speed are responsible for reductions in its strength.

Spatial localization of colour and luminance stimuli in human peripheral vision

A variety of studies suggest the localization of objects in three-dimensional space is predominantly the task of the magnocellular (M) system, and conversely that the parvocellular (P) system plays little or no role in localization. However, there are conflicting reports and the goal of this paper was to determine whether spatial localization is predominantly accomplished by one or the other visual system. Both manual pointing and three-target alignment protocols were used to measure localization accuracy for eccentrically presented patches of a sinewave grating. Two general approaches were adopted to activate preferentially one or the other pathway: (1) we varied the spatio-temporal frequency, contrast and chromatic properties of the stimulus to conform with the physiological response properties of either M or P cells; and (2) some measurements were made both with steady fixation and during large saccades, as the latter have been reported to cause selective suppression of the M system [Burr, Morrone & Ross (1994). Nature, 371, 511–513]. Each stimulus was presented at or near its detection contrast threshold, which was determined separately for each visual field location using forced-choice procedures. Using manual pointing, both M- and P-type stimuli were localized to within about 1.3° at retinal eccentricities near 10°. This accuracy was not affected by distractor targets in the peripheral field or temporal uncertainty in stimulus presentation, but was reduced by a similar amount for each stimulus type during saccadic eye movements. Using the alignment task, localization accuracy remained at about 1.3° for P-type stimuli but improved to 0.5° for M-type stimuli. We conclude that both M and P systems play an equally important role in localizing peripheral targets for the purpose of visuo-motor tasks such as pointing, but that the M system may offer an advantage over the P system for the perceptual task of localizing a stimulus relative to nearby targets.

Ocular gaze is anchored to the target of an ongoing pointing movement.

It is well known that, typically, saccadic eye movements precede goal-directed hand movements to a visual target stimulus. Also pointing in general is more accurate when the pointing target is gazed at. In this study, it is hypothesized that saccades are not only preceding pointing but that gaze also is stabilized during pointing in humans. Subjects, whose eye and pointing movements were recorded, had to make a hand movement and a saccade to a first target. At arm movement peak velocity, when the eyes are usually already fixating the first target, a new target appeared, and subjects had to make a saccade toward it (dynamical trial type). In the statical trial type, a new target was offered when pointing was just completed. In a control experiment, a sequence of two saccades had to be made, with two different interstimulus intervals (ISI), comparable with the ISIs found in the first experiment for dynamic and static trial types. In a third experiment, ocular fixation position and pointing target were dissociated, subjects pointed at not fixated targets. The results showed that latencies of saccades toward the second target were on average 155 ms longer in the dynamic trial types, compared with the static trial types. Saccades evoked during pointing appeared to be delayed with approximately the remaining deceleration time of the pointing movement, resulting in "normal" residual saccadic reaction times (RTs), measured from pointing movement offset to saccade movement onset. In the control experiment, the latency of the second saccade was on average only 29 ms larger when the two targets appeared with a short ISI compared with trials with long ISIs. Therefore the saccadic refractory period cannot be responsible for the substantially bigger delays that were found in the first experiment. The observed saccadic delay during pointing is modulated by the distance between ocular fixation position and pointing target. The largest delays were found when the targets coincided, the smallest delays when they were dissociated. In sum, our results provide evidence for an active saccadic inhibition process, presumably to keep steady ocular fixation at a pointing target and its surroundings. Possible neurophysiological substrates that might underlie the reported phenomena are discussed.

Color filling-in under steady fixation: behavioral demonstration in monkeys and humans.

Color filling-in is a phenomenon in which the color of an object appears to be filled-in by the color of the surrounding field. We have studied the question of whether monkeys perceive color filling-in with near-foveal stimuli under steady fixation. Two monkeys were trained to fixate steadily and to attend to a disk, surrounded by an annulus of the complementary color, in parafoveal vision. Using displays in which the color of the disk was gradually changed to that of the annulus, we trained the animals to signal when they perceived a uniform color field. During the experiment, we introduced a small percentage of trials in which the disk color remained constant, and looked for 'filling-in' responses in these trials. Three human subjects were also tested for comparison. All subjects produced 'filling-in' responses with frequencies that were significantly higher for static disks with blurred borders than for moving disks or disks with sharp borders. This indicates that the monkeys' responses reflected perceptual filling-in, rather than random behavior. The time course of filling-in was similar in monkeys and humans. For the blurred static disks, responses occurred first after 3-4 s of fixation, reaching a probability of 0.2-0.8 by the end of 6 s, depending on the subject.

Selective peripheral fading: evidence for inhibitory sensory effect of attention.

A circular array of six discs, three green and three orange in alternate positions, was presented against a uniform grey background. Sixteen observers maintained steady fixation at the centre of the array, and were instructed to direct their attention to three discs of one colour and to ignore the three discs of the other colour. In about 10 s (mean = 11.35 s), some discs started to fade away from awareness. Of those starting to fade, most (mean = 81.3%) were those selected for attention. The faded discs remained out of awareness for up to a few seconds (mean = 1.55 s) during which other discs were clearly visible. The fading increased with eccentricity, a defining characteristic of Troxler fading. However, the selectivity of the fading strongly suggests that voluntary attention can have an inhibitory effect on early sensory processing. Were the fading entirely due to local sensory adaptation, the unattended stimuli would have to be equally adapted and yet somehow remain visible for seconds, which is not plausible.

Acknowledgment

An in-depth analysis of eye movements of schizophrenics has demonstrated defects in several oculomotor subsystems, likely due to processing of sensory information and not to problems in the motor system itself. Schizophrenic subjects made more pursuit tracking errors, due to higher RMS errors, larger phase lag, and more saccades in pursuit. When making saccadic movements they had normal reaction times, saccade velocity and intersaccadic pause, but made more double-jump saccades and overshot the target. Only some had inability to hold steady fixation, but all had an attentional problem in restraining an inappropriate eye movement. The multiple defects suggest a processing problem that is not strictly motor and does not fit any standard definition of attention.

Square-wave jerks induced by pallidotomy in parkinsonian patients.

Square-wave jerks (SWJs) are small, inappropriate saccades that intrude on steady fixation by taking the eye away from the target and then returning it after approximately 200 msec. The pathophysiology of SWJs is unknown; they have not been attributed to any specific lesion. We found that unilateral pallidotomy substantially increased the frequency of SWJs in three patients with Parkinson's disease. This effect is likely due to imbalance in the fixation system caused by asymmetric reactivation of prefrontal cortex via ascending thalamocortical projections. Alternatively, disruption of nigral projections to the superior colliculus might be responsible.

Influence of Scanning Eye Movements on the Scintillating-Grid Illusion

The scintillating grid is an example of a brightness contrast illusion in which bright disks are superimposed on a Hermann grid. Dark spots are perceived within the bright disks as flashing with each flick of the eye (Schrauf et al Vision Research in press). With steady fixation, stimulation must be brief for the illusion to occur. Varying exposure duration with steady fixation, we found the maximum illusion at durations between 210–350 ms (Schrauf et al, 1996 Perception25 Supplement, 78). In the present study voluntary saccadic eye movements were used to produce brief exposures during fixations. The task of 5 trained subjects was to scan scintillation grids of five different spacings (0.5 – 2.0 deg separation of grid elements, observation time 60 s) in a manner yielding a maximum scintillating effect. Eye movements were recorded binocularly at 100 Hz with the Demel Debic 90 infrared corneal reflection tracker (resolution: 6 min arc). For each fixation we calculated latency and position. Durations and amplitudes of the saccades increased with decreasing angular separation of grid elements. When the illusion was maximal, roughly 60% of fixation durations were between 250 and 550 ms. These durations overlap with those obtained with steady fixation combined with variable exposure durations. Unlike the Hermann grid illusion, where illusory dark spots can be perceived at very brief exposure durations, the scintillating grid illusion takes much more time to develop. The long optimal durations found here are discussed in relation to mechanisms of scanning eye movements.

Validity of Listing's law during fixations, saccades, smooth pursuit eye movements, and blinks.

In its original formulation, Listing's law referred only to eye positions during steady fixation. In recent years, however, several studies have suggested that Listing's law can be extended to the movements of the eyes, including during saccades and smooth pursuit. A major problem in deciding whether or not Listing's law is obeyed during eye movements is the influence of any spontaneous fluctuations in torsional eye position. To try to settle this question, the three-dimensional position of the eyes (around the three axes: horizontal, vertical, and torsional) was recorded with dual search coils in five normal subjects during fixations, 20 degrees saccades, blinks, and 20 degrees pursuit movements with a 20 degrees/s stimulus velocity. Eye movements across a wide range of horizontal positions were measured at different elevations of gaze during 11 min. Variability (as reflected in the standard deviation of torsional eye position) was used as a measure of the validity of Listing's law. After linear detrending single trials, each lasting 21.5 s, to remove the effects of drift over minutes, the reduction in the standard deviation of torsional position in tertiary eye positions was 54% assuming a planar and 58% assuming a second-order curved Listing's surface. We attributed this long-term fluctuation of the torsional signal to slippage of the coil on the eye. The remaining variability was mainly due to short-term fluctuation of eye torsion over seconds. The impact of hysteresis, associated with consecutive centrifugal-centripetal horizontal movements, on the variability of torsional eye position appeared negligible. Peak increases in the standard deviation from the fixation baseline after fitting individual Listing's planes for each trial were 348% during blinks, 141% during saccades, and 72% during pursuit movements (median value of five subjects). In conclusion, Listing's law during blinks, saccades, and pursuit is less valid than during fixations, which raises doubts about the existence of an internal "Listing's law operator" for eye movements. Possibly, central eye velocity commands do not comply with Listing's law.

Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques.

1. Although much is known about the neurons that control saccadic eye movements, the precise manner in which they interact is still uncertain. To test the validity of competing models of the pontine saccade generator, neurotoxic lesions were made in the nucleus raphe interpositus (rip), which contains one of the principal types of saccade-related neurons, the omnipause neurons (OPNs). The correlated changes in eye movement were quantified in three juvenile rhesus macaques and compared with the results predicted by different models. 2. After the location of the OPNs was mapped, the rip was subjected to sequential, punctate pressure injections of ibotenic acid. The resulting progressive damage was correlated with changes in saccade metrics, including a decrease in peak saccadic velocity and an increase in saccade duration. 3. The damage to rip and presumably to the OPNs was not associated with a change in the animals' ability to maintain steady fixation of a stationary target. 4. The results suggest that Robinson's original local feedback model of saccade generation should be modified. Either a second integrator should be added or the concept of local feedback should be abandoned entirely. 5. The suggestion that the OPNs are primarily responsible for fixation is probably incorrect. OPNs may contribute to fixation stability along with a number of other sources.