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Effects of cerebellar lesions on saccadic eye movements.

1. Areas of cerebellar cortex related to saccadic eye movements were ablated in three Macaca mulatta monkeys trained to fixate visual targets. There followed a postoperative dysmetria of saccadic eye movements which appeared to be the result of an impairment specifically within the saccadic system. 2. Convergent evidence from two experimental paradigms indicated that the saccadic deficit was a function of the position of the eye in the orbit and did not involve retinal error processing. 3. The pattern of this position-dependent dysmetria suggests that the eye was no longer fully compensating for the elastic restoring forces imposed by the orbital medium and antagonist muscle(s). 4. The similarity of these data to saccadic eye movements of human cerebellar patients and arm movements of rhesus monkeys with cerebellar lesions indicates that the inability to compensate for the differential loads placed on motor systems by the mechanics of those systems may explain several cerebellar symptoms.

Animals↗

Eye movements affect the perceived speed of visual motion.

Eye movements add a constant displacement to the visual scene, altering the retinal-image velocity. Therefore, in order to recover the real world motion, eye-movement effects must be compensated. If full compensation occurs, the perceived speed of a moving object should be the same regardless of whether the eye is stationary or moving. Using a pursue-fixate procedure in a perceptual matching paradigm, we found that eye movements systematically bias the perceived speed of the distal stimulus, indicating a lack of compensation. Speed judgments depended on the interaction between the distal stimulus size and the eye velocity relative to the distal stimulus motion. When the eyes and distal stimulus moved in the same direction, speed judgments of the distal stimulus approximately matched its retinal-image motion. When the eyes and distal stimulus moved in the opposite direction, speed judgments depended on the stimulus size. For small sizes, perceived speed was typically overestimated. For large sizes, perceived speed was underestimated. Results are explained in terms of retinal-extraretinal interactions and correlate with recent neurophysiological findings.

Humans↗

Alteration of eye movements and motion perception in microgravity.

This review article summarizes the results of space research on eye movements and subjective perception during vestibular stimulation. Inflight and postflight changes in reflex eye movements gain are described for head angular rotation (yaw, pitch, and roll), linear acceleration, off-vertical axis rotation, and optokinetic stimulation. There is evidence that changes in eye movements in microgravity primarily occur for head movements in pitch or roll which normally stimulate the otolith organs on Earth, but the data are not conclusive. The relationship between the eye movements gain and self-motion perception remains to be determined. We advocate the use of a human on- and off-axis rotator combined with the measurements of both tri-dimensional eye movement and perceptual response as a method to systematically investigate the adaptive changes in vestibular function to microgravity.

Eye Movements↗

The effects of combined superior temporal polysensory area and frontal eye field lesions on eye movements in the macaque monkey.

We previously found [42] that lesions of the superior temporal polysensory area (STP) cause temporary deficits in the production of eye movements. In order to both define regions participating in the ensuing recovery and to further explore the cortical control of eye movements, we examined the effects of addition of frontal eye field (FEF) lesions to STP lesions, on visual fixation, saccadic eye movements, and smooth pursuit eye movements. Three monkeys received bilateral STP lesions followed by a FEF lesion and as a control, an additional monkey received a bilateral inferior temporal cortex (IT) lesion followed by a FEF lesion. All animals had a profound impairment in foveating the central fixation point. This impairment was completely eliminated by turning on a dim light in the testing chamber. Large neglect-like impairments in making saccades were only seen after combined STP and FEF lesions. Impairments in making smooth pursuit eye movements after combined lesions of STP and FEF were larger than those seen after STP lesions but within the range of deficits that have been reported after FEF lesions alone. The impairment of visual fixation in darkness and the lack of impairment under conditions of dim illumination appear to reflect a specific role for the FEF in spatial orientation in the absence of visual landmarks. The FEF also appears to play a more critical role than STP in smooth pursuit. By contrast, STP and the FEF appear to work cooperatively with respect to the production of saccades. We suggest that cortical oculomotor control can flow either through the midbrain or through the FEF and that the FEF pathway is specifically involved in tasks with a discontiguity between the stimuli and the behavioral response while the midbrain pathways are preferentially involved in more stimulus-driven eye movements.

Animals↗

Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation.

Extracellular recordings were obtained from 319 input units and 304 Purkinje cells (P-cells) in the dorsal paraflocculus of alert monkeys trained to fixate a visual target. They changed discharge rates with either eye movement, eye position, or visual stimulus movement. Of the 319 input units, recorded in the granular layer or white matter, most were mossy fibers (MFs), but 90 (28%) showed characteristic cellular spikes. The latter units were probably granular cells (p-GC). Of the 319 input units, 163 (51%) showed bursts with saccades (burst units) and 62 (19%) showed a prelude on the average 124 ms prior to the onset of saccade (long-lead burst units). Sixty-five (20%) had tonic activity related to eye position and also showed bursts with saccades (burst-tonic units), and the remaining 29 (9%) showed only tonic activity (tonic units). MFs and p-GCs showed no significant differences in the proportion of each type of unit or in their response properties. The majority of burst units (63%) were pan directional, whereas all long-lead burst units had directional selectivity. The preferred directions of long-lead burst, burst tonic, and directionally selective burst units were found in all four quadrants. Position-related activity was found in 48% of the burst-tonic and tonic units to be linearly related to eye position and to show position threshold. The other units also had position thresholds but their activity was not monotonically related to fixation position. Six climbing fibers (CFs), 32 input units (including 13 p-GC), and 8 P-cells showed cyclic responses during sinusoidal movements of a visual pattern. One class of MF units (57%) responded only to the direction, whereas the others responded to both the direction and retinal-slip velocity. Both CF and P-cell units responded to sinusoidal retinal-slip velocity. Of 67 input units, 23 showed cyclic modulation in firing during sinusoidal eye movements in the horizontal plane. Nineteen were burst-tonic and four were tonic units. They also showed position sensitivity. The phase of the cyclic responses tended to lag behind the eye velocity during low-frequency trackings. Of 237 P-cells, 163 (68.8%) discharged with saccades (burst P-cells), 42 (17.7%) paused with saccades (pause P-cells), and 32 (13.5%) discharged with saccades in one direction and paused in the other (burst-pause P-cells). Position sensitivity was found in 38 P-cells; 12 were burst, 5 were pause, and 10 were burst-pause P-cells. Eleven did not respond with saccades.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗

Pursuit and saccadic eye movements in response to unpredictable constant velocity targets.

Pursuit eye movements in response to unpredictable reversals of constant velocity target motion at 20 degrees, 40 degrees and 60 degrees/s were analysed in 20 normal subjects. The gain in smooth pursuit was originally determined by the preceding target duration; the shorter the preceding movement, the longer was the acceleration of pursuit velocity inhibited. The ongoing target duration secondarily affected the gain at faster target velocities by restricting time for eye velocity acceleration. Whereas the saccadic reaction time was around 200 ms, the intersaccadic interval shortened as target velocity increased. The saccadic amplitude increased in direct proportion to an increase in target velocity. The present study showed that, even under irregular stimulations, pursuit eye movement is regulated in a feedforward manner by the perceptual analysis of the preceding target motion, and that corrective saccades in pursuit eye movement correspond to those observed in step displacements, except for the programming on the basis of the changing rate of position error.

Adult↗

Effects of background stimulation upon eye-movement information.

To investigate the effects of background stimulation upon eye-movement information (EMI), the perceived deceleration of the target motion during pursuit eye movement (Aubert-Fleishl paradox) was analyzed. In the experiment, a striped pattern was used as a background stimulus with various brightness contrasts and spatial frequencies for serially manipulating the attributions of the background stimulus. Analysis showed that the retinal-image motion of the background stimulus (optic flow) affected eye-movement information and that the effects of optic flow became stronger when high contrast and low spatial frequency stripes were presented as the background stimulus. In conclusion, optic flow is one source of eye-movement information in determining real object motion, and the effectiveness of optic flow depends on the attributes of the background stimulus.

Adult↗

Stability of exploratory eye movements as a marker of schizophrenia--a WHO multi-center study. World Health Organization.

The exploratory eye movements of patients with schizophrenia reportedly differ from those of patients without schizophrenia and healthy controls. In an attempt to determine whether exploratory eye movements provide valid markers for schizophrenia, the present collaborative study was conducted in six countries to analyze the stability of and variation in the following parameters of exploratory eye movements: the number of eye fixations (NEFs) and mean eye scanning length (MESL) in a retention task; the cognitive search score (CSS) that indicates how frequently the eye focused on each important area of a figure in order to recognize it in a comparison task; and the responsive search score (RSS), which reflects the frequency of eye fixations on each section of a figure in response to questioning in a comparison task. In addition, we investigated the validity of the currently employed discriminant function to extract a common feature of schizophrenia by applying it to the findings of the present study. The exploratory eye movements of 145 patients with schizophrenia, 116 depressed patients and 124 healthy controls at seven WHO collaborative centers in six countries were measured using eye mark recorders during viewing of stationary S-shaped figures in two sequential tasks. The RSSs of patients with schizophrenia were found to be significantly lower than those of depressed patients or healthy controls irrespective of geographical location, with no significant difference existing between the RSSs for depressed patients and those for healthy controls. By inserting the RSS and NEF data for each subject into the formula used to calculate discriminant function, patients with schizophrenia could be discriminated from depressed patients and healthy controls with a sensitivity of 89.0% and a specificity of 86.7%. The RSS is an exploratory eye movement parameter that detected schizophrenia irrespective of culture, race and various other subject variables. Furthermore, it is indicative of the stable, significant difference that exists between subjects with and without schizophrenia. The results of discriminant analysis confirm the previously reported validity of discriminant function.

Adult↗

Saccades exert spatial control of motion processing for smooth pursuit eye movements.

Saccades modulate the relationship between visual motion and smooth eye movement. Before a saccade, pursuit eye movements reflect a vector average of motion across the visual field. After a saccade, pursuit primarily reflects the motion of the target closest to the endpoint of the saccade. We tested the hypothesis that the saccade produces a spatial weighting of motion around the endpoint of the saccade. Using a moving pursuit stimulus that stepped to a new spatial location just before a targeting saccade, we controlled the distance between the endpoint of the saccade and the position of the moving target. We demonstrate that the smooth eye velocity following the targeting saccade weights the presaccadic visual motion inputs by the distance from their location in space to the endpoint of the saccade, defining the extent of a spatiotemporal filter for driving the eyes. The center of the filter is located at the endpoint of the saccade in space, not at the position of the fovea. The filter is stable in the face of a distracter target, is present for saccades to stationary and moving targets, and affects both the speed and direction of the postsaccadic eye movement. The spatial filter can explain the target-selecting gain change in postsaccadic pursuit, and has intriguing parallels to the process by which perceptual decisions about a restricted region of space are enhanced by attention. The effect of the spatial saccade plan on the pursuit response to a given retinal motion describes the dynamics of a coordinate transformation.

Animals↗

Pursuit eye movements in late-onset esotropia.

Horizontal, smooth pursuit eye movements were recorded from adults and children with infantile and late-onset esotropia using a remote, video-based, eye-movement recording system. Each subject monocularly tracked a 0.5-degree target moving back and forth on a video monitor at a constant velocity of 10 degrees, over a range of 12 degrees. Each subject's nasal and temporal gain (eye velocity/target velocity) was measured. Confirming the results of previous studies, we found that infantile esotropes had asymmetrical pursuit eye movements (nasal gain greater than temporal gain) while late-onset esotropes had symmetrical gains. However, unlike previous investigators, we found that half of the late-onset esotropes had impaired pursuit gain. The magnitude of the pursuit abnormality and the amount of refractive error were correlated--patients with the highest refractive error had the lowest pursuit gain.

Adult↗

Emotional processing during eye movement desensitization and reprocessing therapy of Vietnam veterans with chronic posttraumatic stress disorder.

This study examined emotional processing and outcome in 17 Vietnam veterans with chronic posttraumatic stress disorder (PTSD) who underwent eye movement desensitization and reprocessing (EMDR) therapy, with and without the eye movement component, in a crossover design. Results supported the occurrence of partial emotional processing, but there were no differences in its extent in the eye-movement versus eyes-fixed conditions. Therapy produced a modest to moderate overall improvement, mostly on the impact of Event Scale. There was slightly more improvement in the eyes-fixed than eye-movement condition. There was little association between the extent of emotional processing and therapeutic outcome. In our hands, EMDR was at least as efficacious for combat-related PTSD as imaginal flooding proved to be in a previous study, and was better tolerated by subjects. However, results suggest that eye movements do not play a significant role in processing of traumatic information in EMDR and that factors other than eye movements are responsible for EMDR's therapeutic effect.

Adult↗

Deficits in vertical and torsional eye movements after uni- and bilateral muscimol inactivation of the interstitial nucleus of Cajal of the alert monkey.

The mesencephalic interstitial nucleus of Cajal (iC) is considered the neural integrator for vertical and torsional eye movements and has also been proposed to be involved in saccade generation. The aim of this study was to elucidate the function of iC in neural integration of different types of eye movements and to distinguish eye movement deficits due to iC impairment from that of the immediately adjacent rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). We addressed the following questions: (1) According to the neural integrator hypothesis, all eye movements including the saccadic system and the vestibulo-ocular reflex (VOR) share a common neural integrator. Do iC lesions impair gaze-holding function for vertical and torsional eye positions and the torsional and vertical VOR gain to a similar degree? (2) What are the dynamic properties of vertical and torsional eye movements deficits after iC lesions, e.g., the specificity of torsional and vertical nystagmus? (3) Is iC involved in saccade generation? We performed 13 uni- and three bilateral iC inactivations by muscimol microinjections in four alert monkeys. Three-dimensional eye movements were studied under head-stationary conditions during vertical and torsional VOR. Under static conditions, unilateral iC injections evoked a shift of Listing's plane to the contralesional side (up to 20 degrees), which increased (ipsilesional ear down) or decreased (ipsilesional ear up) by additional static vestibular stimulation in the roll plane, i.e., ocular counterroll was preserved. The monkeys showed a spontaneous torsional nystagmus with a profound downbeat component. The fast phases of torsional nystagmus always beat toward the lesion side (ipsilesional). Pronounced gaze-holding deficit for torsional and vertical eye positions (neural integrator failure) was reflected by the reduction of time constants of the exponential decay of the slow phase to 330-370 ms. Whereas the vertical oculomotor range was profoundly decreased (up to 50%) and vertical saccades were reduced in amplitude, saccade velocity remained normal and horizontal eye movements were not affected. Bilateral iC injections reduced the shift of Listing's plane caused by unilateral injections, i.e., back toward the plane of zero torsion. Torsional nystagmus reversed its direction and ceased, whereas vertical nystagmus persisted. In contrast to unilateral injection, there was additional upbeating nystagmus. Time constants of the position integrator of the gaze-holding system did not differ between unilateral and bilateral injections. The range of stable vertical eye positions and saccade amplitude was smaller when compared with unilateral injections, but the main sequence remained normal. Dynamic vestibular stimulation after unilateral iC injections had virtually no effect on torsional and vertical VOR gain and phase at the same time when time constants already indicated severe integrator failure. Torsional VOR elicited a constant slow-phase velocity offset up to 30 degrees toward the contralesional side, i.e., in the opposite direction to spontaneous torsional nystagmus. Likewise, vertical VOR showed a velocity offset in an upward direction, i.e., opposite to the spontaneous downbeat nystagmus. Contralesional torsional and upward vertical quick phases were missing or severely reduced in amplitude but showed normal velocity. In contrast, bilateral iC injections reduced the gain of the torsional and vertical VOR by 50% and caused a phase lead of 10-20 degrees (eye compared with head velocity). We propose that the slow-phase velocity offset during torsional and vertical VOR reflects a vestibular imbalance. It therefore appears likely that the vertical and torsional nystagmus after iC lesions is not only caused by a neural integrator failure but also by a vestibular imbalance. Unilateral iC injections have clearly differential effects on the VOR and the gaze-holding function. (ABSTRACT TRUNCATED)

Animals↗

Eye movements and reversal rates of ambiguous patterns.

To study the influence of eye movements on the time course of perceptual alternation of ambiguous patterns, we recorded the reversal signals and eye movements of four subjects, during prolonged observations of a Necker cube, under three experimental conditions: unrestricted normal viewing, instruction-restricted normal viewing, and imperfectly stabilized viewing. An important decrease in the frequency of saccadic eye movements and a significant increase in the reversal rates were shown by all subjects under imperfectly stabilized viewing over the normal unrestricted viewing. Moreover, three out of four subjects showed a significant decrease in their reversal rates when changing from the normal to instruction-restricted viewing. Results are discussed in terms of the role and time cost of scanning eye movements in perceptual processes.

Adult↗

Disorders of eye movement in myotonic dystrophy.

Horizontal saccades and smooth pursuit eye movements were studied in 26 patients with myotonic dystrophy. Clinical neuro-ophthalmological investigations in 1 patient revealed an inability to achieve a full range of eye movements. Electro-oculography showed a significant decrease of the maximum velocity of the visually-guided saccades in 83% of the patients. Smooth pursuit eye movements were not significantly different from age-matched controls. Visual evoked potential (VEP) latencies (P100) were significantly prolonged compared with controls in 64% of the patients. The saccadic latency of the visually-guided saccades was correlated with the prolonged VEP latencies, indicating that lesions in the primary visual pathways probably contribute to the oculomotor dysfunction. The isolated decrease of the maximum velocity of the saccades in combination with EMG findings favours a peripheral (dystrophic) pathophysiological mechanism.

Adolescent↗

Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys.

1. Our goal was to assess whether visual motion signals related to changes in image velocity contribute to pursuit eye movements. We recorded the smooth eye movements evoked by ramp target motion at constant speed. In two different kinds of stimuli, the onset of target motion provided either an abrupt, step change in target velocity or a smooth target acceleration that lasted 125 ms followed by prolonged target motion at constant velocity. We measured the eye acceleration in the first 100 ms of pursuit. Because of the 100-ms latency from the onset of visual stimuli to the onset of smooth eye movement, the eye acceleration in this 100-ms interval provides an estimate of the open-loop response of the visuomotor pathways that drive pursuit. 2. For steps of target velocity, eye acceleration in the first 100 ms of pursuit depended on the "motion onset delay," defined as the interval between the appearance of the target and the onset of motion. If the motion onset delay was > 100 ms, then the initial eye movement consisted of separable early and late phases of eye acceleration. The early phase dominated eye acceleration in the interval from 0 to 40 ms after pursuit onset and was relatively insensitive to image speed. The late phase dominated eye acceleration in the interval 40-100 ms after the onset of pursuit and had an amplitude that was proportional to image speed. If there was no delay between the appearance of the target and the onset of its motion, then the early component was not seen, and eye acceleration was related to target speed throughout the first 100 ms of pursuit. 3. For step changes of target velocity, the relationship between eye acceleration in the first 40 ms of pursuit and target velocity saturated at target speeds > 10 degrees /s. In contrast, the relationship was nearly linear when eye acceleration was measured in the interval 40-100 ms after the onset of pursuit. We suggest that the first 40 ms of pursuit are driven by a transient visual motion input that is related to the onset of target motion (motion onset transient component) and that the next 60 ms are driven by a sustained visual motion input (image velocity component). 4. When the target accelerated smoothly for 125 ms before moving at constant speed, the initiation of pursuit resembled that evoked by steps of target velocity. However, the latency of pursuit was consistently longer for smooth target accelerations than for steps of target velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

Acceleration↗

Toward an appropriate baseline for measures of eye movement behavior during reading.

In empirical studies of human eye movement behavior during reading, it is common to compute various summary measures from the data, but these measures are typically not evaluated with respect to corresponding measures of baseline performance. The authors present a method for deriving an appropriate baseline by mapping the actual behavior to a random perturbation of the text being read, and they find surprising similarities between the baseline and the empirical data. The practical message from these findings is that the importance of a particular factor in explaining either empirical or simulated eye movement patterns should be evaluated using an appropriate baseline. In addition to this methodological point, the authors suggest that eye movement behavior in reading may be constrained by the properties of an eye-guidance system that has adapted to the coarse-grained statistical properties of written language.

Eye Movements↗

Are eye movement evoked potentials different from pattern reversal evoked potentials?

The averaged lambda wave elicited by saccadic eye movements across a checkerboard pattern has been reported to differ from checkerboard reversal evoked responses, even when the electroencephalographic responses were corrected for the artefact caused by the movement of the dipole moment of the eye itself. Because of these differences it was suggested that the recording of the lambda wave might provide extra information in pathological circumstances. We performed experiments in which the parameters of the pattern (high contrast checkerboard pattern, 20' checks, large field 72 x 72 degrees) shift across the retina were carefully adjusted. For instance, eye movements were made across an integer and odd number of checks in order to mimic the pattern reversal. Furthermore, the timing of the pattern movement in the pattern reversal condition was adjusted so as to simulate the saccadic eye movement. The results seem to suggest that the reported dissimilarities between pattern reversal and eye movement evoked responses can be accounted for by the small differences of the retinal shift in the two conditions.

Evoked Potentials↗

Pulvinar neuron responses to spontaneous and trained eye movements and to light flashes in squirrel monkeys.

Single unit responses were recorded in the pulvinar nucleus of the squirrel monkey (Saimiri sciureus) while awake and alert, with the head fixed but free to make eye movements. Peri-saccadic time histograms revealed only post-saccadic responses to eye movements made spontaneously in the dark or in a uniformly illuminated field (Ganzfeld), or to trained eye movements made in response to a spot of light in the periphery. Of 120 pulvinar neurons that responded to eye movements in the light, approximately one-quarter was responsive to eye movements in the dark. In one group of monkeys about half of the eye movement-responsive cells in the light were responsive to light flash in the dark; in another group approximately half of the eye movement-responsive cells in the light were also responsive to trained eye movements. Of particular interest is the fact that pulvinar neurons responsive to eye movements were located within a restricted region oriented vertically and cutting across lateral and inferior pulvinar, rostrally, and lateral and medial pulvinar, caudally. The results have been interpreted as supporting the concept of convergence and integration of visual and oculomotor input in the pulvinar and also its potential role in the mediation of visual attention.

Animals↗