Selective adaptation of internally triggered saccades made to visual targets

We examined whether internally triggered saccades made to a nonjumping target (I-saccades) could be adapted independently from externally triggered saccades induced by a jumping target (E-saccades). Five subjects made I-saccades between two fixed targets, one placed straight ahead and the other one positioned at an eccentricity of 17.5°. The peripheral target was displaced to an eccentricity of 8.75° during the saccadic movements toward this target. Amplitudes of the I-saccades made from the central to the peripheral target before and after adaptation were compared with each other. Saccadic amplitudes after adaptation were between 10% and 42% smaller than those before adaptation. E-saccades induced by a single target which jumped from straight ahead to the same peripheral target position as was used for the I-saccades were also measured before and after the adaptation of I-saccades. Amplitudes of E-saccades before and after adaptation were hardly different from each other except in one subject. The mean decreases in amplitude of the two types of saccades, averaged over all subjects, were 21% for I-saccades and 5% for E-saccades. These results show that I-saccades can be adapted to changed visual conditions while E-saccades remain unadapted. We conclude from this finding that I-saccades and E-saccades are generated by at least partially different neural mechanisms.     

Initiation of smooth pursuit in humans

We examined the influence of target saliency on the initiation of smooth pursuit. The eye movements of five human subjects were recorded with the scleral search-coil technique. A video-projection system was used to create a pursuit target, consisting of a cluster of 14 red or green dots (0.5 degrees squares) extending randomly over a 3 degrees x3 degrees region, and a surrounding background, consisting of stationary, random dots of the same size and density extending over an area 70 degrees x 40 degrees. When the dots in the background and the target were of the same color, the target was indistinguishable from the background until it started to move. On the other hand, when the colors were different, the target was salient, even when stationary. We measured the changes in eye position over the 70-ms interval starting 70 ms after the onset of target motion (initial tracking response). When the target moved toward the fovea (centripetal motion), the initial tracking responses developed earlier when the dots in the target and background were of different color than when the two sets of dots were of the same color. However, in order to see this effect of target salience, it was critical that the colors be different before the onset of motion, but not afterwards. When the target moved away from the fovea (centrifugal motion), the initial tracking responses were independent of whether the colors of the target and the background were the same or different. Our data indicate that the initiation of tracking responses is very sensitive to the saliency of the target before the onset of target motion when that motion is toward the fovea.     

Explicit eye movements failed to facilitate the precision of subsequent attentional localization

This study investigated the usefulness of explicit spatial coordinates from eye movements for the precision of covert shifts of attention within dense arrays of items. Observers shifted their attention covertly from one item to the next in response to a series of beeps and reported the color of the disc on which the series ended, providing an estimate of the accuracy of the “attentional walk”. We compared performance in this task when only covert shifts of attention were done to performance when observers first executed an explicit eye movement to the starting point of the attentional walk before beginning the covert attentional walk. The hypothesis was that the eye movement would activate explicit coordinates of the starting point of the attentional walk within brain systems that are involved in controlling both shifts of attention and eye movements. This in turn would provide an anchor for the attentional walk, thereby improving performance. The evidence did not support this hypothesis. Performance was no better with an explicit eye movement prior to the attentional walk than without one. This suggests that covert orienting—shifting attention—and overt orienting—shifting the eyes—access the same coordinate system and therefore activating new coordinates interferes with the old ones, no matter what the system of orienting is.     

Impairment of extraretinal eye position signals after central thalamic lesions in humans

Accuracy of four different types of memory-guided saccades was studied in two patients with a small central thalamic lesion, probably involving the region of the internal medullary lamina (IML), and in a control group. In the first paradigm, the eyes and head remained immobile between the time of the presentation of the visual target to be remembered and the memory-guided saccade. In the other three paradigms, the eyes were displaced during the same period (before the memory-guided saccade) by either visually-guided saccades, a smooth pursuit eye movement or a body movement (with vestibulo-ocular reflex suppression). Therefore, in these three paradigms, the initial eye displacement required the use of extraretinal eye position to produce accurate memory-guided saccades. Compared with the control group, the two patients had normal accuracy in the first memory-guided saccade paradigm, in which there was no initial eye displacement, but markedly impaired saccade accuracy in the other three paradigms. These results suggest that the cortical areas triggering saccades did not receive correct extraretinal eye position signals. They are consistent with an impairment of the efference copy, which could be distributed to the cortical ocular motor areas by the IML.     

Hypometric primary saccades of schizophrenics in a delayed-response task

In this study, the execution of delayed saccades in 15 DSM-III-R-schizophrenic patients and 15 normal subjects was investigated. While looking at a central fixation cross, a peripheral target was randomly presented at 10° eccentricity. Subjects were instructed to saccade to the target when the fixation cross was switched off after 500 ms. Two experiments were conducted: (a) a delayed-saccade task and, (b) a memoryguided saccade task, that is, the peripheral target was switched off together with the fixation cross. In the delayed-saccade task, amplitudes of regular saccades did not differ between schizophrenic patients and normals. In the memory-guided saccade task, schizophrenic subjects showed marked hypometric saccades. Incorrect delayed saccades (while the fixation cross was on) were also hypometric in schizophrenics, but not in normal controls. The final eye position, i.e., the position reached after the execution of correction saccades, however, did not differ between patients and controls. This means that schizophrenics show a deficit in the programming of primary saccades, if the fixation point and the peripheral target are (a) both visually presented or (b) both memorized. The results support the hypothesis that these saccades are the result of an averaging effect between the fixation point and the peripheral target. It is further hypothesized that these deficits might be explained by a lack of prefrontal inhibition of ocular fixation areas.     

Spatial and temporal aspects of eye-hand coordination across different tasks

The way in which saccadic eye movements are elicited influences their latency and accuracy. Accordingly, different tasks elicit different types of saccades. Using the tasks steps, gap, memory, scanning and antisaccade, we analyzed combined eye and hand movements to determine whether both motor systems share control strategies. Errors and latencies were measured to examine whether changes in eye motor behavior are reflected in hand motor behavior. Directional and variable errors of eye and hand changed differently according to the tasks. Moreover, errors of the two systems did not correlate for any of the tasks investigated. Contrary to errors, mean latencies of eye movements were organized in the same pattern as hand movements. A correlation of latencies indicates that both motor systems rely on common information to initiate movement. Temporal coupling was stronger for intentional tasks than for reflexive tasks.     

Auditory cues and inhibition of return: the importance of oculomotor activation

We studied the effects of eccentric auditory cues to clarify the conditions that evoke inhibition of return (IOR). We found that auditory cues positioned 12° to the left or right of midline failed to produce IOR whereas visual cues produced IOR under the same experimental conditions. The eccentric auditory cues elicited automatic orienting as evidenced by more rapid detection of cued than uncued visual targets at short stimulus onset asynchrony. Yet these same cues did not produce IOR unless observers were required to saccade to the cue and back to center before generating a manual detection response. Thus, under the conditions examined herein automatic orienting was not sufficient to evoke IOR, but oculomotor activation appeared to be essential. The functional significance of IOR and the question of modality-specific orienting processes are considered.     

Independent contributions of the orienting of attention,fixation offset and bilateral stimulation on human saccadic latencies

In a series of experiments we examined the effects of the endogenous orienting of visual attention on human saccade latency. Three separate manipulations were performed: the orienting of visual attention, the prior offset of fixation (gap paradigm) and the bilateral presentation of saccade targets. Each of these manipulations was shown to make an independent contribution to saccade latency. In experiments 1 and 2 subjects were instructed to orient their attention covertly to a location by a verbal pre-cue; targets could appear in the attended hemifield (valid) or in the non-attended hemifield (invalid) together with a no-instruction (neutral) condition. Saccades were made under fixation gap and overlap conditions, to either single targets or two bilaterally presented targets which appeared at equal and opposite eccentricities in both hemifields. The results showed a large increase (cost) of saccade latency to invalid targets and a small non-significant decrease (benefit) of saccade latency to valid targets. The cost associated with invalid targets replicates the meridian crossing effect shown in manual reaction time experiments and is consistent with the hemifield inhibition and premotor models of attentional orienting. The use of a gap procedure produced a generalised facilitation of saccade latency, which was not modified by the prior orienting of visual attention. The magnitude of the gap effect was similar for saccades made to attended and non-attended stimulis. This suggests that the gap effect may be due to ocular motor disengagement, or a warning signal effect, rather than to the prior disengagement of visual attention. When two targets were presented simultaneously, one in each hemifield, saccade latency was slowed compared with the single target condition. The magnitude of this slowing was unaffected by the prior orienting of visual attention or by the fixation condition. The slowing was examined in more detail in experiment 3, by presenting targets with brief offset delays. The latency increase was maximal if the two targets were presented simultaneously and decreased if the distractor appeared at short intervals (20–80 ms) before or after the saccade target onset. If the non-attended stimulus was presented at greater intervals (160, 240 ms) before the saccade target, then a facilitation effect was observed. This demonstrates that the onset of a distractor in the non-attended hemifield can have both an inhibitory and a facilitatory effect on a saccade production.     

Effects of anterior cingulate cortex lesions on ocular saccades in humans

Cerebral blood flow studies in humans suggest that the anterior cingulate cortex (ACC) could be involved in eye movement control. In two patients with a small infarction affecting the posterior part of this area (on the right side) and in ten control subjects, we studied several paradigms of saccadic eye movements: gap task, overlap task, antisaccades (using either a 5° or 25° lateral target), memory-guided saccades with a short (1 s) or long (7 s) delay, and sequences of memory-guided saccades. Compared with controls, patients had normal latency in the gap task but increased latency in the other tasks. The gain of memory-guided saccades was markedly decreased, bilaterally, whatever the duration of the delay. Patients made more errors than controls in the antisaccade task when the 5° lateral target was used, and a higher percentage of chronological errors in the sequences of saccades. These results show that the posterior part of the right ACC plays an important role in eye movement control and suggest that this area could correspond to a “cingulate eye field” (CEF). The role of this hypothetical CEF could be an early activation exerted on the frontal ocular motor areas involved in intentional saccades and also a direct action on brainstem ocular premotor structures. Received: 8 November 1996 / Accepted: 14 October 1997     

Binaural weighting of pinna cues in human sound localization

Human sound localization relies on binaural difference cues for sound-source azimuth and pinna-related spectral shape cues for sound elevation. Although the interaural timing and level difference cues are weighted to produce a percept of sound azimuth, much less is known about binaural mechanisms underlying elevation perception. This problem is particularly interesting for the frontal hemifield, where binaural inputs are of comparable strength. In this paper, localization experiments are described in which hearing for each ear was either normal, or spectrally disrupted by a mold fitted to the external ear. Head-fixed saccadic eye movements were used as a rapid and accurate indicator of perceived sound direction in azimuth and elevation. In the control condition (both ears free) azimuth and elevation components of saccadic responses were well described by a linear regression line for the entire measured range. For unilateral mold conditions, the azimuth response components did not differ from controls. The influence of the mold on elevation responses was largest on the ipsilateral side, and declined systematically with azimuth towards the side of the free ear. Near the midsagittal plane the elevation responses were clearly affected by the mold, suggesting a systematic binaural interaction in the neural computation of perceived elevation that straddles the midline. A quantitative comparison of responses from the unilateral mold, the bilateral mold and control condition provided evidence that the fusion process can be described by binaural weighted averaging. Two different conceptual schemes are discussed that could underlie the observed responses. Electronic Publication     

Rehearsal by eye movement improves visuomotor performance in cerebellar patients

In order to assess the effect of rehearsal by eye movement alone on visuomotor performance, the eye movements and visually guided stepping of two cerebellar patients were monitored before and after a first and second batch of eye-movement rehearsals, in which patients made saccadic eye movements to the first 6 footfall targets (in a sequence of 18) whilst standing stationary at the start of the walkway. There was a marked improvement in oculomotor and locomotor performance following the second batch of eye-movement rehearsal. Both patients showed reduced occurrence of saccadic dysmetria, evident as a significant increase in the proportion of single to multi-saccadic eye movements (from 46 to 77% for DB and from 75 to 94% for TP). This was accompanied by increased regularity and accuracy of stepping in both patients, and decreased stance and double support phase durations (one patient only). Separate testing confirmed that these improvements in eye movements and stepping did not result from simple repetition of the task. This is the first demonstration of a technique--rehearsal by eye movement--that improves the visuomotor performance of cerebellar patients. It is compelling evidence for our proposal that during visually guided stepping the locomotor control system is dependent on assistance from the oculomotor control system.     

Experimental tests of a neural-network model for ocular oscillations caused by disease of central myelin

Spontaneous sinusoidal oscillations of the eyes are a feature of disorders affecting central myelin, including multiple sclerosis. The mechanism responsible for these oscillations (pendular nystagmus) is unknown. We tested the hypothesis that pendular nystagmus is due to instability of the neural integrator, a network of neurons that normally guarantees steady gaze by mathematically integrating premotor signals. It was possible to make a model of the neural integrator unstable, and abnormal feedback then produced sustained oscillations so that it simulated pendular nystagmus. One prediction of the model is that a large premotor signal, such as is required to generate a rapid (saccadic) eye movement, will transiently suppress the activity of some neurons in the network, and that this will "reset" the oscillations, i.e., produce a phase shift; larger saccades will produce greater phase shifts. Alternatively, if the source of pendular nystagmus is outside the neural integrator (i.e., is present on velocity inputs to the stable integrator), then it may not be possible to reset the oscillations with a saccadic eye movement. We compared the phase relationships of pendular nystagmus prior to and following saccades in six patients with multiple sclerosis (MS). All patients showed phase shifts (median 64 degrees) of their ocular oscillations following large (more than 10 degrees) saccades; smaller saccades (less than 5 degrees) caused smaller phase shifts (median 17 degrees). Our findings suggest that, in MS, pendular nystagmus arises from an instability in the feedback control of the neural integrator for eye movements, which depends on a distributed network of neurons in the brainstem and cerebellum.     

Mixture analysis of smooth pursuit eye movements in schizophrenia

The goal of this study was to replicate and extend previous findings indicating that the eye movement data of schizophrenic patients is best represented by the mixture of two groups, one of which has distinctly poor performance. Forty-nine schizophrenic patients and 32 normal controls had their smooth pursuit eye movements quantified by calculating the root mean square (RMS) deviation between the target and eye waveforms. Based on the finding of mixture in the distribution of RMS error, the patients were divided in to low (better tracking) and high (worse tracking) RMS error subgroups. The high RMS error patient had abnormally decreased gain. Both patient subgroups had abnormally increased frequency of catch-up saccades and increased phase lag. Distinguishing between these two subgroups may be useful in clarifying the pathophysiology of abnormal pursuit and its relationship to heterogeneity in schizophrenia.     

Eye movement related neurons in the cerebellar nuclei of the alert monkey

Summary In all cerebellar nuclei saccade related neurons can be recorded. In the alert untrained Rhesus monkey these neurons can be classified into short-lead bursters, complex bursters, and tonic burst neurons. Short-lead bursters can be related to the onset or to the length of saccades and blinks. Complex bursters are active in the early (acceleration) or late (deceleration) phase of saccades. Tonic burst neurons, in addition, display maintained activity which is modulated in a complex manner with eye position, during periods of fixation or slow-phase nystagmus. In agreement with clinical and previous experimental data we view these cerebellar output neurons as elements which are not part of the system which basically generates eye movements, but rather as a system which could influence the execution of movements.     

Similarity of Eye Movement Characteristics in REM Sleep and the Awake State

The eye movements of REM (Rapid Eye Movement) sleep have been reported to be slower, i.e., to show reduced velocities, compared to those of the awake state. We demonstrated that REM sleep eye movements are in fact similar in velocity to awake state eye movements under the condition of no visual input (eyes open or closed). Furthermore, we observed that oculomotor velocities and trajectories in REM sleep are more similar to head-unrestrained (normal vision) than head-restrained (bite board) conditions in the awake state. The DC electro-oculogram (EOG) was utilized for all measurements. Both head-unrestrained and REM sleep eye movements contained looped trajectories not present when the head was immobilized. Eyelid closure had little effect beyond that of total darkness. Recumbent body position did not significantly alter velocity characteristics. These data indicate that the eye movements of REM sleep are more congruent with the hallucinated locomotor activity of the dream than with the postural immobility’ of the dreamer.     

Influence of transcranial magnetic stimulation on the execution of memorised sequences of saccades in man

Memorised sequences of saccades are cortically controlled by the supplementary motor area (SMA), as shown in animal experiments and in humans with isolated SMA lesions. We applied transcranial magnetic stimulation (TMS) in eight healthy subjects executing memorised sequences of saccades. Sequences of three targets were presented. Then, upon a go-signal, the subjects had to execute the appropriate sequences. Ten to fifteen sequences were performed in each experiment, and the number of errors were counted. The number of errors increased significantly if TMS was given 80 ms before or 60 ms after the go-signal, with the stimulation coil overlying the SMA. There was no significant increase in errors if different stimulation intervals were chosen (160ms and 120ms before the go-signal; 100 ms, 140 ms or 240 ms after the go-signal), if the coil was positioned inappropriately (e.g. over the occipital cortex), or if the stimulator output was too low. We conclude that TMS can interfere specifically with the function of the SMA during a critical time interval close to the go-signal.     

Amplitude criteria and anticipatory saccades during smooth pursuit eye movements in schizophrenia.

Increased frequency of anticipatory saccades during smooth pursuit eye movements is a potential marker of genetic risk for schizophrenia even in the absence of clinical symptomology. The operational definition of anticipatory saccades has often included an amplitude criterion; however, these amplitude criteria have often differed across studies. This study reports on the effect of varying amplitude criteria on the effect size in a comparison of 29 schizophrenic adults and 29 normal subjects during a 16.7 degrees/s constant velocity task. The inclusion of small amplitude anticipatory saccades, with amplitudes of 1-4 degrees, consistently increased effect size (largest effect size = 1.61). The inclusion of large anticipatory saccades, with amplitudes of 4 degrees or greater, had an inconsistent impact on effect size. The separation of anticipatory saccades into leading saccades (anticipatory saccades with amplitude 1-4 degrees) and large anticipatory saccades (amplitude > 4 degrees) deserves further exploration.     

The gap effect and inhibition of return: interactive effects on eye movement latencies

Three experiments are reported with two types of manipulations that are known to affect the latency with which subjects can initiate saccadic eye movements. The first manipulation involves the temporal relation between the offset of a visual fixation point and the onset of a peripheral target (the gap effect). The second manipulation involves the prior allocation and removal of visual attention (inhibition of return). In two experiments, the gap effect was smaller for saccades to previously attended locations than to previously unattended locations. The results suggest an important link between the two phenomena and provide new insights into the brain mechanisms underlying visual attention and eye movements.     

Why are saccades influenced by the Brentano illusion?

In the Brentano version of the Müller-Lyer illusion one part looks longer and the other looks shorter than it really is. We asked participants to make saccadic eye movements along these parts of the figure and between positions on the figure and a position outside the illusion. By showing that saccades from outside the figure are not influenced by the illusion, we demonstrate that the reason that saccades along the figure are influenced is that the incorrectly judged length is used to plan the amplitude of the saccade. This finding contradicts several current views on the use of visual information for action. We conclude that actions are influenced by visual illusions, but that such influences are only apparent if the action is guided by the attribute that is fooled by the illusion.     

Inhibition of return in saccadic eye movements

Inhibition of return (IOR) is a phenomenon in which responses generated to targets at previously attended locations are delayed. It has been suggested that IOR affords a mechanism for optimizing the inspection of novel locations and that it is generated by oculomotor reflexes mediated by the superior colliculus. In this investigation, we measured the effects of IOR on the metrics of saccadic eye movements made to novel and previously attended locations. Saccades made to cued target locations, as well as to other targets within the same hemifield, had longer latencies than saccades made towards the novel, uncued hemifield. We further found that the amplitudes of saccades towards the cued hemifield were more hypometric, but only when the amplitude could not be pre-programmed. These results provide evidence that IOR influences spatial, as well as temporal, parameters of saccadic eye movements and suggest that the exogenous orienting of attention, in addition to influencing target detection, also influences oculomotor programming.