Primary Saccade Research Articles

Ocular motor differences between melancholic and non-melancholic depression

BackgroundMajor depressive disorder may be a heterogeneous disorder, yet melancholic depression is the most consistently described subtype, regarded as qualitatively different to non-melancholic depression in terms of cognitive and motor impairments. Eye movement studies in depression are infrequent and findings are inconclusive. MethodsThis study employed a battery of saccadic eye movement tasks to explore reflexive saccades, as well as higher order cognitive aspects of saccades including inhibitory control and spatial working memory. Nineteen patients with major depressive disorder (9 melancholic; 10 non-melancholic) and 15 healthy controls participated. ResultsDifferences were revealed between melancholic and non-melancholic patients. Melancholia was associated with longer latencies, difficulty increasing peak velocities as target amplitudes increased, and hypometric primary saccades during the predictable protocol. In contrast, the non-melancholic depression group performed similarly to controls on most tasks, but saccadic peak velocity was increased for reflexive saccades at larger amplitudes. LimitationsMost patients were taking antidepressant medication. ConclusionsThe latency increases, reduced peak velocity and primary saccade hypometria with more severe melancholia may be explained by functional changes in the fronto–striatal–collicular networks, related to dopamine dysfunction. In contrast, the serotonergic system plays a greater role in non-melancholic symptoms and this may underpin the observed increases in saccadic peak velocity. These findings provide neurophysiological support for functional differences between depression subgroups that are consistent with previous motor and cognitive findings.

Saccade Adaptation in Williams-Beuren Syndrome

To investigate the capacity for rapid saccade adaptation in Williams-Beuren Syndrome (WBS), a genetic neurodevelopmental disorder, in which it has been observed that saccadic accuracy is severely reduced. Saccade amplitude modification was elicited by backward steps (30% of target eccentricity) during the primary saccade in a classic saccade-adaptation paradigm. Patients with WBS showed a significant decrease in saccade amplitude. Furthermore, we observed that higher saccade accuracy before adaptation was related to more adaptation. The increased variability in motor performance does not abolish the ability for saccadic adaptation in subjects with WBS. Our results are congruent with the notion that part of the behavioral deficits observed in WBS may have a cerebellar origin.

The impact of mild closed head injury on involuntary saccadic adaptation: Evidence for the preservation of implicit motor learning

Objective: Mild closed head injury (CHI) can impair performance on volitional saccades (fast eye movements), with poorer saccade accuracy being one of the principal deficits. Assessing a patient group with known deficits of volitional saccades, the authors investigated whether mild CHI similarly impairs the implicit adaptation of visually-guided (reflexive) saccades, an important process which maintains saccadic accuracy.Methods: Within 2 weeks following mild CHI, 30 patients and 30 matched controls were compared on a computerized paradigm, which artificially induced saccadic adaptation. In response to an initial stimulus, subjects made a saccade during which the stimulus was displaced centripetally causing the initial (primary) saccade to be inaccurate. While these intra-saccadic changes remained unnoticed by the subjects, the displacements gradually caused adaptive saccadic hypometria.Results: No differences in adaptation were found between the CHI group and the controls (F(1, 29) = 0.51, p = 0.48). This finding indicates that mild CHI does not impair implicit reflexive saccade adaptation and suggests that cerebellar function and functions of deeper brain structures such as the thalamus, superior colliculus and the basal ganglia may be largely preserved following mild CHI. The current results support the notion that the profile of oculomotor function after mild CHI reflects a centripetal gradient of impairment and relates closely to the functional integrity of the injured brain.

How does action resist visual illusion? Uncorrected oculomotor information does not account for accurate pointing in peripersonal space

Using spatially identical displays (variants of the Müller-Lyer illusion), we compared the accuracy of spatial verbal judgments with that of saccadic (eye) and pointing (hand) movements. Verbal judgments showed a clear effect of the illusion. The amplitude of the primary saccade from one endpoint of the pattern (at fixation) to the other also showed an effect of the illusion. Conversely, movement amplitudes when pointing from one endpoint (initial finger position) to the other were significantly more accurate than both saccades and verbal responses. In a control experiment in which the viewing conditions between the saccade and pointing experiments were equalized, saccade amplitude was again affected by the illusion. In several studies, systematic biases in conscious spatial judgments have been contrasted with accurate open-loop pointing in peripersonal space. It has been proposed that such seeming dissociations between vision-for-action and vision-for-consciousness might in fact be because of a simple oculomotor strategy: saccade to the target before it disappears, then use the efference copy of the (accurate) saccadic movement to drive pointing. The present data do not support the hypothesis in this simple form.

Memory-guided saccades in Parkinson’s disease: long delays can improve performance

A recent study in control subjects suggested the existence of separate pathways for oculomotor spatial working memory tasks depending on whether the delay before movement execution is either short or long (>20 s). The long delay pathway might bypass brain areas commonly affected by Parkinson's disease (PD). This study aimed to assess spatial working memory in Parkinson's disease using short (3 s) and long (30 s) delays in a memory-guided saccade task. Fifteen mild-moderately affected PD subjects off-medication, and 15 age and sex-matched controls were tested (PD mean age 65.3; control 65.9). Subjects were tested in a darkened room using a horizontal LED bar to generate eye movements which were recorded using an infrared limbus tracker. Percentage error in amplitude of the primary saccade was analysed by repeated measures ANOVA. There was a significant interaction between the groups and their response to the short and long delay periods (P<0.02). PD subjects were more strongly impaired in the short delay than the long delay trials when compared with controls. Analysis of the percentage error in amplitude of the final eye position showed the same pattern but only in female subjects. This study provides the first evidence that the proposed parallel spatial memory pathway utilised in longer delay periods is relatively unimpaired in PD. In a broader sense, our results suggest there might be other alternative pathways to overcome deficits in functions impaired by PD.

The ability of the saccadic system to change motor plans in scanning letter strings.

Evidence from recent studies bolsters the idea of preestablished motor plans in scanning isolated items. Thus, refixation saccades are preplanned at the same time as the primary saccade directed to a peripheral item and are completed with fixed amplitudes irrespective of the first fixation position in the item. In order to examine the saccadic system's ability to correct the motor plan during its execution on the basis of new visual information, an experiment was conducted in which 11-letter strings were changed to two 5-letter strings at different times after the primary saccade was directed to the stimulus. The results demonstrate that the saccadic system is able to cancel the preplanned refixation saccade and plan a saccade directed to the next item only when the new visual information is available at least 220 msec before the execution of the saccade.

Shifts in the retinal image of a visual scene during saccades contribute to the perception of reached gaze direction in humans

We tested whether the perception of gaze direction is affected by the shifts in the retinal image of the visual scene during eye movements. To do so, we displaced the visual scene during saccadic eye movements and measured whether these unconsciously-detected shifts altered subjects’ perception of the reached gaze direction. While facing a visual environment composed of light-emitting diodes, subjects first performed a rightward saccade of a great amplitude before producing a leftward saccade towards a target that appeared in the environment. During the primary saccade, the visual environment could be shifted by 4.5° on either side. Subjects overestimated the target by 3.69° and underestimated it by 2.45° when the shift of the retinal image of the environment was greater and smaller than the extent of eye deviation, respectively. This suggests that the perception of gaze direction is largely based on the processing of retinal excitation both before and after the eye movements.

Contribution of signals downstream from adaptation to saccade programming.

Information about ongoing behavior is necessary for stable perception and subsequent motor planning. Although many recurrent networks are known in the motor systems, the pathways that transmit the signals for internal monitoring of behavior are not specified. The present study reports that the pathways originating from sites downstream of cerebellar adaptation provide internal signals that are used for subsequent eye-movement programming. When monkeys made two successive saccades toward the locations of previously flashed targets or initial fixation, the second saccade compensated for the adaptive changes in the primary saccade. The use of signals downstream from adaptation for saccade programming contrasts with recent findings that signals upstream from adaptation control the perceptual localization of visual stimuli presented around the time of saccade, suggesting that separate recurrent networks provide behavioral information for perception versus movement programming.

Foveal stimulation and saccadic latencies.

We investigated how a postsaccadic visual error affects the latency of the subsequent saccade. Observers made sequences of saccades directed to a single object or three separate objects, which could be displaced backward or onward during the primary saccade. The results showed an increase of second saccade latency after a backward displacement and a decrease of second saccade latency after an onward displacement. Moreover, second saccade latencies were particularly short after an onward displacement which resulted in a primary saccade landing position outside the boundary of the objects. We interpret the latency differences in terms of known effects within the saccadic system, specifically the sensitivity to the pattern of visual stimulation, particularly at and near the fovea, and the inverse correlation between secondary saccade amplitudes and secondary saccade latencies.

Neural control of on-line guidance of hand reaching movements

Orienting one's gaze towards a peripheral target is usually composed of a hypometric primary saccade followed by a secondary 'corrective saccade' triggered automatically (without conscious perception) by the retinal error at the end of the primary saccade and characterised by a short latency. Due to visual suppression during the saccade, the artificial introduction of a random small target jump during that short period remains undetected and triggers after the end of the primary saccade a normal 'corrective saccade'. As a result this procedure simulates an error in the planning of the primary saccade. On the other hand optimum hand pointing (trade-off between movement time and accuracy) is considered classically to involve a natural parallel initiation of saccade and hand response based on a poor peripheral retinal location, and a further amendment of the hand motor response based on the retinal error provided by the simultaneous vision of target and hand during the movement home phase. To test the hypothesis that the retinal feedback at the end of the primary saccade is used to update the visual target position and amend the ongoing hand motor response, we developed a paradigm involving both an optimum hand pointing and an undetected random target perturbation during the orienting saccade. In order to show that the amendments were controlled by a loop comparing the perceived target location with the dynamic hand position signal, vision of the limb was removed at movement onset. Results showed that the movement was smoothly monitored on-line without additional time processing demands. This functional property of flexibility of the ongoing hand motor response, was generalized from movement extent to movement direction. The undetectability of the perturbation at a conscious level was not a prerequisite for motor flexibility, which was further shown to depend on a critical phase of the limb movement beyond which the latter was no longer amendable, even when the limb was visible. The hand pointing flexibility was further generalised from pointing to the more complex hand reaching and grasping process. It was shown that the flexibility of both the transport and the grasp components were closely coupled. A careful analysis of the data suggested the controlled variable to be the general posture of the upper limb, reaching Bernstein's intuitions about redundancy reduction in skeletomotor systems with degrees of freedom in excess. A kinematics study of the motor flexibility of reaching and grasping in a patient with a bilateral optic ataxia favoured the idea of a posterior parietal cortex involvement in the error processing underlying motor flexibility, reaching the same conclusions as other recent studies using either Positron Emission Tomography or Transcranial Magnetic Stimulation.

Hypometric primary saccades and increased variability in visually-guided saccades in Huntington’s disease

Eye movement abnormalities can be distinctive and suggestive of a specific pathophysiology. To further investigate the deficits in the control of saccades in patients with Huntington’s disease (HD), we investigated the ability of 11 HD patients and 11 matched controls to perform visually-guided saccades. We adopted reflexive saccade tasks involving predictable and unpredictable sequences, at different amplitudes of target step (10°, 20°, 30°, 40°), as well as voluntary self-paced saccades. Prolongation of initiation was observed in the HD group as the target amplitude of predictable saccades increased. During the self-paced saccade task, the HD patients had increased intersaccadic intervals, performed fewer saccades in the allocated time and displayed an increased temporal variability in comparison to the controls. Furthermore, hypometric primary saccades, and an increased number of corrective saccades, were observed during both reflexive and voluntary saccades in the HD group. The delayed initiation of large saccades, deficits in voluntary, self-paced saccades, impaired saccadic accuracy and increased corrective saccades in HD, were interpreted in light of other ocular motor and limb studies, and appear to be due to damage to the fronto-striatal loop, including the supplementary eye fields, as well as possible brainstem and cerebellar involvement.

Differential effect of a distractor on primary saccades and perceptual localization

A distractor presented nearby the target of a goal-directed short latency saccade leads to spatial averaging, that is, the saccade lands between the target and the distractor. This so-called global effect is a characteristic feature of the spatial processing underlying the programming of saccadic eye movements. To determine whether this effect of near distractors on saccade metrics is also reflected in perceptual localization, subjects performed a saccade task and a perceptual localization task using identical, briefly flashed visual stimuli. To make the available visual processing time for saccades and perception more similar, we followed the target with a mask. Without the mask, primary saccades with short latency landed between target and distractor. The distractor had less effect on primary saccades with longer latencies (>200 ms) and did not affect the final eye position after late secondary saccades in the dark. This indicates that the oculomotor system can correctly use information about the target location 200 ms after the target flash even if no visual stimulus is present during this period. Likewise the presence of a distractor did not affect perceptual localization. Under the masking condition a similar global effect occurred for primary saccades with short latencies, but the latency dependence of the global effect was weakened. Secondary saccades and perceptual localization still did not show a global effect. The results suggest that the primary saccade is based on a specific target acquisition process that differs from that used for spatial perception and for the programming of memory-guided corrective saccades.

A turn-key transportable eye-tracking instrument for clinical assessment.

This paper describes a combined instrument (eye tracker and target generator, both head mounted, with integrated data analysis) that tests parameters of saccadic eye movement and fixation control to give insight into the status of functional brain systems. Using three minilasers, the target generato rprojects three visual stimuli, a fixation point and two lateral stimuli, with programmable timing. The controller allows the selection of overlap, 200-msec gap, or remembered saccade trials. Size, maximal velocity, and reaction time are determined for each primary saccade. The number of prosaccades and antisaccades are counted. More saccades--for example, the occurrence and latency of corrective saccades--may be evaluated off line by an interactive PC analysis program. The eye position data can be transferred to a PC. Off-line analysis compares each observed variable relative to an age-matched control group (300 healthy control subjects 7-70 years of age, tested in the overlap condition with prosaccade instructions and in the gap condition with antisaccades). The diagnostic results can be used to elaborate an individual optomotor training program.

The timing of sequences of saccades in visual search.

According to the LATER model (linear approach to thresholds with ergodic rate), the latency of a single saccade in response to target appearance can be understood as a decision process, which is subject to (i) variations in the rate of (visual) information processing; and (ii) the threshold for the decision. We tested whether the LATER model can also be applied to the sequences of saccades in a multiple fixation search, during which latencies of second and subsequent saccades are typically shorter than that of the initial saccade. We found that the distributions of the reciprocal latencies for later saccades, unlike those of the first saccade, are highly asymmetrical, much like a gamma distribution. This suggests that the normal distribution of the rate r, which the LATER model assumes, is not appropriate to describe the rate distributions of subsequent saccades in a scanning sequence. By contrast, the gamma distribution is also appropriate to describe the distribution of reciprocal latencies for the first saccade. The change of the gamma distribution parameters as a function of the ordinal number of the saccade suggests a lowering of the threshold for second and later saccades, as well as a reduction in the number of target elements analysed.

What is pathological with gaze shift fragmentation in Parkinson's disease?

Oculomotor dysfunction in Parkinson's disease (PD) is mainly characterized by a fragmentation of memory-guided gaze shifts (target is reached by several hypometric saccades). Since this phenomenon can also be observed in normal subjects, we scrutinized its pathophysiological significance in PD patients. We recorded horizontal eye movements in eleven mildly- or moderately-affected PD patients and eleven control subjects. A quantitative assessment of gaze shift fragmentation was made possible by increasing its incidence over a sequence of two visually- and two subsequent memory-guided gaze shifts. Basic saccade measures (latency, velocity, etc.) were similar in the two subject groups as well as in fragmented versus non-fragmented gaze shifts. Fragmentation probability is increased in the second memory-guided gaze shift, and this clearly more so in patients than in controls. The fragmentation shows a typical gain pattern (uniform increase of gain of saccadic amplitudes across correction saccades towards 1.0 with the last saccade of the gaze shift) independent of subject group, stimulus mode, and fragmentation degree. Gaze shift fragmentation represents a physiological phenomenon, which has thus far been overlooked. It reflects a robust correction mechanism, which assures that target is reached even if the pre-oculomotor drive through the basal ganglia to the superior colliculus becomes abnormally weak or under inadequately strong inhibition - as is postulated for PD. Thus, only the abnormally high incidence of fragmentation, and of the associated amplitude reduction of the primary saccades, rather than the phenomenon per se, can be used as a diagnostic criterion in early stages of PD.

Visual signals contribute to the coding of gaze direction.

Accurate information about gaze direction is required to direct the hand towards visual objects in the environment. In the present experiments, we tested whether retinal inputs affect the accuracy with which healthy subjects indicate their gaze direction with the unseen index finger after voluntary saccadic eye movements. In experiment 1, subjects produced a series of back and forth saccades (about eight) of self-selected magnitudes before positioning the eyes in a self-chosen direction to the right. The saccades were produced while facing one of four possible visual scenes: (1) complete darkness, (2) a scene composed of a single light-emitting diode (LED) located at 18 degrees to the right, (3) a visually enriched scene made up of three LEDs located at 0 degrees, 18 degrees and 36 degrees to the right, or (4) a normally illuminated scene where the lights in the experimental room were turned on. Subjects were then asked to indicate their gaze direction with their unseen index finger. In the conditions where the visual scenes were composed of LEDs, subjects were instructed to foveate or not foveate one of the LEDs with their last saccade. It was therefore possible to compare subjects' accuracy when pointing in the direction of their gaze in conditions with and without foveal stimulation. The results showed that the accuracy of the pointing movements decreased when subjects produced their saccades in a dark environment or in the presence of a single LED compared to when the saccades were generated in richer visual environments. Visual stimulation of the fovea did not increase subjects' accuracy when pointing in the direction of their gaze compared to conditions where there was only stimulation of the peripheral retina. Experiment 2 tested how the retinal signals could contribute to the coding of eye position after saccadic eye movements. More specifically, we tested whether the shift in the retinal image of the environment during the saccades provided information about the reached position of the eyes. Subjects produced their series of saccades while facing a visual environment made up of three LEDs. In some trials, the whole visual scene was displaced either 4.5 degrees to the left or 3 degrees to the right during the primary saccade. These displacements created mismatches between the shift of the retinal image of the environment and the extent of gaze deviation. The displacements of the visual scene were not perceived by the subjects because they occurred near the peak velocity of the saccade (saccadic suppression phenomenon). Pointing accuracy was not affected by the unperceived shifts of the visual scene. The results of these experiments suggest that the arm motor system receives more precise information about gaze direction when there is retinal stimulation than when there is none. They also suggest that the most relevant factor in defining gaze direction is not the retinal locus of the visual stimulation (that is peripheral or foveal) but rather the amount of visual information. Finally, the results suggest an enhanced egocentric encoding of gaze direction by the retinal inputs and do not support a retinotopic model for encoding gaze direction.

Selective and delay adaptation of human saccades

The consistently triggered step back of a target during primary saccades of a human subject induced a gradual change in gain, the ratio of the saccade amplitude to the target eccentricity. After a few hundred trials, subjects were able to foveate the displaced target in a single saccade. Presentation of a displaced target showed that human memory guided saccades have gain adaptation just like the well-established adaptation of visually guided saccades. Examining the transfer of adaptation between the memory guided saccade and two other types of visually guided saccades showed that each saccade transferred a 10–25% adapted gain change to the other saccades. However, any pair of the three saccades acquired different gains by adaptation in the same horizontal direction simultaneously, hence each saccade had adaptive capability independent of the others. Adaptation took place even when the appearance of a displaced target was delayed by 400–600 ms from the end of a primary saccade. These findings have important implications about the adaptation, particularly the location and temporal property of the adaptive mechanism in saccade generation.

Cerebellar lesions impair rapid saccade amplitude adaptation.

This study investigated whether the cerebellum is essential for rapid saccade adaptation. Saccade adaptation was elicited by 30% backward target steps during the primary saccade. Patients with cerebellar lesions adapted less than normal subjects, but saccade adaptation was most impaired in the group of patients with cerebellar degeneration. As the variability of the saccade gain in patients with cerebellar degeneration did not significantly differ from that in the other patients, the increased variability in motor performance due to a cerebellar lesion cannot alone explain this impaired adaptation.

サッカードの選択的適応のデータとモデル

Target step-back consistently induced during subject's primary saccades evoked gradual change in gain, the ratio of saccade amplitude to target eccentricity. After three hundred trials, the subjects caught a target by a single saccade. Such adaptation occurred with memory-guided saccade, as well as the adaptation of visually guided saccades as has been reported in the literature. These saccades showed selectivity in adaptation. Adaptation took place even when the displaced target appearance was delayed by 400-600 ms from the end of a primary saccade. Based on these findings we propose a selective adaptation model of human saccades which bears important implication for motor learning systems.

Saccadic hypometria in drug‐naïve and drug‐treated schizophrenic patients: A working memory deficit?

In certain conditions patients with schizophrenia make markedly smaller (hypometric) saccades than controls. This hypometria has been thought to reflect dopaminergic blockade as a result of antipsychotic medication. We tested this hypothesis by comparing the performance of an antipsychotic-naïve group and an antipsychotic-treated group of first-episode schizophrenic patients on a predictive saccade paradigm. We explored the possibility that hypometria reflects a spatial working memory deficit by correlating performance on neuropsychological tests of mnemonic function with saccadic accuracy. Both the drug-naïve and treated schizophrenic patients made hypometric saccades when compared with a group of matched controls. Primary saccade amplitude also correlated significantly with performance on some of the neuropsychological tests. These results are discussed in terms of the roles of cortical dopamine and working memory deficits in schizophrenic patients.