A competitive integration model of exogenous and endogenous eye movements

We present a model of the eye movement system in which the programming of an eye movement is the result of the competitive integration of information in the superior colliculi (SC). This brain area receives input from occipital cortex, the frontal eye fields, and the dorsolateral prefrontal cortex, on the basis of which it computes the location of the next saccadic target. Two critical assumptions in the model are that cortical inputs are not only excitatory, but can also inhibit saccades to specific locations, and that the SC continue to influence the trajectory of a saccade while it is being executed. With these assumptions, we account for many neurophysiological and behavioral findings from eye movement research. Interactions within the saccade map are shown to account for effects of distractors on saccadic reaction time (SRT) and saccade trajectory, including the global effect and oculomotor capture. In addition, the model accounts for express saccades, the gap effect, saccadic reaction times for antisaccades, and recorded responses from neurons in the SC and frontal eye fields in these tasks.     

Human fast negative EEG potentials before express saccades

Fast negative EEG potentials preceding fast regular saccades and express saccades were studied by the method of backward averaging under conditions of monocular stimulation of the right and left eye. "Step" and "gap" experimental paradigms were used for visual stimulation. Analysis of parameters of potentials and their spatiotemporal dynamics suggests that, under conditions of the increased attention and optimal readiness of the neural structures, express saccades appear when the previously chosen program of the future eye movement coincides with the actual target coordinates. We assumed that the saccade latency decreases at the expense of the involvement of the main oculomotor areas of motor and saccadic planning in its initiation; an express saccade can be initiated also by means of direct transmission of the signal from the cortex to the brainstem saccadic generator passing by the superior colliculus. Moreover, anticipating release from the central fixation and attention distraction are necessary for the successful initiation of an express saccade.     

Saccades during Attempted Fixation in Parkinsonian Disorders and Recessive Ataxia: From Microsaccades to Square-Wave Jerks

During attempted visual fixation, saccades of a range of sizes occur. These “fixational saccades” include microsaccades, which are not apparent in regular clinical tests, and “saccadic intrusions”, predominantly horizontal saccades that interrupt accurate fixation. Square-wave jerks (SWJs), the most common type of saccadic intrusion, consist of an initial saccade away from the target followed, after a short delay, by a “return saccade” that brings the eye back onto target. SWJs are present in most human subjects, but are prominent by their increased frequency and size in certain parkinsonian disorders and in recessive, hereditary spinocerebellar ataxias. Here we asked whether fixational saccades showed distinctive features in various parkinsonian disorders and in recessive ataxia. Although some saccadic properties differed between patient groups, in all conditions larger saccades were more likely to form SWJs, and the intervals between the first and second saccade of SWJs were similar. These findings support the proposal of a common oculomotor mechanism that generates all fixational saccades, including microsaccades and SWJs. The same mechanism also explains how the return saccade in SWJs is triggered by the position error that occurs when the first saccadic component is large, both in the healthy brain and in neurological disease.     

Looking for Discriminating Is Different from Looking for Looking’s Sake

Recent studies provide evidence for task-specific influences on saccadic eye movements. For instance, saccades exhibit higher peak velocity when the task requires coordinating eye and hand movements. The current study shows that the need to process task-relevant visual information at the saccade endpoint can be, in itself, sufficient to cause such effects. In this study, participants performed a visual discrimination task which required a saccade for successful completion. We compared the characteristics of these task-related saccades to those of classical target-elicited saccades, which required participants to fixate a visual target without performing a discrimination task. The results show that task-related saccades are faster and initiated earlier than target-elicited saccades. Differences between both saccade types are also noted in their saccade reaction time distributions and their main sequences, i.e., the relationship between saccade velocity, duration, and amplitude.     

Craniotopic updating of visual space across saccades in the human posterior parietal cortex

The neural mechanisms underlying the craniotopic updating of visual space across saccadic eye movements are poorly understood. Previous single-unit recording studies in primates and clinical studies in brain-damaged patients have shown that the posterior parietal cortex (PPC) has a key role in this process. In the present study, we used single-pulse transcranial magnetic stimulation (TMS) to disrupt the processing within the PPC during a task that requires craniotopic updating: double saccades. In this task, two targets are presented in quick succession and the subject is required to make a saccade to each location as accurately as possible. We show here that TMS delivered to the PPC just prior to the second saccade effectively disrupts the craniotopic coding normally observed in this task. This causes subjects to revert to saccades more consistent with a representation of the targets based on their positions relative to one another. By contrast, stimulation at earlier times between the two saccades did not disrupt performance. These results suggest that extraretinal information generated during the first perisaccadic period is not put into functional use until just prior to the second saccade.     

A minicomputer program for automatic saccade detection and linear analysis of eye movement systems using sine wave stimulus

A FORTRAN IV program is described, which may be run interactively or in batch and which allows a user to obtain the frequency response amplitude ratio and phase resulting from the linear analysis of an eye movement system using sine wave stimuli. The response (eye position) signal may contain components contributed by the saccadic eye movements. The program can digitize analog signals and store data on a magnetic tape. With the aid of digital filters, the program can detect saccades without requiring any input parameters from the user. The program interpolates the saccade interval using a method of least square curve fitting with a sine wave. The interpolation is relatively noise immune and works well regardless of the stimulus frequencies and the width of a saccade interval. Moreover, the program can handle long duration of signals such as 90 min of data which covers about 5 cycles of a 0.001 Hz sine wave signal. Sample runs for the cases of 0.001 and 0.1 Hz are given. The resident driver and the overlayable segments of the program have been implemented on a DEC (Digital Equipment Corp.) LAB-11 minicomputer (PDP 11/20).     

The saccadic and neurological deficits in type 3 Gaucher disease

Our objective was to characterize the saccadic eye movements in patients with type 3 Gaucher disease (chronic neuronopathic) in relationship to neurological and neurophysiological abnormalities. For approximately 4 years, we prospectively followed a cohort of 15 patients with Gaucher type 3, ages 8-28 years, by measuring saccadic eye movements using the scleral search coil method. We found that patients with type 3 Gaucher disease had a significantly higher regression slope of duration vs amplitude and peak duration vs amplitude compared to healthy controls for both horizontal and vertical saccades. Saccadic latency was significantly increased for horizontal saccades only. Downward saccades were more affected than upward saccades. Saccade abnormalities increased over time in some patients reflecting the slowly progressive nature of the disease. Phase plane plots showed individually characteristic patterns of abnormal saccade trajectories. Oculo-manual dexterity scores on the Purdue Pegboard test were low in virtually all patients, even in those with normal cognitive function. Vertical saccade peak duration vs amplitude slope significantly correlated with IQ and with the performance on the Purdue Pegboard but not with the brainstem and somatosensory evoked potentials. We conclude that, in patients with Gaucher disease type 3, saccadic eye movements and oculo-manual dexterity are representative neurological functions for longitudinal studies and can probably be used as endpoints for therapeutic clinical trials. TRIAL REGISTRATION: ClinicalTrials.gov NCT00001289.     

The three-loop model: a neural network for the generation of saccadic reaction times

This paper presents a computer simulation of the three-loop model for the temporal aspects of the generation of visually guided saccadic eye movements. The intention is to reproduce complex experimental reaction time distributions by a simple neural network. The operating elements are artificial but realistic neurones. Four modules are constructed, each consisting of 16 neural elements. Within each module, the elements are connected in an all-to-all manner. The modules are working parallel and serial according to the anatomically and physiologically identified visuomotor pathways including the superior colliculus, the frontal eye fields, and the parietal cortex. Two transient-sustained input lines drive the network: one represents the visual activity produced by the onset of the saccade target, the other represents a central activity controlling the preparation of saccades, e.g. the end of active fixation. The model works completely deterministically; its stochastic output is a consequence of the stochastic properties of the input only. Simulations show how multimodal distributions of saccadic reaction times are produced as a natural consequence of the model structure. The gap effect on saccadic reaction times is correctly produced by the model: depending only on the gap duration (all model parameters unchanged) express, fast-regular, and slow-regular saccades are obtained in different numbers. In agreement with the experiments, bi- or trimodal distributions are produced only for medium gap durations (around 200 ms), while for shorter or longer gaps the express mode disappears and the distributions turn bi- or even unimodal. The effect of varying the strength of the transient-sustained components and the ongoing activity driving the hierarchically highest module are considered to account for the interindividual variability of the latency distributions obtained from different subjects, effects of different instructions to the same subject, and the observation of express makers (subjects who produce exclusively express saccades). How the model can be extended to describe the spatial aspects of the saccade system will be discussed as well as the effects of training and/or rapid adaptation to experimental conditions.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Binocular coupling in chameleon saccade generation

Chameleons are capable of making a saccade with one eye while the other does not move. This virtually unique feature poses questions regarding the organization of the saccadic system of the chameleon. By comparing real data with a simulated test signal, we studied whether the saccade generation of the left and right eye can be considered as truly independent. This appeared not to be the case, since there was an increased likelihood to start saccades in close temporal proximity in the two eyes. However, the coupling does not reflect a common saccadic motor signal for both eyes, since even saccades that were made in close temporal proximity did not have correlated metrics. Received: 21 April 1997 / Accepted in revised form: 15 September 1997     

Effect of dopamine deficiency on the preparation of visually guided saccadic eye movements

Parameters of saccadic eye movements were studied in patients with Parkinson's disease and control subjects. In parkinsonian patients, the number of slow regular saccades was shown to be increased, and the number of express saccades was shown to be decreased. As a result the mean of saccade latency in patients was longer than in the control group. Moreover, the percentage of multistep saccades in patients with Parkinson's disease. In this case, not one but two or three saccades were performed with smaller amplitude to the target. We point, that the multistep saccades occurred mainly among the express saccades. Obviously, the dopamine deficiency distinguishing parkinsonian patients takes the primary part in the development of saccadic disorders. Degeneration of the nigrostriatal dopamine pathway results in imbalance in activity of the direct and indirect output pathways of the striatum. We suppose that this leads to inhibition of neurons activity in the superior colliculus during the saccade performance, which results in the early saccade interruption. In support of this reasoning, the mean of saccade latency and the percentage of the multistep saccades decreased in patients with Parkinson's disease after dopamine D2/D3 agonist (piribedil) treatment, due to activity restoration of the indirect pathway.     

Saccadic eye movements and the detection of fast-moving gratings

Experiments are presented in which the effect of saccadic eye movements on the visibility of sinusoidal gratings drifting with velocities between 2 deg/s and 400 deg/s is investigated. The results demonstrate that saccades are highly useful for detecting this class of stimuli. Due to a saccade, otherwise subthreshold stimuli become visible as short, distinct flashes of the seemingly statinoary pattern. The paper analyzes in detail the dependence of the amount of facilitation on saccade size and relative direction and isolates the additional effect of saccadic suppression. A simple model is proposed which predicts the experimental findings.     

Saccadic Momentum and Facilitation of Return Saccades Contribute to an Optimal Foraging Strategy

The interest in saccadic IOR is funneled by the hypothesis that it serves a clear functional purpose in the selection of fixation points: the facilitation of foraging. In this study, we arrive at a different interpretation of saccadic IOR. First, we find that return saccades are performed much more often than expected from the statistical properties of saccades and saccade pairs. Second, we find that fixation durations before a saccade are modulated by the relative angle of the saccade, but return saccades show no sign of an additional temporal inhibition. Thus, we do not find temporal saccadic inhibition of return. Interestingly, we find that return locations are more salient, according to empirically measured saliency (locations that are fixated by many observers) as well as stimulus dependent saliency (defined by image features), than regular fixation locations. These results and the finding that return saccades increase the match of individual trajectories with a grand total priority map evidences the return saccades being part of a fixation selection strategy that trades off exploration and exploitation.     

A Mathematical Model of Optimal Saccadic Eye Movement by a Pair of Muscles

This paper presents a model of saccadic eye movements. Eye movements are considered as being ballistic, since saccades (rapid concurrent movements of both eyes) occur several hundred thousand times per day; visual perception of the environment is interrupted by a saccade. The optimal control was constructed for the motion considered in three consecutively refined assumptions. The controls included in the time-optimal problem were the resultant moment of force exerted by the extraocular muscles, individual moments of force exerted by either muscle of the agonist–antagonist pair, and finally, the rate of change of these moments. This approach is consistent with the view that is currently upheld by physiologists, who believe that a saccade is programmed by the central nervous system before the beginning of an eye movement and is scarcely adjusted during the movement itself. The solution of the optimal control problem and the results obtained by subsequent numerical modeling of saccadic trajectories were compared with the published experimental data. The saccadic trajectories were compared based on the main sequence, the known consistent relationship between saccade amplitude and duration, which is the most widely applied and commonly accepted way of describing saccade data. The main sequence of saccades obtained from the solution of the optimal control problem formulated in the most complete form agreed well with published experimental results.     

Probability of Seeing Increases Saccadic Readiness

Associating movement directions or endpoints with monetary rewards or costs influences movement parameters in humans, and associating movement directions or endpoints with food reward influences movement parameters in non-human primates. Rewarded movements are facilitated relative to non-rewarded movements. The present study examined to what extent successful foveation facilitated saccadic eye movement behavior, with the hypothesis that foveation may constitute an informational reward. Human adults performed saccades to peripheral targets that either remained visible after saccade completion or were extinguished, preventing visual feedback. Saccades to targets that were systematically extinguished were slower and easier to inhibit than saccades to targets that afforded successful foveation, and this effect was modulated by the probability of successful foveation. These results suggest that successful foveation facilitates behavior, and that obtaining the expected sensory consequences of a saccadic eye movement may serve as a reward for the oculomotor system.     

Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.     

Both Lexical and Non-Lexical Characters Are Processed during Saccadic Eye Movements

On average our eyes make 3–5 saccadic movements per second when we read, although their neural mechanism is still unclear. It is generally thought that saccades help redirect the retinal fovea to specific characters and words but that actual discrimination of information only occurs during periods of fixation. Indeed, it has been proposed that there is active and selective suppression of information processing during saccades to avoid experience of blurring due to the high-speed movement. Here, using a paradigm where a string of either lexical (Chinese) or non-lexical (alphabetic) characters are triggered by saccadic eye movements, we show that subjects can discriminate both while making saccadic eye movement. Moreover, discrimination accuracy is significantly better for characters scanned during the saccadic movement to a fixation point than those not scanned beyond it. Our results showed that character information can be processed during the saccade, therefore saccades during reading not only function to redirect the fovea to fixate the next character or word but allow pre-processing of information from the ones adjacent to the fixation locations to help target the next most salient one. In this way saccades can not only promote continuity in reading words but also actively facilitate reading comprehension.     

The effect of illumination on involuntary eye saccades]

A study was made of the influence of sudden illumination micromovements of the eyes. Sudden contour illumination of the eye by a 15 degrees field with a crossing in the centre and a brightness of 100 nit reduced the amplitude of involuntary saccades and their frequency. The effect was particularly distinct with preliminary recording of the eye micromovement in complete darkness without a fixation point. In the case of fixation of a stationary point with one eye and of illumination of the other, the effect was also manifest, but it was less pronounced. During illumination of the eye with diffused light (through spectacles with frosted glasses) the effect of diminution of the saccade amplitude was smaller, though the brightness remained unchanged. A decrease in the saccade amplitude was practically not observed when the point was fixed at diffuse illumination. It has also been shown that with greater brightness of the fixation point (0.3; 25; 92 and 1000 nit), the amplitude and frequency of involuntary saccades diminish. The results attest that in choosing the conditions of work of the saccadic system two factors should be taken into consideration: the presence of the contours of the visible object and its brightness, the latter by itself having a lesser effect than the former.     

Dysfunctional mode switching between fixation and saccades: collaborative insights into two unusual clinical disorders

Voluntary rapid eye movements (saccades) redirect the fovea toward objects of visual interest. The saccadic system can be considered as a dual-mode system: in one mode the eye is fixating, in the other it is making a saccade. In this review, we consider two examples of dysfunctional saccades, interrupted saccades in late-onset Tay-Sachs disease and gaze-position dependent opsoclonus after concussion, which fail to properly shift between fixation and saccade modes. Insights and benefits gained from bi-directional collaborative exchange between clinical and basic scientists are emphasized. In the case of interrupted saccades, existing mathematical models were sufficiently detailed to provide support for the cause of interrupted saccades. In the case of gaze-position dependent opsoclonus, existing models could not explain the behavior, but further development provided a reasonable hypothesis for the mechanism underlying the behavior. Collaboration between clinical and basic science is a rich source of progress for developing biologically plausible models and understanding neurological disease. Approaching a clinical problem with a specific hypothesis (model) in mind often prompts new experimental tests and provides insights into basic mechanisms.

     

The Fixation and Saccade P3

Although most instances of object recognition during natural viewing occur in the presence of saccades, the neural correlates of objection recognition have almost exclusively been examined during fixation. Recent studies have indicated that there are post-saccadic modulations of neural activity immediately following eye movement landing; however, whether post-saccadic modulations affect relatively late occurring cognitive components such as the P3 has not been explored. The P3 as conventionally measured at fixation is commonly used in brain computer interfaces, hence characterizing the post-saccadic P3 could aid in the development of improved brain computer interfaces that allow for eye movements. In this study, the P3 observed after saccadic landing was compared to the P3 measured at fixation. No significant differences in P3 start time, temporal persistence, or amplitude were found between fixation and saccade trials. Importantly, sensory neural responses canceled in the target minus distracter comparisons used to identify the P3. Our results indicate that relatively late occurring cognitive neural components such as the P3 are likely less sensitive to post saccadic modulations than sensory neural components and other neural activity occurring shortly after eye movement landing. Furthermore, due to the similarity of the fixation and saccade P3, we conclude that the P3 following saccadic landing could possibly be used as a viable signal in brain computer interfaces allowing for eye movements.