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.     

Distractor Evoked Deviations of Saccade Trajectory Are Modulated by Fixation Activity in the Superior Colliculus: Computational and Behavioral Evidence

Previous studies have shown that saccades may deviate towards or away from task irrelevant visual distractors. This observation has been attributed to active suppression (inhibition) of the distractor location unfolding over time: early in time inhibition at the distractor location is incomplete causing deviation towards the distractor, while later in time when inhibition is complete the eyes deviate away from the distractor. In a recent computational study, Wang, Kruijne and Theeuwes proposed an alternative theory that the lateral interactions in the superior colliculus (SC), which are characterized by short-distance excitation and long-distance inhibition, are sufficient for generating both deviations towards and away from distractors. In the present study, we performed a meta-analysis of the literature, ran model simulations and conducted two behavioral experiments to further explore this unconventional theory. Confirming predictions generated by the model simulations, the behavioral experiments show that a) saccades deviate towards close distractors and away from remote distractors, and b) the amount of deviation depends on the strength of fixation activity in the SC, which can be manipulated by turning off the fixation stimulus before or after target onset (Experiment 1), or by varying the eccentricity of the target and distractor (Experiment 2).     

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.     

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.     

Mechanisms of neural integration in the parietal lobe for visual attention.

The impulse discharges of neurons in the inferior parietal association cortex (area 7) were studied in the alert, behaving rhesus monkey, trained to fixate and follow visual targets. Four classes of cells related to visual or visuomotor function were found. Cells of one of these are sensitive to visual stimuli and have large, contralateral receptive fields with maximal sensitivity in the far temporal quadrants. Cells of the other three classes are related to visuomotor functions: visual fixation, tracking, and saccades. They are neither sensory nor motor in the usual sense for they are activated only by interested fixation of gaze or tracking, or before visually evoked saccadic eye movements. They are not activated during the spontaneous saccades and fixations that the monkey makes while casually exploring his environment. It is hypothesized that the light-sensitive neurons provide the visual input to the visuomotor cells that, in turn, produce a command signal for the direction of visual attention and for shifting the focus of attention from one target to another.     

Stimulus sequence effects on human express saccades described by a Markov model

Express saccades predominantly occur in experiments employing the gap paradigm where the target onset is separated from the fixation point offset by a blank period. Their relative frequency is distinctly influenced by catch trials (i.e. trials without a saccadic target) mixed into the stream of regular target trials. Generalizing this concept for other stimulus uncertainties (direction, amplitude), we found that the preparation time of a saccade depends on both the type of uncertainty used and the sequence of trial type (e.g., target vs catch, left vs right) in the experiment. This stimulus sequence effect is most prominent for catch trials. A similar but less pronounced effect can still be observed in the case of direction uncertainty but not in that of amplitude uncertainty. A two-state Markov process model is proposed which is based on the dichotomy of express and regular saccades in the gap paradigm. According to this model the actual state of the saccadic system, which determines the type of saccade just in preparation, depends on the "trial history". The implications for models of saccade programming are discussed. Received: 14 April 1993/Accepted in revised form: 2 July 1993     

Causal Inference for Spatial Constancy across Saccades

Our ability to interact with the environment hinges on creating a stable visual world despite the continuous changes in retinal input. To achieve visual stability, the brain must distinguish the retinal image shifts caused by eye movements and shifts due to movements of the visual scene. This process appears not to be flawless: during saccades, we often fail to detect whether visual objects remain stable or move, which is called saccadic suppression of displacement (SSD). How does the brain evaluate the memorized information of the presaccadic scene and the actual visual feedback of the postsaccadic visual scene in the computations for visual stability? Using a SSD task, we test how participants localize the presaccadic position of the fixation target, the saccade target or a peripheral non-foveated target that was displaced parallel or orthogonal during a horizontal saccade, and subsequently viewed for three different durations. Results showed different localization errors of the three targets, depending on the viewing time of the postsaccadic stimulus and its spatial separation from the presaccadic location. We modeled the data through a Bayesian causal inference mechanism, in which at the trial level an optimal mixing of two possible strategies, integration vs. separation of the presaccadic memory and the postsaccadic sensory signals, is applied. Fits of this model generally outperformed other plausible decision strategies for producing SSD. Our findings suggest that humans exploit a Bayesian inference process with two causal structures to mediate visual stability.     

Slow Cortical Potentials Preceeding Visually Guided Saccades in Schizophrenics

The parameters of saccades and presaccadic slow potentials were studied in right-handed men with a dominant right eye, including 19 schizophrenics and 12 healthy subjects. For visual stimulation, three light-emitting diodes were used, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli). Two stimulation protocols were used: with a simultaneous switching off of the central fixation stimulus and switching on of the peripheral stimuli (test 1) and with an interstimulus gap of 200 ms (test 2). According to the latency, saccades were divided into anticipatory, express, and regular. Slow EEG potentials preceding regular saccades were analyzed. It was found that the proportion of anticipatory saccades is considerably higher than the normal value in schizophrenia. The analysis of the presaccadic potentials demonstrated a significant decrease in the amplitude of negative potentials in the vertex region at early stages of presaccadic preparation and its increase in the occipital region at late stages. Test 2 in the patients demonstrated an increase in the positivity focus in the frontal region of the right hemisphere. It was assumed that the alterations found in schizophrenia result from the deficit of frontal cortical fields.     

Saccadic motor planning by integrating visual information and pre-information on neural dynamic fields

A functional model of target selection in the saccadic system is presented, incorporating elements of visual processing, motor planning, and motor control. We address the integration of visual information with pre-information. which is provided by manipulating the probability that a target appears at a certain location. This integration is achieved within a dynamic representation of planned eye movement which is modeled through distributions of activation on a topographic field. Visual input evokes activation, which is also constrained by lateral interaction within the field and by preshaping input representing pre-information. The model describes target selection observable in paradigms in which visual goals are presented at more than one location. Specifically, we model the transition from averaging, where endpoints of first saccades fall between two visual target locations, to decision making, where endpoints of first saccades fall accurately onto one of two simultaneously presented visual targets. We make predictions about how metrical biases of first saccades are induced by pre-information about target locations acquired by learning. When coupled to a motor control stage, activation dynamics on the planning level contribute to stabilizing gaze under fixation conditions. The neurophysiological relevance of our functional model is discussed.     

A model of the saccade-generating system that accounts for trajectory variations produced by competing visual stimuli

Variable saccade trajectories are produced in visual search paradigms in which multiple potential target stimuli are present. These variable trajectories provide a rich source of information that may lead to a deeper understanding of the basic control mechanisms of the saccadic system. We have used published behavioral observations and neural recordings in the superior colliculus (SC), gathered in monkeys performing visual search paradigms, to guide the construction of a new distributed model of the saccadic system. The new model can account for many of the variations in saccade trajectory produced by the appearance of multiple visual stimuli in a search paradigm. The model uses distributed feedback about current eye motion from the brainstem to the SC to reduce activity there at physiologically realistic rates during saccades. The long-range lateral inhibitory connections between SC cells used in previous models have been eliminated to match recent physiological evidence. The model features interactions between visually activated multiple populations of cells in the SC and distributed and topologically organized inhibitory input to the SC from the SNr to produce some of the types of variable saccadic trajectories, including slightly curved and averaging saccades, observed in visual search tasks. The distributed perisaccadic disinhibition of SC from the substantia nigra (SNr) is assumed to have broad spatial tuning. In order to produce the strongly curved saccades occasionally recorded in visual search, the existence of a parallel input to the saccadic burst generators in addition to that provided by the distributed input from the SC is required. The spatiotemporal form of this additional parallel input is computed based on the assumption that the input from the model SC is realistic. In accordance with other recent models, it is assumed that the parallel input comes from the cerebellum, but our model predicts that the parallel input is delayed during highly curved saccadic trajectories.     

Parallel and serial processes in the human oculomotor system: bimodal integration and express saccades

Saccadic reaction times (SRTs) were analyzed in the context of stochastic models of information processing (e.g., Townsend and Ashby 1983) to reveal the processing architecture(s) underlying integrative interactions between visual and auditory inputs and the mechanisms of express saccades. The results support the following conclusions. Bimodal (visual + auditory) targets are processed in parallel, and facilitate SRT to an extent that exceeds levels attainable by probability summation. This strongly implies neural summation between elements responding to spatially aligned visual and auditory inputs in the human oculomotor system. Second, express saccades are produced within a separable processing stage that is organized in series with that responsible for intersensory integration. A model is developed that implements this combination of parallel and serial processing. The activity in parallel input channels is summed within a sensory stage which is organized in series with a pre-motor and motor stage. The time course of each subprocess is considered a random variable, and different experimental manipulations can selectively influence different stages. Parallels between the model and physiological data are explored.     

Latency of visually evoked saccadic eye movements

The validness of a model describing the relation between mean saccadic latency and stimulus asynchrony based on facilitation instead of suppression was tested experimentally. As a result, suppression of signals generated by the onset of a peripheral stimulus due to fixation of another target, giving rise to an increase of mean saccadic latency, does not seem very likely. The influence of the intensity of the fixation target on the latency of visually evoked saccades was studied. According to the facilitation model, the offset of the fixation target induces after an afferent delay, a transition of the state of the facilitation mechanism from the unfacilitated condition into a mode of maximal facilitation. The time-period during which this change is accomplished is called Facilitation-Rise-Time (FRT). An interpretation within the context of the facilitation model of gap-overlap latency data for different values of the intensity of the fixation stimulus suggests, in combination with computer-computations of the model, that lowering of this intensity causes an increase in FRT. The results in normal subjects of step stimulus experiments with a dim fixation point substantiate the hypothesis of a facilitation mechanism, which is triggerable not only by an external signal such as the offset of the fixation point, but also by some internal stimulus independent signal. Moreover, data for tracking by an amblyopic eye seem to support this conclusion. The findings of increased saccadic latencies in amblyopic and Optic Neuritis (ON) eyes suggest a slowing of processing of visual information in the sensory pathways from the central retina, subsequently utilized by the oculomotor system in the generation of saccades.(ABSTRACT TRUNCATED AT 250 WORDS)     

Manipulating intent: evidence for a causal role of the superior colliculus in target selection

The superior colliculus (SC) is well known for its role in the motor control of saccades. Recent work has shown that it also plays a role in the selection of saccades, but a causal role in the process of target selection has not been demonstrated. We applied subthreshold microstimulation to the SC while monkeys performed a task requiring them to select a stimulus as the target for a pursuit or saccade movement. Stimulation increased the proportion of selections toward the stimulus that appeared contralateral to the site of stimulation and also decreased their latencies. For pursuit, this stimulation-induced contralateral response bias was with respect to the initial target location and not the direction of eye movement, demonstrating a causal effect on target choice distinct from any effect on motor preparation. These results show that the SC helps decide the object of the next movement, beyond its traditional responsibility of saccade production.     

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.     

High-Field fMRI Reveals Brain Activation Patterns Underlying Saccade Execution in the Human Superior Colliculus

Background

The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans.

Methodology/Principal Findings

The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar.

Conclusions/Significance

Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned.     

Neural network simulations of the primate oculomotor system III. An one-dimensional, one-directional model of the superior colliculus

This report evaluates the performance of a biologically motivated neural network model of the primate superior colliculus (SC). Consistent with known anatomy and physiology, its major features include excitatory connections between its output elements, nigral gating mechanisms, and an eye displacement feedback of reticular origin to recalculate the metrics of saccades to memorized targets in retinotopic coordinates. Despite the fact that it makes no use of eye position or eye velocity information, the model can account for the accuracy of saccades in double step stimulation experiments. Further, the model accounts for the effects of focal SC lesions. Finally, it accounts for the properties of saccades evoked in response to the electrical stimulation of the SC. These include the approximate size constancy of evoked saccades despite increases of stimulus intensity, the fact that the size of evoked saccades depends on the time that has elapsed from a previous saccade, the fact that staircases of saccades are evoked in response to prolonged stimuli, and the fact that the size of saccades evoked in response to the simultaneous stimulation of two SC sites is the average of the saccades that are evoked when the two sites are separately stimulated. Received: 3 November 1997 / Accepted in revised form: 30 June 1998     

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.     

Human visual search does not maximize the post-saccadic probability of identifying targets

Researchers have conjectured that eye movements during visual search are selected to minimize the number of saccades. The optimal Bayesian eye movement strategy minimizing saccades does not simply direct the eye to whichever location is judged most likely to contain the target but makes use of the entire retina as an information gathering device during each fixation. Here we show that human observers do not minimize the expected number of saccades in planning saccades in a simple visual search task composed of three tokens. In this task, the optimal eye movement strategy varied, depending on the spacing between tokens (in the first experiment) or the size of tokens (in the second experiment), and changed abruptly once the separation or size surpassed a critical value. None of our observers changed strategy as a function of separation or size. Human performance fell far short of ideal, both qualitatively and quantitatively.     

Dyslexic children are confronted with unstable binocular fixation while reading

Reading requires three-dimensional motor control: saccades bring the eyes from left to right, fixating word after word; and oblique saccades bring the eyes to the next line of the text. The angle of vergence of the two optic axes should be adjusted to the depth of the book or screen and--most importantly--should be maintained in a sustained manner during saccades and fixations. Maintenance of vergence is important as it is a prerequisite for a single clear image of each word to be projected onto the fovea of the eyes. Deficits in the binocular control of saccades and of vergence in dyslexics have been reported previously but only for tasks using single targets. This study examines saccades and vergence control during real text reading. Thirteen dyslexic and seven non-dyslexic children read the French text "L'Allouette" in two viewing distances (40 cm vs. 100 cm), while binocular eye movements were measured with the Chronos Eye-tracking system. We found that the binocular yoking of reading saccades was poor in dyslexic children (relative to non-dyslexics) resulting in vergence errors; their disconjugate drift during fixations was not correlated with the disconjugacy during their saccades, causing considerable variability of vergence angle from fixation to fixation. Due to such poor oculomotor adjustments during reading, the overall fixation disparity was larger for dyslexic children, putting larger demand on their sensory fusion processes. Moreover, for dyslexics the standard deviation of fixation disparity was larger particularly when reading at near distance. We conclude that besides documented phoneme processing disorders, visual/ocular motor imperfections may exist in dyslexics that lead to fixation instability and thus, to instability of the letters or words during reading; such instability may perturb fusional processes and might--in part--complicate letter/word identification.     

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.