Saccade generation by the frontal eye fields in rhesus monkeys is separable from visual detection and bottom-up attention shift

The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.     

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.     

Enhanced tactile performance at the destination of an upcoming saccade

Previous work has demonstrated that upcoming saccades influence visual and auditory performance even for stimuli presented before the saccade is executed. These studies suggest a close relationship between saccade generation and visual/auditory attention. Furthermore, they provide support for Rizzolatti et al.'s premotor model of attention, which suggests that the same circuits involved in motor programming are also responsible for shifts in covert orienting (shifting attention without moving the eyes or changing posture). In a series of experiments, we demonstrate that saccade programming also affects tactile perception. Participants made speeded saccades to the left and right side as well as tactile discriminations of up versus down. The first experiment demonstrates that participants were reliably faster at responding to tactile stimuli near the location of upcoming saccades. In our second experiment, we had the subjects cross their hands and demonstrated that the effect occurs in visual space (rather than the early representations of touch). In our third experiment, the tactile events usually occurred on the opposite side of upcoming eye movement. We found that the benefit at the saccade target location vanished, suggesting that this shift is not obligatory but that it may be vetoed on the basis of expectation.     

Optimal control of saccades by spatial-temporal activity patterns in the monkey superior colliculus

A major challenge in computational neurobiology is to understand how populations of noisy, broadly-tuned neurons produce accurate goal-directed actions such as saccades. Saccades are high-velocity eye movements that have stereotyped, nonlinear kinematics; their duration increases with amplitude, while peak eye-velocity saturates for large saccades. Recent theories suggest that these characteristics reflect a deliberate strategy that optimizes a speed-accuracy tradeoff in the presence of signal-dependent noise in the neural control signals. Here we argue that the midbrain superior colliculus (SC), a key sensorimotor interface that contains a topographically-organized map of saccade vectors, is in an ideal position to implement such an optimization principle. Most models attribute the nonlinear saccade kinematics to saturation in the brainstem pulse generator downstream from the SC. However, there is little data to support this assumption. We now present new neurophysiological evidence for an alternative scheme, which proposes that these properties reside in the spatial-temporal dynamics of SC activity. As predicted by this scheme, we found a remarkably systematic organization in the burst properties of saccade-related neurons along the rostral-to-caudal (i.e., amplitude-coding) dimension of the SC motor map: peak firing-rates systematically decrease for cells encoding larger saccades, while burst durations and skewness increase, suggesting that this spatial gradient underlies the increase in duration and skewness of the eye velocity profiles with amplitude. We also show that all neurons in the recruited population synchronize their burst profiles, indicating that the burst-timing of each cell is determined by the planned saccade vector in which it participates, rather than by its anatomical location. Together with the observation that saccade-related SC cells indeed show signal-dependent noise, this precisely tuned organization of SC burst activity strongly supports the notion of an optimal motor-control principle embedded in the SC motor map as it fully accounts for the straight trajectories and kinematic nonlinearity of saccades.     

Is Mislocalization during Saccades Related to the Position of the Saccade Target within the Image or to the Gaze Position at the End of the Saccade?

A stimulus that is flashed around the time of a saccade tends to be mislocalized in the direction of the saccade target. Our question is whether the mislocalization is related to the position of the saccade target within the image or to the gaze position at the end of the saccade. We separated the two with a visual illusion that influences the perceived distance to the target of the saccade and thus saccade endpoint without affecting the perceived position of the saccade target within the image. We asked participants to make horizontal saccades from the left to the right end of the shaft of a Müller-Lyer figure. Around the time of the saccade, we flashed a bar at one of five possible positions and asked participants to indicate its location by touching the screen. As expected, participants made shorter saccades along the fins-in (<–>) configuration than along the fins-out (>–<) configuration of the figure. The illusion also influenced the mislocalization pattern during saccades, with flashes presented with the fins-out configuration being perceived beyond flashes presented with the fins-in configuration. The difference between the patterns of mislocalization for bars flashed during the saccade for the two configurations corresponded quantitatively with a prediction based on compression towards the saccade endpoint considering the magnitude of the effect of the illusion on saccade amplitude. We conclude that mislocalization is related to the eye position at the end of the saccade, rather than to the position of the saccade target within the image.     

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.     

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.     

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     

Exploring the fundamental dynamics of error-based motor learning using a stationary predictive-saccade task

The maintenance of movement accuracy uses prior performance errors to correct future motor plans; this motor-learning process ensures that movements remain quick and accurate. The control of predictive saccades, in which anticipatory movements are made to future targets before visual stimulus information becomes available, serves as an ideal paradigm to analyze how the motor system utilizes prior errors to drive movements to a desired goal. Predictive saccades constitute a stationary process (the mean and to a rough approximation the variability of the data do not vary over time, unlike a typical motor adaptation paradigm). This enables us to study inter-trial correlations, both on a trial-by-trial basis and across long blocks of trials. Saccade errors are found to be corrected on a trial-by-trial basis in a direction-specific manner (the next saccade made in the same direction will reflect a correction for errors made on the current saccade). Additionally, there is evidence for a second, modulating process that exhibits long memory. That is, performance information, as measured via inter-trial correlations, is strongly retained across a large number of saccades (about 100 trials). Together, this evidence indicates that the dynamics of motor learning exhibit complexities that must be carefully considered, as they cannot be fully described with current state-space (ARMA) modeling efforts.     

Linear ensemble-coding in midbrain superior colliculus specifies the saccade kinematics

Recently, we proposed an ensemble-coding scheme of the midbrain superior colliculus (SC) in which, during a saccade, each spike emitted by each recruited SC neuron contributes a fixed minivector to the gaze-control motor output. The size and direction of this 'spike vector' depend exclusively on a cell's location within the SC motor map (Goossens and Van Opstal, in J Neurophysiol 95: 2326-2341, 2006). According to this simple scheme, the planned saccade trajectory results from instantaneous linear summation of all spike vectors across the motor map. In our simulations with this model, the brainstem saccade generator was simplified by a linear feedback system, rendering the total model (which has only three free parameters) essentially linear. Interestingly, when this scheme was applied to actually recorded spike trains from 139 saccade-related SC neurons, measured during thousands of eye movements to single visual targets, straight saccades resulted with the correct velocity profiles and nonlinear kinematic relations ('main sequence properties' and 'component stretching'). Hence, we concluded that the kinematic nonlinearity of saccades resides in the spatial-temporal distribution of SC activity, rather than in the brainstem burst generator. The latter is generally assumed in models of the saccadic system. Here we analyze how this behaviour might emerge from this simple scheme. In addition, we will show new experimental evidence in support of the proposed mechanism.     

Separate, causal roles of the caudate in saccadic choice and execution in a perceptual decision task

In contrast to the well-established roles of the striatum in movement generation and value-based decisions, its contributions to perceptual decisions lack direct experimental support. Here, we show that electrical microstimulation in the monkey caudate nucleus influences both choice and saccade response time on a visual motion discrimination task. Within a drift-diffusion framework, these effects consist of two components. The perceptual component biases choices toward ipsilateral targets, away from the neurons' predominantly contralateral response fields. The choice bias is consistent with a nonzero starting value of the diffusion process, which increases and decreases decision times for contralateral and ipsilateral choices, respectively. The nonperceptual component decreases and increases nondecision times toward contralateral and ipsilateral targets, respectively, consistent with the caudate's role in saccade generation. The results imply a causal role for the caudate in perceptual decisions used to select saccades that may be distinct from its role in executing those saccades. VIDEO ABSTRACT:     

A spiking neural network model of the midbrain superior colliculus that generates saccadic motor commands

Single-unit recordings suggest that the midbrain superior colliculus (SC) acts as an optimal controller for saccadic gaze shifts. The SC is proposed to be the site within the visuomotor system where the nonlinear spatial-to-temporal transformation is carried out: the population encodes the intended saccade vector by its location in the motor map (spatial), and its trajectory and velocity by the distribution of firing rates (temporal). The neurons’ burst profiles vary systematically with their anatomical positions and intended saccade vectors, to account for the nonlinear main-sequence kinematics of saccades. Yet, the underlying collicular mechanisms that could result in these firing patterns are inaccessible to current neurobiological techniques. Here, we propose a simple spiking neural network model that reproduces the spike trains of saccade-related cells in the intermediate and deep SC layers during saccades. The model assumes that SC neurons have distinct biophysical properties for spike generation that depend on their anatomical position in combination with a center–surround lateral connectivity. Both factors are needed to account for the observed firing patterns. Our model offers a basis for neuronal algorithms for spatiotemporal transformations and bio-inspired optimal controllers.     

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     

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.     

The effect of eye movement on the control of arm movement to a target

Abstract

The purpose of this study was to investigate the effect of eye movement on the control of arm movement to a target. Healthy humans flexed the elbow to a stationary target in response to a start tone. Simultaneously, the subject moved the eyes to the target (saccade eye movement), visually tracked a laser point moving with the arm (smooth pursuit eye movement), or gazed at a stationary start point at the midline of the horizontal visual angle (non-eye movement—NEM). Arm movement onset was delayed when saccade eye movement accompanied it. The onset of an electromyographic burst in the biceps muscle and the onset of saccade eye movement were almost simultaneous when both the arm and the eyes moved to the target. Arm movement duration during smooth pursuit eye movement was significantly longer than that during saccade eye movement or NEM. In spite of these findings, amplitudes of motor-evoked potential in the biceps and triceps brachii muscles were not significantly different among the eye movement conditions. These findings indicate that eye movement certainly affects the temporal control of arm movement, but may not affect corticospinal excitability in the arm muscles during arm movement.     

Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero-lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.     

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.     

Visual stability and the motion aftereffect: a psychophysical study revealing spatial updating

Eye movements create an ever-changing image of the world on the retina. In particular, frequent saccades call for a compensatory mechanism to transform the changing visual information into a stable percept. To this end, the brain presumably uses internal copies of motor commands. Electrophysiological recordings of visual neurons in the primate lateral intraparietal cortex, the frontal eye fields, and the superior colliculus suggest that the receptive fields (RFs) of special neurons shift towards their post-saccadic positions before the onset of a saccade. However, the perceptual consequences of these shifts remain controversial. We wanted to test in humans whether a remapping of motion adaptation occurs in visual perception.The motion aftereffect (MAE) occurs after viewing of a moving stimulus as an apparent movement to the opposite direction. We designed a saccade paradigm suitable for revealing pre-saccadic remapping of the MAE. Indeed, a transfer of motion adaptation from pre-saccadic to post-saccadic position could be observed when subjects prepared saccades. In the remapping condition, the strength of the MAE was comparable to the effect measured in a control condition (33±7% vs. 27±4%). Contrary, after a saccade or without saccade planning, the MAE was weak or absent when adaptation and test stimulus were located at different retinal locations, i.e. the effect was clearly retinotopic. Regarding visual cognition, our study reveals for the first time predictive remapping of the MAE but no spatiotopic transfer across saccades. Since the cortical sites involved in motion adaptation in primates are most likely the primary visual cortex and the middle temporal area (MT/V5) corresponding to human MT, our results suggest that pre-saccadic remapping extends to these areas, which have been associated with strict retinotopy and therefore with classical RF organization. The pre-saccadic transfer of visual features demonstrated here may be a crucial determinant for a stable percept despite saccades.     

Saccadic adaptation to moving targets

Saccades are so called ballistic movements which are executed without online visual feedback. After each saccade the saccadic motor plan is modified in response to post-saccadic feedback with the mechanism of saccadic adaptation. The post-saccadic feedback is provided by the retinal position of the target after the saccade. If the target moves after the saccade, gaze may follow the moving target. In that case, the eyes are controlled by the pursuit system, a system that controls smooth eye movements. Although these two systems have in the past been considered as mostly independent, recent lines of research point towards many interactions between them. We were interested in the question if saccade amplitude adaptation is induced when the target moves smoothly after the saccade. Prior studies of saccadic adaptation have considered intra-saccadic target steps as learning signals. In the present study, the intra-saccadic target step of the McLaughlin paradigm of saccadic adaptation was replaced by target movement, and a post-saccadic pursuit of the target. We found that saccadic adaptation occurred in this situation, a further indication of an interaction of the saccadic system and the pursuit system with the aim of optimized eye movements.     

Modeling Inter-trial Variability of Saccade Trajectories: Effects of Lesions of the Oculomotor Part of the Fastigial Nucleus

This study investigates the inter-trial variability of saccade trajectories observed in five rhesus macaques (Macaca mulatta). For each time point during a saccade, the inter-trial variance of eye position and its covariance with eye end position were evaluated. Data were modeled by a superposition of three noise components due to 1) planning noise, 2) signal-dependent motor noise, and 3) signal-dependent premotor noise entering within an internal feedback loop. Both planning noise and signal-dependent motor noise (together called accumulating noise) predict a simple S-shaped variance increase during saccades, which was not sufficient to explain the data. Adding noise within an internal feedback loop enabled the model to mimic variance/covariance structure in each monkey, and to estimate the noise amplitudes and the feedback gain. Feedback noise had little effect on end point noise, which was dominated by accumulating noise. This analysis was further extended to saccades executed during inactivation of the caudal fastigial nucleus (cFN) on one side of the cerebellum. Saccades ipsiversive to an inactivated cFN showed more end point variance than did normal saccades. During cFN inactivation, eye position during saccades was statistically more strongly coupled to eye position at saccade end. The proposed model could fit the variance/covariance structure of ipsiversive and contraversive saccades. Inactivation effects on saccade noise are explained by a decrease of the feedback gain and an increase of planning and/or signal-dependent motor noise. The decrease of the fitted feedback gain is consistent with previous studies suggesting a role for the cerebellum in an internal feedback mechanism. Increased end point variance did not result from impaired feedback but from the increase of accumulating noise. The effects of cFN inactivation on saccade noise indicate that the effects of cFN inactivation cannot be explained entirely with the cFN’s direct connections to the saccade-related premotor centers in the brainstem.