Incomplete suppression of distractor-related activity in the frontal eye field results in curved saccades

Saccades in the presence of distractors show significant trajectory curvature. Based on previous work in the superior colliculus (SC), we speculated that curvature arises when a movement is initiated before competition between the target and distractor goals has been fully resolved. To test this hypothesis, we recorded frontal eye field (FEF) activity for curved and straight saccades in search. In contrast to the SC, activity in FEF is normally poorly correlated with saccade dynamics. However, the FEF, like the SC, is involved in target selection. Thus if curvature is caused by incomplete target selection, we expect to see its neural correlates in the FEF. We found that saccades that curve toward a distractor are accompanied by an increase in perisaccadic activity of FEF neurons coding the distractor location, and saccades that curve away are accompanied by a decrease in activity. In contrast, for FEF neurons coding the target location, there is no significant difference in activity between curved and straight saccades. To establish that the distractor-related activity is causally related to saccade curvature, we applied microstimulation to sites in the FEF before saccades to targets presented without distractors. The stimulation was subthreshold for evoking saccades and the temporal structure of the stimulation train resembled the activity recorded for curved saccades. The resulting movements curved toward the location coded by the stimulation site. These results support the idea that saccade curvature results from incomplete suppression of distractor-related activity during target selection.     

Difficulty of visual search modulates neuronal interactions and response variability in the frontal eye field

The frontal eye field (FEF) is involved in selecting visual targets for eye movements. To understand how populations of FEF neurons interact during target selection, we recorded activity from multiple neurons simultaneously while macaques performed two versions of a visual search task. We used a multivariate analysis in a point process statistical framework to estimate the instantaneous firing rate and compare interactions among neurons between tasks. We found that FEF neurons were engaged in more interactions during easier visual search tasks compared with harder search tasks. In particular, eye movement-related neurons were involved in more interactions than visual-related neurons. In addition, our analysis revealed a decrease in the variability of spiking activity in the FEF beginning approximately 100 ms before saccade onset. The minimum in response variability occurred approximately 20 ms earlier for the easier search task compared with the harder one. This difference is positively correlated with the difference in saccade reaction times for the two tasks. These findings show that a multivariate analysis can provide a measure of neuronal interactions and characterize the spiking activity of FEF neurons in the context of a population of neurons.     

Primate frontal eye fields. I. Single neurons discharging before saccades

We studied the activity of single neurons in the frontal eye fields of awake macaque monkeys trained to perform several oculomotor tasks. Fifty-four percent of neurons discharged before visually guided saccades. Three different types of presaccadic activity were observed: visual, movement, and anticipatory. Visual activity occurred in response to visual stimuli whether or not the monkey made saccades. Movement activity preceded purposive saccades, even those made without visual targets. Anticipatory activity preceded even the cue to make a saccade if the monkey could reliably predict what saccade he had to make. These three different activities were found in different presaccadic cells in different proportions. Forty percent of presaccadic cells had visual activity (visual cells) but no movement activity. For about half of the visual cells the response was enhanced if the monkey made saccades to the receptive-field stimulus, but there was no discharge before similar saccades made without visual targets. Twenty percent of presaccadic neurons discharged as briskly before purposive saccades made without a visual target as they did before visually guided saccades, and had weak or absent visual responses. These cells were defined as movement cells. Movement cells discharged much less or not at all before saccades made spontaneously without a task requirement or an overt visual target. The remaining presaccadic neurons (40%) had both visual and movement activity (visuomovement cells). They discharged most briskly before visually guided eye movements, but also discharged before purposive eye movements made in darkness and responded to visual stimuli in the absence of saccades. There was a continuum of visuomovement cells, from cells in which visual activity predominated to cells in which movement activity predominated. This continuum suggests that although visual cells are quite distinct from movement cells, the division of cell types into three classes may be only a heuristic means of describing the processing flow from visual input to eye-movement output. Twenty percent of visuomovement and movement cells, but fewer than 2% of visual cells, had anticipatory activity. Only one cell had anticipatory activity as its sole response. When the saccade was delayed relative to the target onset, visual cells responded to the target appearance, movement cells discharged before the saccade, and visuomovement cells discharged in different ways during the delay, usually with some discharge following the target and an increase in rate immediately before the saccade. Presaccadic neurons of all types were actively suppressed following a saccade into their response fields.(ABSTRACT TRUNCATED AT 400 WORDS)     

Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades.

Muscimol-induced inactivation of the monkey frontal eye field: effects on visually and memory-guided saccades. Although neurophysiological, anatomic, and imaging evidence suggest that the frontal eye field (FEF) participates in the generation of eye movements, chronic lesions of the FEF in both humans and monkeys appear to cause only minor deficits in visually guided saccade generation. Stronger effects are observed when subjects are tested in tasks with more cognitive requirements. We tested oculomotor function after acutely inactivating regions of the FEF to minimize the effects of plasticity and reallocation of function after the loss of the FEF and gain more insight into the FEF contribution to the guidance of eye movements in the intact brain. Inactivation was induced by microinjecting muscimol directly into physiologically defined sites in the FEF of three monkeys. FEF inactivation severely impaired the monkeys' performance of both visually guided and memory-guided saccades. The monkeys initiated fewer saccades to the retinotopic representation of the inactivated FEF site than to any other location in the visual field. The saccades that were initiated had longer latencies, slower velocities, and larger targeting errors than controls. These effects were present both for visually guided and for memory-guided saccades, although the memory-guided saccades were more disrupted. Initially, the effects were restricted spatially, concentrating around the retinotopic representation at the center of the inactivated site, but, during the course of several hours, these effects spread to flanking representations. Predictability of target location and motivation of the monkey also affected saccadic performance. For memory-guided saccades, increases in the time during which the monkey had to remember the spatial location of a target resulted in further decreases in the accuracy of the saccades and in smaller peak velocities, suggesting a progressive loss of the capacity to maintain a representation of target location in relation to the fovea after FEF inactivation. In addition, the monkeys frequently made premature saccades to targets in the hemifield ipsilateral to the injection site when performing the memory task, indicating a deficit in the control of fixation that could be a consequence of an imbalance between ipsilateral and contralateral FEF activity after the injection. There was also a progressive loss of fixation accuracy, and the monkeys tended to restrict spontaneous visual scanning to the ipsilateral hemifield. These results emphasize the strong role of the FEF in the intact monkey in the generation of all voluntary saccadic eye movements, as well as in the control of fixation.     

Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields.

1. The purpose of this study was to analyze the response properties of neurons in the frontal eye fields (FEF) of rhesus monkeys (Macaca mulatta) and to compare and contrast the various functional classes with those recorded in the supplementary eye fields (SEF) of the same animals performing the same go/no-go visual tracking task. Three hundred ten cells recorded in FEF provided the data for this investigation. 2. Visual cells in FEF responded to the stimuli that guided the eye movements. The visual cells in FEF responded with a slightly shorter latency and were more consistent and phasic in their activation than their counterparts in SEF. The receptive fields tended to emphasize the contralateral hemifield to the same extent as those observed in SEF visual cells. 3. Preparatory set cells began to discharge after the presentation of the target and ceased firing before the saccade, after the go/no-go cue was given. These neurons comprised a smaller proportion in FEF than in SEF. In contrast to their counterparts in SEF, the preparatory set cells in FEF did not respond preferentially in relation to contralateral movements, even though most responded preferentially for movements in one particular direction. The time course of the discharge of the FEF set cells was similar to that of their SEF counterparts, except that they reached their peak level of activation sooner. The few preparatory set cells in FEF tested with both auditory and visual stimuli tended to respond preferentially to the visual targets, whereas, in contrast, most set cells in SEF were bimodal. 4. Sensory-movement cells represented the largest population of cells recorded in FEF, responding in relation to both the presentation of the targets and the execution of the saccade. Although some of these sensory-movement cells resembled their counterparts in SEF by exhibiting a sustained elevation of activity, most of the FEF sensory-movement cells gave two discrete bursts, one after the presentation of the target and another before and during the saccade. Like their counterparts in SEF, the sensory-movement cells tended to be tuned for saccades into the contralateral hemifield, but this tendency was more pronounced in FEF than in SEF. The FEF sensory-movement cells discharged more briskly, with a shorter latency relative to the presentation of the target, than their counterparts in SEF. In addition, the FEF sensory-movement neurons reached their peak activation sooner than SEF sensory-movement neurons. Most FEF sensory-movement cells exhibited different patterns of activation in response to visual and auditory targets.(ABSTRACT TRUNCATED AT 400 WORDS)     

The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation

The dorsomedial frontal cortex (DMFC) of monkeys has been implicated in mediating visually guided saccadic eye movements. The purpose of this study was to determine whether the DMFC has a topographic map coding final eye position, and to ascertain whether this region subserves the maintenance of eye position. The DMFC was stimulated electrically while monkeys fixated a target presented somewhere in visual space. A series of parametric tests was conducted to ascertain the best stimulation parameters to evoke saccades. Electrical stimulation typically produced contraversive saccades that converged onto a region of space, the termination zone. For some stimulation sites, however, stimulation produced ipsiversive saccades. This occurred when the termination zone was located straight ahead of the monkey. Convergence onto an orbital position was never observed during stimulation of the frontal eye fields (FEF), stimulation of which evoked fixed-vector saccades. The latency to evoke a saccade from the DMFC varied with fixation position, such that it increased monotonically the closer the fix spot was to the termination zone. Moreover, the probability of evoking a saccade from the DMFC decreased the closer the fix spot was to the termination zone. The latency for evoking a saccade and the probability of evoking a saccade from the FEF did not vary with fixation position. Horizontal head movements were not evoked from the DMFC while a monkey fixated targets presented in different positions of visual space. Moveover, changing the position of the head with respect to the body did not change the location of a termination zone with respect to the head. The DMFC was found to contain a topographic coding of termination zones, with rostral sites representing zones in extreme contralateral visual space, and caudal sites representing zones straight ahead or ipsilaterally. Furthermore, lateral sites represented zones in upper visual space, whereas medial sites represented zones in lower visual space. Once the eyes were positioned within a termination zone, further stimulation fixed the gaze and inhibited visually evoked saccades. Following release from inhibition, which occurred shortly after the end of stimulation, the saccades reached the visual target accurately. This shows that the stimulation delayed the execution of the saccades without actually aborting their execution. We conclude that the DMFC contains a map representing eye position in craniotopic coordinates, and we argue that this map is utilized to maintain eye position.     

Dynamic dissociation of visual selection from saccade programming in frontal eye field.

Previous studies of visually responsive neurons in the frontal eye fields have identified a selection process preceding saccades during visual search. The goal of this experiment was to determine whether the selection process corresponds to the selection of a conspicuous stimulus or to preparation of the next saccade. This was accomplished with the use of a novel task, called search-step, in which the target of a singleton visual search array switches location with a distracter on random trials. The target step trials created a condition in which the same stimulus yielded saccades either toward or away from the target. Visually responsive neurons in frontal eye field selected the current location of the conspicuous target even when gaze shifted to the location of a distractor. This dissociation demonstrates that the selection process manifest in visual neurons in the frontal eye field may be an explicit interpretation of the image and not an obligatory saccade command.     

Visual and vergence eye movement-related responses of pursuit neurons in the caudal frontal eye fields to motion-in-depth stimuli

The caudal parts of the frontal eye fields (FEF) contain smooth-pursuit related neurons. Previous studies show that most FEF pursuit neurons carry visual signals in relation to frontal spot motion and discharge before the initiation of smooth-pursuit. It has also been demonstrated that most FEF pursuit neurons discharge during vergence tracking. Accurate vergence tracking requires information about target motion-in-depth. To further understand the role of the FEF in vergence tracking and to determine whether FEF pursuit neurons carry visual information about target motion-in-depth, we examined visual and vergence eye movement-related responses of FEF pursuit neurons to sinusoidal spot motion-in-depth. During vergence tracking, most FEF pursuit neurons exhibited both vergence eye position and velocity sensitivity. Phase shifts (re target velocity) of most neurons remained virtually constant up to 1.5 Hz. About half of FEF pursuit neurons exhibited visual responses to spot motion-in-depth. The preferred directions for visual responses of most neurons were similar to those during vergence tracking. Visual responses of most of these neurons exhibited sensitivity to the velocity of spot motion-in-depth. Phase shifts of most of the responding neurons remained virtually constant up to 2.0 Hz. Neurons that exhibited visual responses in-depth were mostly separate from neurons that showed visual responses in the frontal plane. To further examine whether FEF pursuit neurons could participate in initiation of vergence tracking, we examined latencies of neuronal responses with respect to vergence eye movements induced by step target motion-in-depth. About half of FEF pursuit neurons discharged before the onset of vergence eye movements with lead times longer than 20 ms. These results together with previous observations suggest that the caudal FEF carries visual signals appropriate to be converted into motor commands for pursuit in depth and frontal plane.     

Frontal eye field activity before visual search errors reveals the integration of bottom-up and top-down salience

We investigated the saccade decision process by examining activity recorded in the frontal eye field (FEF) of monkeys performing 2 separate visual search experiments in which there were errors in saccade target choice. In the first experiment, the difficulty of a singleton search task was manipulated by varying the similarity between the target and distractors; errors were made more often when the distractors were similar to the target. On catch trials in which the target was absent the monkeys occasionally made false alarm errors by shifting gaze to one of the distractors. The second experiment was a popout color visual search task in which the target and distractor colors switched unpredictably across trials. Errors occurred most frequently on the first trial after the switch and less often on subsequent trials. In both experiments, FEF neurons selected the saccade goal on error trials, not the singleton target of the search array. Although saccades were made to the same stimulus locations, presaccadic activation and the magnitude of selection differed across trial conditions. The variation in presaccadic selective activity was accounted for by the variation in saccade probability across the stimulus-response conditions, but not by variations in saccade metrics. These results suggest that FEF serves as a saccade probability map derived from the combination of bottom-up and top-down influences. Peaks on this map represent the behavioral relevance of each item in the visual field rather than just reflecting saccade preparation. This map in FEF may correspond to the theoretical salience map of many models of attention and saccade target selection.     

Reversible inactivation of macaque frontal eye field

 The macaque frontal eye field (FEF) is involved in the generation of saccadic eye movements and fixations. To better understand the role of the FEF, we reversibly inactivated a portion of it while a monkey made saccades and fixations in response to visual stimuli. Lidocaine was infused into a FEF and neural inactivation was monitored with a nearby microelectrode. We used two saccadic tasks. In the delay task, a target was presented and then extinguished, but the monkey was not allowed to make a saccade to its location until a cue to move was given. In the step task, the monkey was allowed to look at a target as soon as it appeared. During FEF inactivation, monkeys were severely impaired at making saccades to locations of extinguished contralateral targets in the delay task. They were similarly impaired at making saccades to locations of contralateral targets in the step task if the target was flashed for ≤100 ms, such that it was gone before the saccade was initiated. Deficits included increases in saccadic latency, increases in saccadic error, and increases in the frequency of trials in which a saccade was not made. We varied the initial fixation location and found that the impairment specifically affected contraversive saccades rather than affecting all saccades made into head-centered contralateral space. Monkeys were impaired only slightly at making saccades to contralateral targets in the step task if the target duration was 1000 ms, such that the target was present during the saccade: latency increased, but increases in saccadic error were mild and increases in the frequency of trials in which a saccade was not made were insignificant. During FEF inactivation there usually was a direct correlation between the latency and the error of saccades made in response to contralateral targets. In the delay task, FEF inactivation increased the frequency of making premature saccades to ipsilateral targets. FEF inactivation had inconsistent and mild effects on saccadic peak velocity. FEF inactivation caused impairments in the ability to fixate lights steadily in contralateral space. FEF inactivation always caused an ipsiversive deviation of the eyes in darkness. In summary, our results suggest that the FEF plays major roles in (1) generating contraversive saccades to locations of extinguished or flashed targets, (2) maintaining contralateral fixations, and (3) suppressing inappropriate ipsiversive saccades. Received: 2 February 1996 / Accepted: 26 February 1997     

The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

Summary The activity of 249 neurons in the dorsomedial frontal cortex was studied in two macaque monkeys. The animals were trained to release a bar when a visual stimulus changed color in order to receive reward. An acoustic cue signaled the start of a series of trials to the animal, which was then free to begin each trial at will. The monkeys tended to fixate the visual stimuli and to make saccades when the stimuli moved. The monkeys were neither rewarded for making proper eye movements nor punished for making extraneous ones. We found neurons whose discharge was related to various movements including those of the eye, neck, and arm. In this report, we describe the properties of neurons that showed activity related to visual fixation and saccadic eye movement. Fixation neurons discharged during active fixation with the eye in a given position in the orbit, but did not discharge when the eye occupied the same orbital positions during nonactive fixation. These neurons showed neither a classic nor a complex visual receptive field, nor a foveal receptive visual field. Electrical stimulation at the site of the fixation neurons often drove the eye to the orbital position associated with maximal activity of the cell. Several different kinds of neurons were found to discharge before saccades: 1) checking-saccade neurons, which discharged when the monkeys made self-generated saccades to extinguish LED's; 2) novelty-detection saccade neurons, which discharged before the first saccade made to a new visual target but whose activity waned with successive presentations of the same target. These results suggest that the dorsomedial frontal cortex is involved in attentive fixation. We hypothesize that the fixation neurons may be involved in codifying the saccade toward a target. We propose that their involvement in arm-eye-head motor-planning rests primarily in targeting the goal of the movement. The fact that saccaderelated neurons discharge when the saccades are self initiated, implies that this area of the cortex may share the control of voluntary saccades with the frontal eye fields and that the activation is involved in intentional motor processes.     

Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey

Recent work has shown that humans and monkeys utilize both retinal error and eye position signals to compute the direction and amplitude of saccadic eye movements (Hallett and Lightstone 1976a, b; Mays and Sparks 1980b). The aim of this study was to examine the role the frontal eye fields (FEF) and the superior colliculi (SC) play in this computation. Rhesus monkeys were trained to acquire small, briefly flashed spots of light with saccadic eye movements. During the latency period between target extinction and saccade initiation, their eyes were displaced, in total darkness, by electrical stimulation of either the FEF, the SC or the abducens nucleus area. Under such conditions animals compensated for the electrically induced ocular displacement and correctly reached the visual target area, suggesting that both a retinal error and eye position error signal were computed. The amplitude and direction of the electrically induced saccades depended not only on the site stimulated but also on the amplitude and direction of the eye movement initiated by the animal to acquire the target. When the eye movements initiated by the animal coincided with the saccades initiated by electrical stimulation, the resultant saccade was the weighted average of the two, where one weighing factor was the intensity of the electrical stimulus. Animals did not acquire targets correctly when their eyes were displaced, prior to their intended eye movements, by stimulating in the abducens nucleus area. After bilateral ablation of either the FEF or the SC monkeys were still able to acquire visual targets when their eyes were displaced, prior to saccade initiation, by electrical stimulation of the remaining intact structure. These results suggest that neither the FEF nor the SC is uniquely responsible for the combined computation of the retinal error and the eye position error signals.     

Relation of frontal eye field activity to saccade initiation during a countermanding task

The countermanding (or stop signal) task probes the control of the initiation of a movement by measuring subjects’ ability to withhold a movement in various degrees of preparation in response to an infrequent stop signal. Previous research found that saccades are initiated when the activity of movement-related neurons reaches a threshold, and saccades are withheld if the growth of activity is interrupted. To extend and evaluate this relationship of frontal eye field (FEF) activity to saccade initiation, two new analyses were performed. First, we fit a neurometric function that describes the proportion of trials with a stop signal in which neural activity exceeded a criterion discharge rate as a function of stop signal delay, to the inhibition function that describes the probability of producing a saccade as a function of stop signal delay. The activity of movement-related but not visual neurons provided the best correspondence between neurometric and inhibition functions. Second, we determined the criterion discharge rate that optimally discriminated between the distributions of discharge rates measured on trials when saccades were produced or withheld. Differential activity of movement-related but not visual neurons could distinguish whether a saccade occurred. The threshold discharge rates determined for individual neurons through these two methods agreed. To investigate how reliably movement-related activity predicted movement initiation; the analyses were carried out with samples of activity from increasing numbers of trials from the same or from different neurons. The reliability of both measures of initiation threshold improved with number of trials and neurons to an asymptote of between 10 and 20 movement-related neurons. Combining the activity of visual neurons did not improve the reliability of predicting saccade initiation. These results demonstrate how the activity of a population of movement-related but not visual neurons in the FEF contributes to the control of saccade initiation. The results also validate these analytical procedures for identifying signals that control saccade initiation in other brain structures.

Intrasaccadic target steps during the deceleration of primary saccades affect the latency of corrective saccades

This study investigates how visually guided saccades and subsequent corrective saccades are affected by a secondary target step occurring at different times during the primary saccade. Eye movements of human subjects were measured by means of a differential infrared light reflection technique while the subjects performed visually guided saccades to a laser spot in darkness. The target was stepped backward or onward during the targeting saccade. While the intrasaccadic target step did not influence gain, peak velocity or skewness of the primary saccade, it had a significant effect on the subsequent corrective saccade when the secondary target step occurred during the deceleration phase of the primary saccade: the latency of the corrective saccade was significantly increased compared with the one performed under the single-step control condition. This increase also occurred when single target steps were presented randomly intermixed with backward and onward double target steps and even between selected sub-samples of saccades with identical postsaccadic visual error. If the target step occurred early during the primary saccade, the latency of the corrective saccade was not changed. This indicates that visual information sampled during the deceleration phase of a saccade can lead to a cancellation of the normal trigger mode of corrective saccades. Received: 9 April 1999 / Accepted: 23 June 1999     

Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets

Neurons in the rostral superior colliculus (SC) of alert cats exhibit quasi-sustained discharge patterns related to the fixation of visual targets. Because some SC neurons also respond to auditory stimuli, we investigated whether there is a population of neurons in the rostral SC which is active in relation to fixation of both auditory and visual targets. We identified cells which were active with visual fixation and which continued to discharge if the fixation stimulus was briefly extinguished. The population of neurons exhibited similar discharge characteristics when the fixation stimulus was auditory. Few neurons were significantly more active during fixation of visual targets than during fixation of auditory targets. Most fixation neurons showed a diminished discharge rate during spontaneous (self-generated) saccadic eye movements away from a visual fixation stimulus, regardless of the direction of the saccade. this diminished discharge rate (or pause) typically began, on average, 12.2 ms before saccade onset and the duration of the pause was Ionger than the duration of the saccade. These observations are consistent with the hypothesis that increased discharge of these neurons is related to active fixation and that reductions in their activity are important for the generation of saccades. However, the lack of a precise relationship between pause duration and saccade duration implies that these neurons would be unlikely to project directly to the saccadic burst generator. The mean interval from the beginning of the pauses of fixation neurons to be beginning of the saccades away from fixation targets is also shorter than has been found in brainstem omnipause neurons. By analogy with the concept of a receptive field, agaze position error field depicts the range of gaze position error for which a cell is active. Although fixation neurons appear to encode the magnitude and direction of the error between visual targets and the visual axis, visual error fields at the end of fixating eye movements were significantly larger than those at stimulus onset. For auditory stimuli, this difference was not significant. These observations are compatible with a number of recent experiments indicating that neural signals of eye position are damped or delayed with respect to current eye position.     

Modulation of shifting receptive field activity in frontal eye field by visual salience

In the monkey frontal eye field (FEF), the sensitivity of some neurons to visual stimulation changes just before a saccade. Sensitivity shifts from the spatial location of its current receptive field (RF) to the location of that field after the saccade is completed (the future field, FF). These shifting RFs are thought to contribute to the stability of visual perception across saccades, and in this study we investigated whether the salience of the FF stimulus alters the magnitude of FF activity. We reduced the salience of the usually single flashed stimulus by adding other visual stimuli. We isolated 171 neurons in the FEF of 2 monkeys and did experiments on 50 that had FF activity. In 30% of these, that activity was higher before salience was reduced by adding stimuli. The mean magnitude reduction was 16%. We then determined whether the shifting RFs were more frequent in the central visual field, which would be expected if vision across saccades were only stabilized for the visual field near the fovea. We found no evidence of any skewing of the frequency of shifting receptive fields (or the effects of salience) toward the central visual field. We conclude that the salience of the FF stimulus makes a substantial contribution to the magnitude of FF activity in FEF. In so far as FF activity contributes to visual stability, the salience of the stimulus is probably more important than the region of the visual field in which it falls for determining which objects remain perceptually stable across saccades.     

Eye position and memory saccade related responses in substantia nigra pars reticulata

The substantia nigra pars reticulata (SNr), a major output nucleus of the basal ganglia, has been implicated anatomically, pharmacologically and physiologically in the generation of saccadic eye movements. However, the unique contribution of the SNr to saccade generation remains elusive. We studied the activity of SNr neurons while rhesus monkeys made saccades from different initial orbital positions, to determine what effects, if any, eye position had on SNr neuronal activity. We found that there was no effect of eye position on SNr neuronal responses. We also examined the responses of SNr neurons during memory-guided saccades to determine whether SNr discharges were affected by whether the target of the upcoming saccade was visible. We found that there was no change in response properties during memory saccade trials as compared to otherwise identical visually guided trials. SNr neurons appear to carry no information about either eye position or whether a movement is guided by a visible or remembered target. These results suggest that nigral signals are encoded in the same coordinate frame as those in the SC and FEF, but that unlike neuronal responses in these areas, SNr activity is not influenced by whether the saccade target remains visible until the movement is executed.     

Neuronal responses to moving targets in monkey frontal eye fields

Due to delays in visuomotor processing, eye movements directed toward moving targets must integrate both target position and velocity to be accurate. It is unknown where and how target velocity information is incorporated into the planning of rapid (saccadic) eye movements. We recorded the activity of neurons in frontal eye fields (FEFs) while monkeys made saccades to stationary and moving targets. A substantial fraction of FEF neurons was found to encode not only the initial position of a moving target, but the metrics (amplitude and direction) of the saccade needed to intercept the target. Many neurons also encoded target velocity in a nearly linear manner. The quasi-linear dependence of firing rate on target velocity means that the neuronal response can be directly read out to compute the future position of a target moving with constant velocity. This is demonstrated using a quantitative model in which saccade amplitude is encoded in the population response of neurons tuned to retinal target position and modulated by target velocity.     

Electrical stimulation of the frontal eye fields in the head-free macaque evokes kinematically normal 3D gaze shifts

The frontal eye field (FEF) is a region of the primate prefrontal cortex that is central to eye-movement generation and target selection. It has been shown that neurons in this area encode commands for saccadic eye movements. Furthermore, it has been suggested that the FEF may be involved in the generation of gaze commands for the eye and the head. To test this suggestion, we systematically stimulated (with pulses of 300 Hz frequency, 200 ms duration, 30-100 μA intensity) the FEF of two macaques, with the head unrestrained, while recording three-dimensional (3D) eye and head rotations. In a total of 95 sites, the stimulation consistently elicited gaze-orienting movements ranging in amplitude from 2 to 172°, directed contralateral to the stimulation site, and with variable vertical components. These movements were typically a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between the stimulation-evoked movements and gaze shifts voluntarily made by the animal. The kinematics of the stimulation-evoked movements (i.e., their spatiotemporal properties, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were very similar to those of natural gaze shifts. Moreover, they obeyed the same 3D constraints as the natural gaze shifts (i.e., modified Listing's law for eye-in-head movements). As in natural gaze shifts, saccade and vestibuloocular reflex torsion during stimulation-evoked movements were coordinated so that at the end of the head movement the eye-in-head ended up in Listing's plane. In summary, movements evoked by stimulation of the FEF closely resembled those of naturally occurring eye-head gaze shifts. Thus we conclude that the FEF explicitly encodes gaze commands and that the kinematic aspects of eye-head coordination are likely specified by downstream mechanisms.     

Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task

Several lines of evidence suggest that the pars reticulata subdivision of the substantia nigra (SNr) plays a role in the generation of saccadic eye movements. However, the responses of SNr neurons during saccades have not been examined with the same level of quantitative detail as the responses of neurons in other key saccadic areas. For this report, we examined the firing rates of 72 SNr neurons while awake-behaving primates correctly performed an average of 136 trials of a visually guided delayed saccade task. On each trial, the location of the visual target was chosen randomly from a grid spanning 40 degrees of horizontal and vertical visual angle. We measured the firing rates of each neuron during five intervals on every trial: a baseline interval, a fixation interval, a visual interval, a movement interval, and a reward interval. We found four distinct classes of SNr neurons. Two classes of neurons had firing rates that decreased during delayed saccade trials. The firing rates of discrete pausers decreased after the onset of a contralateral target and/or before the onset of a saccade that would align gaze with that target. The firing rates of universal pausers decreased after fixation on all trials and remained below baseline until the delivery of reinforcement. We also found two classes of SNr neurons with firing rates that increased during delayed saccade trials. The firing rates of bursters increased after the onset of a contralateral target and/or before the onset of a saccade aligning gaze with that target. The firing rates of pause-bursters increased after the onset of a contralateral target but decreased after the illumination of an ipsilateral target. Our quantification of the response profiles of SNr neurons yielded three novel findings. First, we found that some SNr neurons generate saccade-related increases in activity. Second, we found that, for nearly all SNr neurons, the relationship between firing rate and horizontal and vertical saccade amplitude could be well described by a planar surface within the range of movements we sampled. Finally we found that for most SNr neurons, saccade-related modulations in activity were highly variable on a trial-by-trial basis.