Simulations of saccade curvature by models that place superior colliculus upstream from the local feedback loop

When humans or monkeys are asked to make saccades to visual targets accompanied by one or more distractors, the two dimensional trajectory of the saccade will sometimes display significant curvature. Port and Wurtz used dual electrode recordings to show that this phenomenon is associated with activity at more than one site in superior colliculus (SC). The timing and initial direction of the curvature could be predicted by computing a weighted vector average of the normalized activity of the two neurons. As these authors noted, however, this approach does not result in correct predictions of the final direction of curved saccades. We show that the final direction of these movements can be predicted by taking into account the brain stem saccade generator and the local feedback loop. If the output of SC is computed as a weighted vector average of the saccades requested by the activated sites, and this collicular output is interpreted by downstream structures as desired displacement, existing models that place SC upstream from the local feedback loop can generate realistic saccade trajectories, including the final direction. We propose that saccade curvature is the result of a change in the relative level of activity at the two sites, which the brain stem saccade generator interprets as a change in desired displacement.     

Competition between saccade goals in the superior colliculus produces saccade curvature

When saccadic eye movements are made in a search task that requires selecting a target from distractors, the movements show greater curvature in their trajectories than similar saccades made to single stimuli. To test the hypothesis that this increase in curvature arises from competitive interactions between saccade goals occurring near the time of movement onset, we performed single-unit recording and microstimulation experiments in the superior colliculus (SC). We found that saccades that ended near the target but curved toward a distractor were accompanied by increased presaccadic activity of SC neurons coding the distractor site. This increased activity occurred approximately 30 ms before saccade onset and was abruptly quenched on saccade initiation. The magnitude of increased activity at the distractor site was correlated with the amount of curvature toward the distractor. In contrast, neurons coding the target location did not show any significant difference in discharge for curved versus straight saccades. To determine whether this pattern of SC discharge is causally related to saccade curvature, we performed a second series of experiments using electrical microstimulation. Monkeys made saccades to single visual stimuli presented without distractors, and we stimulated sites in the SC that would have corresponded to distractor sites in the search task. The stimulation was subthreshold for evoking saccades, but when its temporal structure mimicked the activity recorded for curved saccades in search, the subsequent saccades to the visual target showed curvature toward the location coded by the stimulation site. The effect was larger for higher stimulation frequencies and when the stimulation site was in the same colliculus as the representation of the visual target. These results support the hypothesis that the increased saccade curvature observed in search arises from rivalry between target and distractor goals and are consistent with the idea that the SC is involved in the competitive neural interactions underlying saccade target selection.     

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.     

Multielectrode evidence for spreading activity across the superior colliculus movement map

The monkey superior colliculus (SC) has maps for both visual input and movement output in the superficial and intermediate layers, respectively, and activity on these maps is generally related to visual stimuli only in one part of the visual field and/or to a restricted range of saccadic eye movements to those stimuli. For some neurons within these maps, however, activity has been reported to spread from the caudal SC to the rostral SC during the course of a saccade. This spread of activity was inferred from averages of recordings at different sites on the SC movement map during saccades of different amplitudes and even in different monkeys. In the present experiments, SC activity was recorded simultaneously in pairs of neurons to observe the spread of activity during individual saccades. Two electrodes were positioned along the rostral-caudal axis of the SC with one being more caudal than the other, and 60 neuron pairs whose movement fields were large enough to see a spread of activity were studied. During individual saccades, the relative time of discharge of the two neurons was compared using 1) the time difference between peak discharge of the two neurons, 2) the difference between the "median activation time" of the two neurons, and 3) the shift required to align the two discharge patterns using cross-correlation. All three analysis methods gave comparable results. Many pairs of neurons were activated in sequence during saccade generation, and the order of activation was most frequently caudal to rostral. Such a sequence of activation was not observed in every neuron pair, but over the sample of neuron pairs studied, the spread was statistically significant. When we compared the time of neuronal activity to the time of saccade onset, we found that the caudal neuronal activity was more likely to be before the saccade, whereas the rostral neuronal activity was more likely to be during the saccade. These results demonstrate that when individual pairs of neurons are examined during single saccades there is evidence of a caudal to rostral spread of activity within the monkey SC, and they confirm the previous inferences of a spread of activity drawn from observations on averaged neuronal activity during multiple saccades. The functional contribution of this spread of activity remains to be determined.     

Target selection for saccadic eye movements: direction-selective visual responses in the superior colliculus.

We investigated the role of the superior colliculus (SC) in saccade target selection in rhesus monkeys who were trained to perform a direction-discrimination task. In this task, the monkey discriminated between opposed directions of visual motion and indicated its judgment by making a saccadic eye movement to one of two visual targets that were spatially aligned with the two possible directions of motion in the display. Thus the neural circuits that implement target selection in this task are likely to receive directionally selective visual inputs and be closely linked to the saccadic system. We therefore studied prelude neurons in the intermediate and deep layers of the SC that can discharge up to several seconds before an impending saccade, indicating a relatively high-level role in saccade planning. We used the direction-discrimination task to identify neurons whose prelude activity "predicted" the impending perceptual report several seconds before the animal actually executed the operant eye movement; these "choice predicting" cells comprised approximately 30% of the neurons we encountered in the intermediate and deep layers of the SC. Surprisingly, about half of these prelude cells yielded direction-selective responses to our motion stimulus during a passive fixation task. In general, these neurons responded to motion stimuli in many locations around the visual field including the center of gaze where the visual discriminanda were positioned during the direction-discrimination task. Preferred directions generally pointed toward the location of the movement field of the SC neuron in accordance with the sensorimotor demands of the discrimination task. Control experiments indicate that the directional responses do not simply reflect covertly planned saccades. Our results indicate that a small population of SC prelude neurons exhibits properties appropriate for linking stimulus cues to saccade target selection in the context of a visual discrimination task.     

Frontal eye field contributions to rapid corrective saccades

Visually guided movements can be inaccurate, especially if unexpected events occur while the movement is programmed. Often errors of gaze are corrected before external feedback can be processed. Evidence is presented from macaque monkey frontal eye field (FEF), a cortical area that selects visual targets, allocates attention, and programs saccadic eye movements, for a neural mechanism that can correct saccade errors before visual afferent or performance monitoring signals can register the error. Macaques performed visual search for a color singleton that unpredictably changed position in a circular array as in classic double-step experiments. Consequently, some saccades were directed in error to the original target location. These were followed frequently by unrewarded, corrective saccades to the final target location. We previously showed that visually responsive neurons represent the new target location even if gaze shifted errantly to the original target location. Now we show that the latency of corrective saccades is predicted by the timing of movement-related activity in the FEF. Preceding rapid corrective saccades, the movement-related activity of all neurons began before explicit error signals arise in the medial frontal cortex. The movement-related activity of many neurons began before visual feedback of the error was registered and that of a few neurons began before the error saccade was completed. Thus movement-related activity leading to rapid corrective saccades can be guided by an internal representation of the environment updated with a forward model of the error.     

Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task.

We investigated the role of the superior colliculus (SC) in saccade target selection while macaque monkeys performed a direction-discrimination task. The monkeys selected one of two possible saccade targets based on the direction of motion in a stochastic random-dot display; the difficulty of the task was varied by adjusting the strength of the motion signal in the display. One of the two saccade targets was positioned within the movement field of the SC neuron under study while the other target was positioned well outside the movement field. Approximately 30% of the neurons in the intermediate and deep layers of the SC discharged target-specific preludes of activity that "predicted" target choices well before execution of the saccadic eye movement. Across the population of neurons, the strength of the motion signal in the display influenced the intensity of this "predictive" prelude activity: SC activity signaled the impending saccade more reliably when the motion signal was strong than when it was weak. The dependence of neural activity on motion strength could not be explained by small variations in the metrics of the saccadic eye movements. Predictive activity was particularly strong in a subpopulation of neurons with directional visual responses that we have described previously. For a subset of SC neurons, therefore, prelude activity reflects the difficulty of the direction discrimination in addition to the target of the impending saccade. These results are consistent with the notion that a restricted network of SC neurons plays a role in the process of saccade target selection.     

Evidence that the superior colliculus participates in the feedback control of saccadic eye movements

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17 degrees. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.     

Target selection and saccade generation in monkey superior colliculus

The superior colliculus (SC) of the monkey has been shown to be involved in not only initiation of saccades but in the selection of the target to which the saccade can be directed. The present experiments examine whether SC neuronal activity related to target selection is also related to saccade generation. In an asynchronous target task, the monkey was required to make a saccade to the first of two spots of light to appear. Using choice probability analysis over multiple trials, we determined the earliest time at which neurons in the SC intermediate layers indicated target selection. We then determined how closely the neuronal selection was correlated to saccade onset by using our asynchronous reaction time task, which allowed the monkey to make a saccade to the target as soon as the selection had been made. We found that the selection became evident at widely differing times for different neurons. Some neurons indicated target selection just before the saccade (close to the pre-saccadic burst of activity), others did so at the time of the visual response, and some showed an increase in their activity even before the target appeared. A fraction of this pre-stimulus bias resulted from a priming effect of the previous trial; a saccade to the target in the movement field on the previous trial produced both a higher level of neuronal activity and a higher probability for a saccade to that target on the current trial. We found that most of the neurons (76%) showed a correlation between selection time and reaction time. Furthermore, within this 76% of neurons, many indicated a selection very early during the visual response. There was no evidence of a sequence from target selection first and saccade selection later, but rather that target selection and saccade initiation are intertwined and are probably inseparable.     

Evidence against a moving hill in the superior colliculus during saccadic eye movements in the monkey

Saccadic eye movements of different sizes and directions are represented in an orderly topographic map across the intermediate and deep layers of the superior colliculus (SC), where large saccades are encoded caudally and small saccades rostrally. Based on experiments in the cat, it has been suggested that saccades are initiated by a hill of activity at the caudal site appropriate for a particular saccade. As the saccade evolves and the remaining distance to the target, the motor error, decreases, the hill moves rostrally across successive SC sites responsible for saccades of increasingly smaller amplitudes. When the hill reaches the "fixation zone" in the rostral SC, the saccade is terminated. A moving hill of activity has also been posited for the monkey, in which it is supposed to be transported via so-called build-up neurons (BUNs), which have a prelude of activity that culminates in a burst for saccades. However, several studies using a variety of approaches have yet to provide conclusive evidence for or against a moving hill. The moving hill scenario predicts that during a large saccade the burst of a BUN in the rostral SC will be delayed until the motor error remaining in the evolving saccade is equal to the saccadic amplitude for which that BUN discharges best, i.e., its optimal amplitude. Therefore a plot of the burst lead preceding the "optimal" motor error against the time of occurrence of the optimal motor error should have a slope of zero. A slope of -1 indicates no moving hill. For our 20 BUNs, we used three measures of burst timing: the leads to the onset, peak, and center of the burst. The average slopes of these relations were -1.09, -0.79, and -0.58, respectively. For individual BUNs, the slopes of all three relations always differed significantly from zero. Although the peak and center leads fall between -1 and 0, a hill of activity moving rostrally at a rate indicated by either of these slopes would arrive at the fixation zone much too late to terminate the saccade at the appropriate time. Calculating our same three timing measures from averaged data leads us to the same conclusion. Thus our data do not support the moving hill model. However, we argue in the DISCUSSION that the constant lead of the burst onset relative to saccade onset (approximately 27 ms) suggests that the BUNs may help to trigger the saccade.     

Role of the rostral superior colliculus in active visual fixation and execution of express saccades.

1. In the rostral pole of the monkey superior colliculus (SC) a subset of neurons (fixation cells) discharge tonically when a monkey actively fixates a target spot and pause during the execution of saccadic eye movements. 2. To test whether these fixation cells are necessary for the control of visual fixation and saccade suppression, we artificially inhibited them with a local injection of muscimol, an agonist of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). After injection of muscimol into the rostral pole of one SC, the monkey was less able to suppress the initiation of saccades. Many unwanted visually guided saccades were initiated less than 100 ms after onset of a peripheral visual stimulus and therefore fell into the range of express saccades. 3. We propose that fixation cells in the rostral SC form part of a fixation system that facilitates active visual fixation and suppresses the initiation of unwanted saccadic eye movements. Express saccades can only occur when activity in this fixation system is reduced.     

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.     

Expression of a re-centering bias in saccade regulation by superior colliculus neurons

In previous studies of saccadic eye movement reaction time, the manipulation of initial eye position revealed a behavioral bias that facilitates the initiation of movements towards the central orbital position. An interesting hypothesis for this re-centering bias suggests that it reflects a visuo-motor optimizing strategy, rather than peripheral muscular constraints. Given that the range of positions that the eyes can take in the orbits delimits the extent of visual exploration by head-fixed subjects, keeping the eyes centered in the orbits may indeed permit flexible orienting responses to engaging stimuli. To investigate the influence of initial eye position on central processes such as saccade selection and initiation, we examined the activity of saccade-related neurons in the primate superior colliculus (SC). Using a simple reaction time paradigm wherein an initially fixated visual stimulus varying in position was extinguished 200 ms before the presentation of a saccadic target, we studied the relationship between initial eye position and neuronal activation in advance of saccade initiation. We found that the magnitude of the early activity of SC neurons, especially during the immediate pre-target period that followed the fixation stimulus disappearance, was correlated with changes in initial eye position. For the great majority of neurons, the pre-target activity increased with changes in initial eye position in the direction opposite to their movement fields, and it was also strongly correlated with the concomitant reduction in reaction time of centripetal saccades directed within their movement fields. Taking into account the correlation with saccadic reaction time, the relationship between neuronal activity and initial eye position remained significant. These results suggest that eye-position-dependent changes in the excitability of SC neurons could represent the neural substrate underlying a re-centering bias in saccade regulation. More generally, the low frequency SC pre-target activity could use eccentric eye position signals to regulate both when and which saccades are produced by promoting the emergence of a high frequency burst of activity that can act as a saccadic command. However, only saccades initiated within ~200 ms of target presentation were associated with SC pre-target activity. This eye-dependent pre-target activation mechanism therefore appears to be restricted to the initiation of saccades with relatively short reaction times, which specifically require the integrity of the SC. Electronic Publication     

Multisensory interactions in saccade target selection: Curved saccade trajectories

In a series of experiments, we examined the change in saccade trajectories observed when distractors are presented at non-target locations. The primary aim of the experiments was to examine multisensory interaction effects between the visual, auditory and somatosensory modalities in saccade generation. In each experiment observers made saccades to visual targets above and below fixation in the presence of visual, auditory or tactile stimuli to the left or right of fixation. In experiment 1 distractor location indicated which of two stimuli was the target for the saccade. Saccade trajectories showed strong leftward curvature following right-side distractors and showed rightward curvature following left-side distractors. The largest effects on trajectories were observed for visual distractors, but significant curvature was observed with auditory and somatosensory distractors. In experiment 2 saccades were made following the onset of a visual target (reflexive) or following presentation of an arrow at fixation (voluntary), and task-irrelevant crossmodal distractors were presented simultaneously with target onset. Both voluntary and reflexive saccades were found to curve away from task-irrelevant visual distractors, but auditory and somatosensory distractors did not modulate saccade trajectories. In experiment 3 task-irrelevant distractors preceded the onset of the target by 100 ms. Reflexive saccades were found to curve away from visual, auditory and somatosensory distractors, but voluntary saccades curved away from visual distractors only. The modulation of saccade trajectories by distractors from different modalities is interpreted in terms of inhibitory processes operating in neural structures involved in saccade generation. Our findings suggest that visual, auditory and somatosensory distractors can all modulate saccade trajectories. Such effects could be related to the inhibition of populations of neurons, in a common motor map, for the selection of a saccade target.     

Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal

1. We studied the activity of single neurons in the monkey frontal eye fields during oculomotor tasks designed to assess the activity of these neurons when there was a dissonance between the spatial location of a target and its position on the retina. 2. Neurons with presaccadic activity were first studied to determine their receptive or movement fields and to classify them as visual, visuomovement, or movement cells with the use of the criteria described previously (Bruce and Goldberg 1985). The neurons were then studied by the use of double-step tasks that dissociated the retinal coordinates of visual targets from the dimensions of saccadic eye movements necessary to acquire those targets. These tasks required that the monkeys make two successive saccades to follow two sequentially flashed targets. Because the second target disappeared before the first saccade occurred, the dimensions of the second saccade could not be based solely on the retinal coordinates of the target but also depended on the dimensions of the first saccade. We used two versions of the double-step task. In one version neither target appeared in the cell's receptive or movement field, but the second eye movement was the optimum amplitude and direction for the cell (right-EM/wrong-RF task). In the other the second stimulus appeared in the cell's receptive field, but neither eye movement was appropriate for the cell (wrong-EM/right-RF task). 3. Most frontal-eye-field cells discharged in the right-EM/wrong-RF version of the double-step task. Their discharge began after the first saccade and continued until the second saccade was made. They usually discharged even on occasional trials in which the monkey failed to make the second saccade. They discharged much less, or not at all, in the wrong-EM/right-RF version of the double-step paradigm. Thus most presaccadic cells in the frontal eye fields were tuned to the dimensions of saccadic eye movements rather than to the coordinates of retinal stimulation. 4. Eleven movement cells (including 1 which also had independent postsaccadic activity for saccades opposite its presaccadic movement field) were studied, and all had significant activity in the right-EM/wrong-RF task. 5. Almost all (28/32) visuomovement cells, including 12 with independent postsaccadic activity, discharged in the right-EM/wrong-RF task. None of the four that failed had independent postsaccadic activity. 6. The majority (26/40) of visual cells were responsive in the right-EM/wrong-RF task.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

Discharge properties of monkey tectoreticular neurons

The intermediate layers of the superior colliculus (SC) contain neurons that clearly play a major role in regulating the production of saccadic eye movements: a burst of activity from saccade neurons (SNs) is thought to provide a drive signal to set the eyes in motion, whereas the tonic activity of fixation neurons (FNs) is thought to suppress saccades during fixation. The exact contribution of these neurons to saccade control is, however, unclear because the nature of the signals sent by the SC to the brain stem saccade generation circuit has not been studied in detail. Here we tested the hypothesis that the SC output signal is sufficient to control saccades by examining whether antidromically identified tectoreticular neurons (TRNs: 33 SNs and 13 FNs) determine the end of saccades. First, TRNs had discharge properties similar to those of nonidentified SC neurons and a proportion of output SNs had visually evoked responses, which signify that the saccade generator must receive and process visual information. Second, only a minority of TRNs possessed the temporal patterns of activity sufficient to terminate saccades: Output SNs did not cease discharging at the time of saccade end, possibly continuing to drive the brain stem during postsaccadic fixations, and output FNs did not resume their activity before saccade end. These results argue against a role for SC in regulating the timing of saccade termination by a temporal code and suggest that other saccade centers act to thwart the extraneous SC drive signal, unless it controls saccade termination by a spatial code.     

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     

Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus

Damage to the monkey superior colliculus (SC) produces deficits in the generation of saccadic eye movements. Recovery of the accuracy of saccades is rapid, but saccadic latency and peak velocity recover slowly or not at all. In the present experiments we revisited the issue of recovery of function following localized lesions of the SC using three methodological advances: implantation of wire recording electrodes into the SC for the duration of the experiment to ensure that we were recording from the same site on the SC map on successive days; quantification of changes in saccadic accuracy, latency, and velocity using a standard grid of target points in the visual field contralateral to the SC lesion; measurement of movement field size to quantitatively determine any changes following the lesion. We confirmed a decrease in saccadic accuracy following electrolytic lesions of the SC, and we found that this dysmetria recovered within about 4 days. Saccadic latency increased for saccades to the lesion area and this deficit persisted. Peak saccadic velocity decreased immediately after the lesion and decreased further during the 10 days to 2 weeks of the experiment. We found no indication of an expansion of the movement fields of neurons adjacent to the lesion area. This lack of reorganization suggests that movement field changes within the SC cannot mediate the recovery in accuracy of the saccade. The persistence of the latency and velocity deficits despite the recovery of amplitude deficits indicates that saccadic latency and peak velocity are dependent upon the SC whereas saccadic amplitude is not.     

Functional imaging of the primate superior colliculus during saccades to visual targets

The primate superior colliculus (SC) is a midbrain nucleus crucial for the control of rapid eye movements (saccades). Its neurons are topographically arranged over the rostrocaudal and mediolateral extent of its deeper layers so that saccade metrics (amplitude and direction) are coded in terms of the location of active neurons. We used the quantitative [14C]-deoxyglucose method to obtain a map of the two-dimensional pattern of activity throughout the SC of rhesus monkeys repeatedly executing visually guided saccades of the same amplitude and direction for the duration of the experiment. Increased metabolic activity was confined to a circumscribed region of the two-dimensional reconstructed map of the SC contralateral to the direction of the movement. The precise rostrocaudal and mediolateral location of the area activated depended on saccade metrics. Our data support the notion that the population of active SC cells remains stationary in collicular space during saccades.