Dependence of saccade-related activity in the primate superior colliculus on visual target presence

Neurons in the intermediate layers of the superior colliculus respond to visual targets and/or discharge immediately before and during saccades. These visual and motor responses have generally been considered independent, with the visual response dependent on the nature of the stimulus, and the saccade-related activity related to the attributes of the saccade, but not to how the saccade was elicited. In these experiments we asked whether saccade-related discharge in the superior colliculus depended on whether the saccade was directed to a visual target. We recorded extracellular activity of neurons in the intermediate layers of the superior colliculus of three rhesus monkeys during saccades in tasks in which we varied the presence or absence of a visual target and the temporal delays between the appearance and disappearance of a target and saccade initiation. Across our sample of neurons (n = 64), discharge was highest when a saccade was made to a still-present visual target, regardless of whether the target had recently appeared or had been present for several hundred milliseconds. Discharge was intermediate when the target had recently disappeared and lowest when the target had never appeared during that trial. These results are consistent with the hypothesis that saccade-related discharge decreases as the time between the target disappearance and saccade initiation increases. Saccade velocity was also higher for saccades to visual targets, and correlated on a trial-by-trial basis with perisaccadic discharge for many neurons. However, discharge of many neurons was dependent on task but independent of saccade velocity, and across our sample of neurons, saccade velocity was higher for saccades made immediately after target appearance than would be predicted by discharge level. A tighter relationship was found between saccade precision and perisaccadic discharge. These findings suggest that just as the purpose of the saccadic system in primates is to drive the fovea to a visual target, presaccadic motor activity in the superior colliculus is most intense when such a target is actually present. This enhanced activity may, itself, contribute to the enhanced performance of the saccade system when the saccade is made to a real visual target.     

The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons

The superior colliculus has long been recognized as an important structure in the generation of saccadic displacements of the visual axis. Neurons with presaccadic activity encoding saccade vectors are topographically organized and form a motor map. Recently, neurons with fixation-related activity have been recorded at the collicular rostral pole, at the area centralis representation or fixation area. Another collicular function which deals with the maintenance of fixation behavior by means of active inhibition of orientation commands was then suggested. We tested that hypothesis as it relates to the suppression of gaze saccades (gaze = eye in space = eye in head + head in space) in the head-free cat by increasing the activity of the fixation cells at the rostral pole with electrical microstimulation. Long stimulation trains applied before gaze saccades delayed their initiation. Short stimuli, delivered during the gaze saccades, transiently interrupted both eye and head components. These results provide further support for a role in fixation behavior for collicular fixation neurons. Brainstem omnipause neurons also exhibit fixation-related activity and have been shown to receive a direct excitatory input from the superior colliculus. To determine whether the collicular projection to omnipause neurons arises from the fixation area, the deep layers of the superior colliculus were electrically stimulated either at the rostral pole including the fixation area or in more caudal regions where stimulation evokes orienting responses. Forty-nine neurons were examined in three cats. 61% of the neurons were found to be orthodromically excited by single-pulse stimulation of the rostral pole, whereas only 29% responded to caudal stimulation. In addition, stimuli delivered to the rostral pole activated, on average, omnipause neurons at shorter latencies and with lower currents than those applied in caudal regions. These results suggest that excitatory inputs to omnipause neurons from the superior colliculus are principally provided by the fixation area, via which the superior colliculus could play a role in suppression of gaze shifts.     

Effects of eye position on saccades evoked electrically from superior colliculus of alert cats

Electrical stimulation was carried out in the intermediate and deep gray layers of the superior colliculus in alert cats. The heads of the animals were fixed, and their eye movements were recorded with the scleral search coil method. Stimulation in the anterior two-thirds of the colliculus with long-duration pulse trains produced multiple saccades, as in the primate (45, 51), but their directions and amplitudes were influenced significantly by the initial position of the eye. Stimulation in the posterior part of the colliculus evoked saccades that appeared to be "goal-directed," whereas stimulation at the extreme caudal edge of the colliculus yielded centering saccades. These observations confirm previous reports of Roucoux and Crommelinck (48) and Guitton et al. (24). Saccades evoked during bilateral simultaneous stimulation of the superior colliculi were also dependent on the initial position of the eye. At certain relative intensities of stimulation on the two sides, saccades failed to occur when the eye was within a particular part of the oculomotor range. When the eye was outside this region, the same stimuli triggered an eye movement that drove the eye toward the zone of saccade failure. These findings indicate that saccadic commands resulting from focal collicular stimulation in the cat can be modified by information about current eye position. It is not certain where in the brain this occurs or by what neural mechanisms, but a local feedback model of the saccadic control system (46) can account for the main observations. The functional significance of these findings depends in large measure on the degree to which focal collicular stimulation reproduces naturally occurring patterns of neural activity.     

A new local feedback model of the saccadic burst generator

1. To accommodate the finding that the superior colliculus is an important input to the brain stem pathways that generate saccades (the saccadic burst generator), a new model of the burst generator is proposed. Unlike the model of Robinson (61) from which it was derived, the model attempts to match a neural replica of change in eye position, which is the output of the burst generator, to a neural replica of change in target position, which is the output of the colliculus and the input to the model. 2. The elements of the model correspond to neurons known or thought to be associated with the actual primate saccadic burst generator and are mostly connected together in accord with the results of anatomical and physiological experiments. 3. The model was simulated on a digital computer to compare its behavior with that of the actual burst generator under normal and experimental conditions. Simulated peak burst frequency and saccade duration matched that obtained from monkey excitatory burst neurons and inhibitory burst neurons for saccades up to 15 degrees but did not match at larger sizes; stimulation of the omnipause neurons caused an interruption of the saccade, and the saccade resumed at the end of stimulation as in actual data; the model can generate the abnormally long-duration saccades seen under decreased alertness or various pathologies by changing the burst generator inputs and without having to change any properties of the neurons themselves or their connections; a simulated horizontal and vertical burst generator pair connected only through the omnipause neurons can generate realistic oblique saccades. 4. The implications of the model for higher-order control of the saccadic burst generator are discussed.     

Activity of the brain stem omnipause neurons during saccades perturbed by stimulation of the primate superior colliculus

Stimulation of the rostral approximately 2 mm of the superior colliculus (SC) during a large, visual target-initiated saccade produces a spatial deviation of the ongoing saccade and then stops it in midflight. After the termination of the stimulation, the saccade resumes and ends near the location of the flashed target. The density of collicular projections to the omnipause neuron (OPN) region is greatest from the rostral SC and decreases gradually for the more caudal regions. It has been hypothesized that the microstimulation excites the OPNs through these direct connections, and the reactivation of OPNs, which are normally silent during saccades, stops the initial component in midflight by gating off the saccadic burst generator. Two predictions emerge from this hypothesis: 1) for microstimulation triggered on the onset of large saccades, the time from stimulation onset to resumption of OPN discharge should decrease as the stimulation site is moved rostral and 2) the lead time from reactivation of OPNs to the end of the initial saccade on stimulation trials should be equal to the lead time of pause end with respect to the end of control saccades. We tested this hypothesis by recording OPN activity during saccades perturbed by stimulation of the rostral approximately 2 mm of the SC. The distance of the stimulation site from the most rostral extent of the SC and the time of reactivation with respect to stimulation onset were not significantly correlated. The mean lead of reactivation of OPNs relative to the end of the initial component of perturbed saccades (6.5 ms) was significantly less than the mean lead with respect to the end of control (9.6 ms) and resumed saccades (10.4 ms). These results do not support the notion that the excitatory input from SC neurons-in particular, the fixation neurons in the rostral SC-provide the major signal to reactivate OPNs and end saccades. An alternative, conceptual model to explain the temporal sequence of events induced by stimulation of the SC during large saccades is presented. Other OPN activity parameters also were measured and compared for control and stimulation conditions. The onset of pause with respect to resumed saccade onset was larger and more variable than the onset of pause with respect to control saccades, whereas pause end with respect to the end of resumed and control saccades was similar. The reactivated discharge of OPNs during the period between the end of the initial and the onset of the resumed saccades was at least as strong as that following control movements. This latter observation is interpreted in terms of the resettable neural integrator hypothesis.     

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.     

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.     

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.     

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.     

Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus

Neurons in both the lateral intraparietal area (LIP) of the monkey parietal cortex and the intermediate layers of the superior colliculus (SC) are activated well in advance of the initiation of saccadic eye movements. To determine whether there is a progression in the covert processing for saccades from area LIP to SC, we systematically compared the discharge properties of LIP output neurons identified by antidromic activation with those of SC neurons collected from the same monkeys. First, we compared activity patterns during a delayed saccade task and found that LIP and SC neurons showed an extensive overlap in their responses to visual stimuli and in their sustained activity during the delay period. The saccade activity of LIP neurons was, however, remarkably weaker than that of SC neurons and never occurred without any preceding delay activity. Second, we assessed the dependence of LIP and SC activity on the presence of a visual stimulus by contrasting their activity in delayed saccade trials in which the presentation of the visual stimulus was either sustained (visual trials) or brief (memory trials). Both the delay and the presaccadic activity levels of the LIP neuronal sample significantly depended on the sustained presence of the visual stimulus, whereas those of the SC neuronal sample did not. Third, we examined how the LIP and SC delay activity relates to the future production of a saccade using a delayed GO/NOGO saccade task, in which a change in color of the fixation stimulus instructed the monkey either to make a saccade to a peripheral visual stimulus or to withhold its response and maintain fixation. The average delay activity of both LIP and SC neuronal samples significantly increased by the advance instruction to make a saccade, but LIP neurons were significantly less dependent on the response instruction than SC neurons, and only a minority of LIP neurons was significantly modulated. Thus despite some overlap in their discharge properties, the neurons in the SC intermediate layers showed a greater independence from sustained visual stimulation and a tighter relationship to the production of an impending saccade than the LIP neurons supplying inputs to the SC. Rather than representing the transmission of one processing stage in parietal cortex area LIP to a subsequent processing stage in SC, the differences in neuronal activity that we observed suggest instead a progressive evolution in the neuronal processing for saccades.     

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.     

The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey

Rhesus monkeys were trained to make saccadic eye movements to visual targets using detection and discrimination paradigms in which they were required to make a saccade either to a solitary stimulus (detection) or to that same stimulus when it appeared simultaneously with several other stimuli (discrimination). The detection paradigm yielded a bimodal distribution of saccadic latencies with the faster mode peaking around 100 ms (express saccades); the introduction of a pause between the termination of the fixation spot and the onset of the target (gap) increased the frequency of express saccades. The discrimination paradigm, on the other hand, yielded only a unimodal distribution of latencies even when a gap was introduced, and there was no evidence for short-latency "express" saccades. In three monkeys either the frontal eye field or the superior colliculus was ablated unilaterally. Frontal eye field ablation had no discernible long-term effects on the distribution of saccadic latencies in either the detection or discrimination tasks. After unilateral collicular ablation, on the other hand, express saccades obtained in the detection paradigm were eliminated for eye movements contralateral to the lesion, leaving only a unimodal distribution of latencies. This deficit persisted throughout testing, which in one monkey continued for 9 mo. Express saccades were not observed again for saccades contralateral to the lesion, and the mean latency of the contralateral saccades was longer than the mean latency of the second peak for the ipsiversive saccades. The latency distribution of saccades ipsiversive to the collicular lesion was unaffected except for a few days after surgery, during which time an increase in the proportion of express saccades was evident. Saccades obtained with the discrimination paradigm yielded a small but reliable increase in saccadic latencies following collicular lesions, without altering the shape of the distribution. Unilateral muscimol injections into the superior colliculus produced results similar to those obtained immediately after collicular lesions: saccades contralateral to the injection site were strongly inhibited and showed increased saccadic latencies. This was accompanied by a decrease of ipsilateral saccadic latencies and an increase in the number of saccades falling into the express range. The results suggest that the superior colliculus is essential for the generation of short-latency (express) saccades and that the frontal eye fields do not play a significant role in shaping the distribution of saccadic latencies in the paradigms used in this study.(ABSTRACT TRUNCATED AT 400 WORDS)     

Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys

1. The discharge of 255 neurons in the fastigial nuclei of three trained macaque monkeys was investigated during visually guided saccades. Responses of these neurons were examined also during horizontal head rotation and during microstimulation of the oculomotor vermis (lobules VIc and VII). 2. One hundred and two units were characterized by bursts of firing in response to visually guided saccades. Ninety-eight of these (96.1%) were located within the anatomic confines of the fastigial oculomotor region (FOR), on the basis of reconstruction of recording sites. During contralateral saccades, these neurons showed bursts that preceded the onset of saccades (presaccadic burst), whereas, during ipsilateral saccades, they showed bursts associated with the end of saccades (late saccadic burst). They were hence named saccadic burst neurons. Sixty-one saccadic burst neurons (62.2%) were inhibited during microstimulation of the oculomotor vermis with currents less than 10 microA. 3. All saccadic burst neurons were spontaneously active, and the resting firing rate varied considerably among units, ranging from 10 to 50 imp/s. The tonic levels of activity did not correlate significantly with eye position. 4. The presaccadic burst started 18.5 +/- 4.7 (SD) ms (n = 45) before the onset of saccades in the optimal direction (the direction associated with the maximum values of burst lead time, number of spikes per burst, and burst duration). Optimal directions covered the entire contralateral hemifield, although there was a slightly higher incidence in both horizontal and upper-oblique directions in the present sample. The duration of the presaccadic burst was highly correlated with the duration of saccade (0.85 less than or equal to r less than or equal to 0.97). 5. The late saccadic burst was most robust in the direction opposite to the optimal in each unit (the nonoptimal direction). Its onset preceded the completion of ipsilateral saccade by 30.4 +/- 5.9 ms. The lead time to the end of saccade was consistent among different units and was constant also for saccades of various sizes. Thus the late saccadic burst started even before the saccade onset when the saccade duration was less than 30 ms. Unlike the presaccadic burst, its duration was not related to the duration of saccade. 6. Discharge rates of saccadic burst neurons were correlated neither to eye positions during fixation nor to the initial eye positions before saccades. 7. Eye-position units and horizontal head-velocity units were located rostral to the FOR.(ABSTRACT TRUNCATED AT 400 WORDS)     

Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity

In our previous paper we demonstrated that electrical microstimulation of the fixation area at the rostral pole of the cat superior colliculus (SC) elicits no gaze movement but, rather, transiently suppresses eye-head gaze saccades. In this paper, we investigated the more caudal region of the SC and its interaction with the fixation area. In the alert head-free cat, supra-threshold stimulation in the anterior portion of the SC but outside the fixation area evoked small saccadic shifts of gaze consisting mainly of an eye movement, the head's contribution being small. Stimulating more posteriorly elicited large gaze saccades consisting of an ocular saccade combined with a rapid head movement. At these latter stimulation sites, craniocentric (goal-directed) eye movements were evoked when the cat's head was restrained. The amplitude of eye-head gaze saccades elicited at a particular stimulation site increased with stimulus duration, current strength, and pulse rate, until a constant or unit value was reached. The peak velocity of gaze shifts depended on both pulse rate and current strength. The movement direction was not affected by stimulus parameters. The unit gaze vector evoked, in the head-free condition, by stimulating one collicular site was similar to that coded by efferent neurons recorded at that site, thereby indicating a retinotopically coded gaze error representation on the collicular motor map which is not revealed by stimulating the head-fixed animal. Evoked gaze saccades were found to be influenced by fixation behavior. The amplitude of evoked gaze shifts was reduced if stimulation occurred when the hungry animal fixated a food target. Electrical activation of the collicular fixation area was found to mimic well the effects of natural fixation on evoked gaze shifts. Taken together, our results support the view that the overall distribution and level of collicular activity contributes to the encoding of the metrics of gaze saccades. We suggest that the combined levels of activity at the site being stimulated and at the fixation area influence the amplitude of evoked gaze saccades through competition. When stimulation is at low intensities, fixation-related activity reduces the amplitude of evoked gaze saccades. At high activation levels, the site being stimulated dominates and the gaze vector is specified only by that site's collicular output neurons, from which arises the close correspondence between the unit-evoked gaze saccades and the neurally coded gaze vector at that site.     

Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region

Over the past decade, considerable research efforts have been focused on the role of the rostral superior colliculus (SC) in control of saccades. The most recent theory separates the deeper intermediate layers of the SC into two functional regions: the rostral pole of these layers constitutes a fixation zone and the caudal region comprises the saccade zone. Sustained activity of fixation neurons in the fixation zone is argued to maintain fixation and help prevent saccade generation by exciting the omnipause neurons (OPNs) in the brain stem. This hypothesis is in contrast to the traditional view that the SC contains a topographic representation of the saccade motor map on which the rostral pole of the SC encodes signals for generating small saccades (<2 degrees ) instead of preventing them. There is therefore an unresolved controversy about the specific role on the most rostral region of the SC, and we reexamined its functional contribution by quantifying and comparing spatial and temporal trajectories of 30 degrees saccades perturbed by electrical stimulation of the rostral pole and more caudal regions in the SC and of the OPN region. If the rostral pole serves to preserve fixation, then saccades perturbed by stimulation should closely resemble interrupted saccades produced by stimulation of the OPN region. If it also contributes to saccade generation, then the disrupted movements would better compare with redirected saccades observed after stimulation of the caudal SC. Our experiments revealed two significant findings: 1) the locus of stimulation was the primary factor determining the perturbation effect. If the directions of the target-directed saccade and stimulation-evoked saccade were aligned and if the stimulation was delivered within approximately the rostral 2 mm (<10 degrees amplitude) of SC, the ongoing saccade stopped in midflight but then resumed after stimulation end to reach the original visually specified goal with close to normal accuracy. When stimulation was applied at more caudal sites, the ongoing saccade directly reached the target location without stopping at an intermediate position. If the directions differed considerably, both initial and resumed components were typically observed for all stimulation sites. 2) A quantitative analysis of the saccades perturbed from the fixation zone showed significant deviations from their control spatial trajectories. Thus they resembled redirected saccades induced by caudal SC stimulation and differed significantly from interrupted saccades produced by OPN stimulation. The amplitude of the initial saccade, latency of perturbation, and spatial redirection were greatest for the most caudal sites and decreased gradually for rostral sites. For stimulation sites within the rostral pole of SC, the measures formed a smooth continuation of the trends observed in the saccade zone. As these results argue for the saccade zone concept, we offer reinterpretations of the data used to support the fixation zone model. However, we also discuss scenarios that do not allow an outright rejection of the fixation zone hypothesis.     

Sensorimotor integration in the primate superior colliculus. I. Motor convergence

Orienting movements of the eyes and head are made to both auditory and visual stimuli even though in the primary sensory pathways the locations of auditory and visual stimuli are encoded in different coordinates. This study was designed to differentiate between two possible mechanisms for sensory-to-motor transformation. Auditory and visual signals could be translated into common coordinates in order to share a single motor pathway or they could maintain anatomically separate sensory and motor routes for the initiation and guidance of orienting eye movements. The primary purpose of the study was to determine whether neurons in the superior colliculus (SC) that discharge before saccades to visual targets also discharge before saccades directed toward auditory targets. If they do, this would indicate that auditory and visual signals, originally encoded in different coordinates, have been converted into a single coordinate system and are sharing a motor circuit. Trained monkeys made saccadic eye movements to auditory or visual targets while the activity of visual-motor (V-M) cells and saccade-related burst (SRB) cells was monitored. The pattern of spike activity observed during trials in which saccades were made to visual targets was compared with that observed when comparable saccades were made to auditory targets. For most (57 of 59) V-M cells, sensory responses were observed only on visual trials. Auditory stimuli originating from the same region of space did not activate these cells. Yet, of the 72 V-M and SRB cells studied, 79% showed motor bursts prior to saccades to either auditory or visual targets. This finding indicates that visual and auditory signals, originally encoded in retinal and head-centered coordinates, respectively, have undergone a transformation that allows them to share a common efferent pathway for the generation of saccadic eye movements. Saccades to auditory targets usually have lower velocities than saccades of the same amplitude and direction made to acquire visual targets. Since fewer collicular cells are active prior to saccades to auditory targets, one determinant of saccadic velocity may be the number of collicular neurons discharging before a particular saccade.     

The direct visuo-motor pathway in mammalian superior colliculus; novel perspective on the interlaminar connection

The mammalian superior colliculus (SC) is a center controlling the orienting behaviors such as saccadic eye movements. The superficial layers receive visual inputs and the deeper layers send descending motor command to the brainstem and spinal cord. Existence of the interlaminar connection from the superficial to the deeper layers has been an issue of debate during the last two decades. Recent studies have proved the existence of the interlaminar connection by introducing the in vitro slice preparations. When the collicular circuit is disinhibited from gamma-amino butyric acid A (GABA(A)) receptor-mediated inhibition, the signal transmission through the interlaminar connection is enormously facilitated and neurons in the deeper layers exhibit bursting response to stimulation of the superficial layer with non-linear amplification mechanism that depends on the activation of NMDA-type glutamate receptors. In addition, the cholinergic input to the intermediate layer lowers the threshold for the bursting response and facilitates the transmission through the interlaminar connection via activation of nicotinic receptors. The signal transmission through the interlaminar connection may lead to execution of extremely short latency saccades called express saccades.     

Further evidence that a shared efferent collicular pathway drives separate circuits for smooth eye movements and saccades

The aim of the present study was to find out whether smooth eye movements (SEMs) evoked by superior colliculus (SC) stimulation are, as suggested by Breznen et al. (1996), artefactual eye movements resulting from a non-physiological response of the saccadic generator. This question was reinvestigated in head-restrained cats. Long-lasting SC stimulation was found to evoke, in a comparable proportion, either a single saccade followed by an uninterrupted SEM or a staircase of two or three saccades interleaved with SEMs. These two different patterns of eye movements could be elicited at a near-threshold current and at low stimulation frequencies. In most cases, SEM direction clearly differed from that of the preceding saccade. This difference between SEM and saccade directions varied in a systematic way as a function of the initial saccade direction. As demonstrated by computer simulation, this observation can be explained if the neural circuit controlling SEMs reaches a saturation level earlier than the saccadic burst-generator. Our results in cats were reminiscent of those reported by Breznen et al. (1996) in the monkey only in some instances, when high frequency stimulation (400–600 Hz) was applied. Indeed, in the case of near-threshold stimulation-elicited staircase saccades, increasing the stimulation frequency led to a progressive disappearance of the smaller subsequent saccades that were substituted by uninterrupted SEM-like movements. Altogether, the present results confirm the view that SEMs are genuine eye movements. These results rule out the hypothesis that SEMs result from a saturation of the saccadic generator and strengthen the hypothesis that SEMs and saccades are distinct movements. We suggest that the same collicular efferent cells carry out the motor command to saccadic and SEM circuits and that the position error originating from the SC may be distributed amongst separate downstream motor systems. Electronic Publication     

Collicular ensemble coding of saccades based on vector summation

The superior colliculus in the monkey contains a topographically organized representation of the target in its upper layers and saccade-related activity in its deeper layers. Since collicular movement fields are quite large, a considerable region of the colliculus is active whenever a saccade is made. We have modelled the collicular role in saccade generation based on the idea, proposed earlier in the literature, that each movement cell causes a movement tendency in the direction of the external world point which it represents in the collicular map. The model is organized as follows: An anisotropic logarithmic mapping transforms retinal coordinates into collicular coordinates. A two-dimensional Gaussian function describes the spatial extent of the movement-related activity in the deeper layers. An efferent mapping function specifies how the direction and the size of the movement contribution of each colliculus neuron depends on its location and its firing rate. The total saccade is the vector sum of the individual cell contributions. This very simple model (seven fixed parameters) has been used to simulate metrical properties of saccades: in response to visual targets; in response to electrical stimulation in one colliculus, and after a colliculus lesion. Model performance appears to be remarkably realistic but cannot account for some border effects and responses to double stimulation. Suggestions on how the model can be improved and extended will be presented.     

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.