Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements

The intermediate and deep layers of the monkey superior colliculus (SC) comprise a retinotopically organized map for eye movements. The rostral end of this map, corresponding to the representation of the fovea, contains neurons that have been referred to as "fixation cells" because they discharge tonically during active fixation and pause during the generation of most saccades. These neurons also possess movement fields and are most active for targets close to the fixation point. Because the parafoveal locations encoded by these neurons are also important for guiding pursuit eye movements, we studied these neurons in two monkeys as they generated smooth pursuit. We found that fixation cells exhibit the same directional preferences during pursuit as during small saccades-they increase their discharge during movements toward the contralateral side and decrease their discharge during movements toward the ipsilateral side. This pursuit-related activity could be observed during saccade-free pursuit and was not predictive of small saccades that often accompanied pursuit. When we plotted the discharge rate from individual neurons during pursuit as a function of the position error associated with the moving target, we found tuning curves with peaks within a few degrees contralateral of the fovea. We compared these pursuit-related tuning curves from each neuron to the tuning curves for a saccade task from which we separately measured the visual, delay, and peri-saccadic activity. We found the highest and most consistent correlation with the delay activity recorded while the monkey viewed parafoveal stimuli during fixation. The directional preferences exhibited during pursuit can therefore be attributed to the tuning of these neurons for contralateral locations near the fovea. These results support the idea that fixation cells are the rostral extension of the buildup neurons found in the more caudal colliculus and that their activity conveys information about the size of the mismatch between a parafoveal stimulus and the currently foveated location. Because the generation of pursuit requires a break from fixation, the pursuit-related activity indicates that these neurons are not strictly involved with maintaining fixation. Conversely, because activity during the delay period was found for many neurons even when no eye movement was made, these neurons are also not obligatorily related to the generation of a movement. Thus the tonic activity of these rostral neurons provides a potential position-error signal rather than a motor command-a principle that may be applicable to buildup neurons elsewhere in the SC.     

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.     

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.     

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.     

Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades

The visual world presents multiple potential targets that can be brought to the fovea by saccadic eye movements. These targets produce activity at multiple sites on a movement map in the superior colliculus (SC), an area of the brain related to saccade generation. The saccade made must result from competition between the populations of neurons representing these many saccadic goals, and in the present experiments we used multiple moveable microelectrodes to follow this competition. We recorded simultaneously from two sites on the SC map where each site was related to a different saccade target. The two targets appeared in rapid sequence, and the monkey was rewarded for making a saccade toward the one appearing first. Our study concentrated on trials in which the monkey made strongly curved saccades that were directed first toward one target and then toward the other. These curved saccades activated both sites on the SC map as they veered from one target to the other. The major finding was that the strongly curved saccades were preceded by sequential activity in the two neurons as indicated by three observations: the firing rate for the neuron related to the first target reached its peak earlier than did the rate of the neuron for the second target; the timing of the peak activity of the two neurons was related to the beginning and end of the saccade curvature; a weighted vector-average model based on the activity of the two neurons predicted the timing of saccade curvature. Straight averaging saccades ended between the targets so that they did not go to either target, and they were accompanied by simultaneous rather than sequential activation of the two neurons. Thus when multiple populations of neurons are active on the SC movement map, the resulting saccade is determined by the relative timing of the activity in the populations as well as their magnitude. In contrast, SC activity at the two sites did not predict the final direction of the saccade, and several control experiments found insufficient activity at other sites on the SC map to account for that final direction. We conclude that the SC neuronal activity predicts the timing of the saccade curvature, but not the final direction of the trajectory. These observations are consistent with SC activity being critical in selecting the goal of the saccade, but not in determining the exact trajectory.     

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.     

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)     

Activity in deep intermediate layer collicular neurons during interrupted saccades

The activity of neurons located in the deep intermediate and adjacent deep layers (hereafter called just deep intermediate layer neurons) of the superior colliculus (SC) in monkeys was recorded during saccades interrupted by electrical stimulation of the brainstem omnipause neuron (OPN) region. The goal of the experiment was to determine if these neurons maintained their discharge during the saccadic interruption, and thus, could potentially provide a memory trace for the intended movement which ends accurately on target in spite of the perturbation. The collicular neurons recorded in the present study were located in the rostral three-fifths of the colliculus. Most of these cells tended to show considerable presaccadic activity during a delayed saccade paradigm, and, therefore, probably overlap with the population of SC cells called buildup neurons or prelude bursters in previous studies. The effect of electrical stimulation in the OPN region (which interrupted ongoing saccades) on the discharge of these neurons was measured by computing the percentage reduction in a cell's activity compared to that present during non-interrupted saccades. During saccade interruption about 70% of deep intermediate layer neurons experienced a major reduction (30% or greater) in their activity, but discharge recovered quickly after the termination of the stimulation as the eyes resumed their movement to finish the saccade on the target. Therefore, the pattern of activity recorded in most of the deep intermediate layer neurons during interrupted saccades qualitatively resembled that previously reported for the saccade-related burst neurons which tend to be located more dorsally in the intermediate layer. In contrast, some of our cells (30%) showed little or no perturbation in their activity caused by the saccade interrupting stimulation. Because all the more dorsally located burst neurons and the majority of our deep intermediate layer neurons show a total or major suppression in their discharge during interrupted saccades, it seems unlikely that the colliculus by itself could maintain an accurate memory of the desired saccadic goal or the remaining dynamic motor error required to account for the accuracy of the resumed movement which occurs following the interruption. However, it remains possible that the smaller proportion of our neurons whose activity was not perturbed during interrupted movements could play a role in the mechanisms underlying saccade accuracy in the interrupted saccade paradigm. Interrupted saccades have longer durations than normal saccades to the same target. Therefore, we investigated whether the discharge of our deeper collicular cells was also necessarily prolonged during interrupted saccades, and, if so, how the prolongation compared to the prolongation of the saccade. Sixty percent of our sample neurons showed a prolongation in discharge that was approximately the same as the prolongation in saccade duration (difference < 15 ms in magnitude). The, observation that temporal discharge in our neurons was perturbed to roughly match saccadic temporal perturbation suggests that dynamic feedback about ongoing saccadic motion is provided to the colliculus, but does not necessarily imply that this structure is the site responsible for the computation of dynamic motor error.     

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.     

Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence

It has long been believed that the superior colliculus (SC) is involved in the production of saccades but plays no role in the generation of vergence eye movements. However, results from several recent studies suggest that it may be worthwhile to examine the role of the SC in saccade-vergence interactions. Specifically, the available literature suggests two questions: do saccade-related neurons in SC have three-dimensional movement fields and is the slowing of saccades by vergence attributable, in part, to changes in the level of activity in SC? Single-unit data were recorded from 51 saccade-related neurons in rhesus monkey SC during saccades without vergence, saccades accompanied by convergence, and saccades accompanied by divergence. Most cells (78% for convergence, 86% for divergence) showed a significant reduction in peak spike density when the saccade was accompanied by vergence. A minority of cells (16% for convergence, 2% for divergence) increased their firing rate for saccades accompanied by vergence. Three cells were found that discharged in association with saccades, vergence, and the combination of the two. There were no cells that exhibited the pattern of discharge that would be expected of a cell tuned for saccades with divergence. Thus the present results do not support the hypothesis that saccade-related SC neurons are, as a rule, tuned in three dimensions. Small, but significant, differences in firing rate were often found for saccades without vergence at near and far distances. Approximately half of the cells showed a significant relationship between spike activity and saccade velocity, but the correlations tended to be very weak. This suggests that the decreased neuronal activity of SC neurons has only a limited effect on saccade velocity. For some cells, the movement field shifted for saccades with vergence. These shifts were highly variable from one cell to another.     

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.     

Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus

The caudal superior colliculus (SC) contains movement neurons that fire during saccades and the rostral SC contains fixation neurons that fire during visual fixation, suggesting potentially different functions for these 2 regions. To study whether these areas might have different projections, we characterized synaptic inputs from the rostral and caudal SC to inhibitory burst neurons (IBNs) in anesthetized cats. We recorded intracellular potentials from neurons in the IBN region and identified them as IBNs based on their antidromic activation from the contralateral abducens nucleus and short-latency excitation from the contralateral caudal SC and/or single-cell morphology. IBNs received disynaptic inhibition from the ipsilateral caudal SC and disynaptic inhibition from the rostral SC on both sides. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in IBNs, which was enhanced by preconditioning stimulation of the ipsilateral caudal SC. A midline section between the IBN regions eliminated inhibition from the ipsilateral caudal SC, but inhibition from the rostral SC remained unaffected, indicating that the latter inhibition was mediated by inhibitory interneurons other than IBNs. A transverse section of the brain stem rostral to the pause neuron (PN) region eliminated inhibition from the rostral SC, suggesting that this inhibition is mediated by PNs. These results indicate that the most rostral SC inhibits bilateral IBNs, most likely via PNs, and the more caudal SC exerts monosynaptic excitation on contralateral IBNs and antagonistic inhibition on ipsilateral IBNs via contralateral IBNs. The most rostral SC may play roles in maintaining fixation by inhibition of burst neurons and facilitating saccadic initiation by releasing their inhibition.     

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     

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.     

Commissural excitation and inhibition by the superior colliculus in tectoreticular neurons projecting to omnipause neuron and inhibitory burst neuron regions

Previous electrophysiological studies have shown that the commissural connections between the two superior colliculi are mainly inhibitory with fewer excitatory connections. However, the functional roles of the commissural connections are not well understood, so we sought to clarify the physiology of tectal commissural excitation and inhibition of tectoreticular neurons (TRNs) in the "fixation " and "saccade " zones of the superior colliculus (SC). By recording intracellular potentials, we identified TRNs by their antidromic responses to stimulation of the omnipause neuron (OPN) and inhibitory burst neuron (IBN) regions and analyzed the effects of stimulation of the contralateral SC on these TRNs in anesthetized cats. TRNs in the caudal SC (saccade neurons) projected to the IBN region, and received mono- or disynaptic inhibition from the entire rostrocaudal extent of the contralateral SC. In contrast, TRNs in the rostral SC projected to the OPN or IBN region and received monosynaptic excitation from the most rostral level of the contralateral SC, and mono- or disynaptic inhibition from its entire rostrocaudal extent. Among the rostral TRNs with commissural excitation, IBN-projecting TRNs also projected to Forel's field H (vertical gaze center), suggesting that they were most likely saccade neurons related to vertical saccades. In contrast, TRNs projecting only to the OPN region were most likely fixation neurons. Most putative inhibitory neurons in the rostral SC had multiple axon branches throughout the rostrocaudal extent of the contralateral SC, whereas excitatory commissural neurons, most of which were rostral TRNs, distributed terminals to a discrete region in the rostral SC.     

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.     

Transient pauses in delay-period activity of superior colliculus neurons

A feature of neurons in the mammalian superior colliclus (SC) is the robust discharge of action potentials preceding the onset of rapid eye movements called saccades. The burst, which commands ocular motoneurons, is often preceded by persistent, low-level activity, likely reflecting neuronal processes such as target selection, saccade selection and preparation. Here, we report on a transient pause in persistent activity of SC neurons. We trained monkeys to make or withhold saccades based on the shape of a centrally located cue. We found that after the cue changed shape, there was a measurable pause in persistent activity of SC neurons, even though the cue was located well outside the response field of the neurons. We show here that this pause is not a simple, transient inhibitory drive from neurons representing the central visual field. Rather, the occurrence of the pause depends on the occurrence of saccades made much later in the trial. The characteristics of the pause such as magnitude or duration are not predictable from the task condition, rather the occurrence of the pause across the SC neuronal population varies with whether a saccade is made much later in the trial. We developed a model that accounts for our results and makes testable predictions about the effects of signals related to inhibition in SC neuronal populations.     

Extraretinal inputs to neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements.

The intermediate and deep layers of the monkey superior colliculus (SC) are known to be important for the generation of saccadic eye movements. Recent studies have also provided evidence that the rostral SC might be involved in the control of pursuit eye movements. However, because rostral SC neurons respond to visual stimuli used to guide pursuit, it is also possible that the pursuit-related activity is simply a visual response. To test this possibility, we recorded the activity of neurons in the rostral SC as monkeys smoothly pursued a target that was briefly extinguished. We found that almost all rostral SC neurons in our sample maintained their pursuit-related activity during a brief visual blink, which was similar to the maintained activity they also exhibited during blinks imposed during fixation. These results indicate that discharge of rostral SC neurons during pursuit is not simply a visual response, but includes extraretinal signals.     

Activity changes in monkey superior colliculus during saccade adaptation

Saccades are eye movements that are used to foveate targets rapidly and accurately. Their amplitude must be adjusted continually, throughout life, to compensate for movement inaccuracies due to maturation, pathology, or aging. One possible locus for such saccade adaptation is the superior colliculus (SC), the relay for cortical commands to the premotor brain stem generator for saccades. However, previous stimulation and recording studies have disagreed as to whether saccade adaptation occurs up- or downstream of the SC. Therefore we have reexamined the behavior of SC burst neurons during saccade adaptation under conditions that were optimized to produce the biggest possible change in neuronal activity. We show that behavioral adaptation of saccade amplitude was associated with significant increases or decreases, in the number of spikes in the burst and/or changes in the shape of the movement field in 35 of 43 SC neurons tested. Of the 35, 29 had closed movement fields and 14 were classified indeterminate because the movement field could not be definitively diagnosed. Changes in the number of spikes occurred gradually during adaptation and resulted from correlated changes in burst lead and duration without consistent changes in peak burst rate. These data indicate that the great majority of SC neurons show a change in discharge in association with saccade amplitude adaptation. Based on these and previous results, we speculate that the site for saccade adaptation resides in the SC or that the SC is the final common pathway for adaptive changes that occur elsewhere in the saccade system.