Saccade target selection in the superior colliculus during a visual search task

Because real-world scenes typically contain many different potential objects of interest, selecting one goal from many is clearly a fundamental problem faced by the saccadic system. We recorded from visual, movement, and visuo-movement (VM) neurons in the superior colliculus (SC) of monkeys performing a reaction-time visual-search task requiring them to make saccades to an odd-colored target presented with distractors. First, we compared the responses of SC neurons in search with their responses when a single target was presented without distractors (single-stimulus task). Consistent with earlier reports, initial visual activity was smaller in search than in the single-stimulus task, while movement-related activity in the two tasks was comparable. Further experiments showed that much of the reduction in the initial visual response during search was due to lateral inhibition, although a top-down task-related component was also evident. Although the initial visual activity did not discriminate the target from the distractors, some neurons showed a biphasic pattern of visual activity. In VM burst neurons, the second phase of this activity was significantly larger when the target, rather than a distractor, was in the response field. We traced the time course of target/distractor discrimination using receiver operating characteristic (ROC) analysis and found that VM burst neurons, VM prelude neurons, and pure movement neurons discriminated the target from distractors before saccade onset but that phasic and tonic pure visual neurons did not. We also examined the relationship between target/distractor discrimination time and saccade latency. Discrimination in VM burst neurons having a biphasic pattern of visual activity and in many VM prelude neurons occurred after a consistent delay that did not depend on saccade latency, suggesting that these neurons are involved in target selection as well as movement initiation. In contrast, VM burst neurons lacking a biphasic pattern of visual activity, pure movement neurons, and a subset of VM prelude neurons discriminated the target at a time that was well correlated with saccade latency, suggesting that this latter group of neurons is involved in triggering movement execution but not in target selection. Thus a mix of signals likely related to target selection and movement initiation co-exists in different groups of SC neurons. This suggests that certain types of SC neurons participate in the target selection process and that the SC as a whole represents a gateway for target selection signals to be converted into a saccadic command.     

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.     

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.     

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.     

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.     

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.     

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     

Symbolic cue-driven activity in superior colliculus neurons in a peripheral visual choice task

Recent evidence implicates the superior colliculus (SC) in cognitive processes, such as target selection and control of spatial attention, in addition to the execution of saccadic eye movements. We report here the presence of a cognitive response in some cells in the SC in a task that requires the long-term association of spatial location with an arbitrary color. In this study, using a visual choice response task, we demonstrate that visuomotor neurons in the SC were activated by the appearance of a central symbolic cue delivered outside of the visual response fields of the recorded neurons. This procedure ensures that cognitively generated activity in these SC cells is not confounded with modulation of activity from previous visual stimuli that appeared in the response field of the neurons. The experiments suggest that cognitive signals can activate SC cells by themselves instead of only being able to modulate activities already evoked by visual events. Furthermore, a substantial fraction of these cells accurately reflected cue-aligned target selection in advance of saccade initiation. Our results add further support to other studies that have demonstrated that internally generated signals exist in SC cells.     

Search target selection in monkey prefrontal cortex

To explore a visual scene, the brain must detect an object of interest and direct the eyes to it. To investigate the brain's mechanism of saccade target selection, we trained monkeys to perform a visual search task with a response delay and recorded neuronal activity in the prefrontal (PF) cortex. Even though the monkey was not allowed to express its choice until after a delay, the response field of a class of PF neurons was able to differentiate between target and distractors from the very beginning of their response (135 ms). Strong responses were obtained only when the target was presented at the field. Neurons responded much less during a nonsearch task in which saccade target was presented alone in this response field. These results suggest that the PF cortex may be involved in the decision-making process and the focal attention for saccade target selection.     

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.     

Temporal processing of saccade targets in parietal cortex area LIP during visual search

We studied whether the lateral intraparietal (LIP) area-a subdivision of parietal cortex anatomically interposed between visual cortical areas and saccade executive centers-contains neurons with activity patterns sufficient to contribute to the active process of selecting saccade targets in visual search. Visually responsive neurons were recorded while monkeys searched for a color-different target presented concurrently with seven distractors evenly distributed in a circular search array. We found that LIP neurons initially responded indiscriminately to the presentation of a visual stimulus in their response fields, regardless of its feature and identity. Their activation nevertheless evolved to signal the search target before saccade initiation: an ideal observer could reliably discriminate the target from the individual activation of 60% of neurons, on average, 138 ms after stimulus presentation and 26 ms before saccade initiation. Importantly, the timing of LIP neuronal discrimination varied proportionally with reaction times. These findings suggest that LIP activity reflects the selection of both the search target and the targeting saccade during active visual search.     

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.     

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

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

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.     

Neuronal activity related to rule and conflict in macaque supplementary eye field

Neuronal activity in macaque supplementary eye field (SEF) is enhanced during performance of the antisaccade task. This could be related to the selection of targets by a difficult rule (move to a location diametrically opposite the cue) or to conflict between the automatic tendency to look at the cue and the voluntary intention to look away. To distinguish between rule- and conflict-based mechanisms of enhancement, we monitored neuronal activity in the SEF during performance of a delayed response task in which monkeys selected saccade targets in response to peripheral visual cues. In spatial trials, the monkey had to select as target the location marked by the cue. In color trials, the monkey had to select as target the location associated with the color of the cue. 'Color-congruent' trials resembled spatial trials in that saccades were directed to the location occupied by the cue. Nevertheless, many SEF neurons were sensitive to the rule being used, with the majority firing more strongly under the color-rule condition. 'Color-incongruent' trials resembled 'color-congruent' trials in that a color rule guided target selection. Nevertheless, many SEF neurons were sensitive to the spatial relation between cue and saccade, with the majority firing more strongly on trials in which they were incongruent. We conclude that neuronal activity in the SEF is enhanced in connection both with the use of a more difficult rule and with conflict.     

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.     

Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus

Many neurons within prefrontal cortex exhibit a tonic discharge between visual stimulation and motor response. This delay activity may contribute to movement, memory, and vision. We studied delay activity sent from the frontal eye field (FEF) in prefrontal cortex to the superior colliculus (SC). We evaluated whether this efferent delay activity was related to movement, memory, or vision, to establish its possible functions. Using antidromic stimulation, we identified 66 FEF neurons projecting to the SC and we recorded from them while monkeys performed a Go/Nogo task. Early in every trial, a monkey was instructed as to whether it would have to make a saccade (Go) or not (Nogo) to a target location, which permitted identification of delay activity related to movement. In half of the trials (memory trials), the target disappeared, which permitted identification of delay activity related to memory. In the remaining trials (visual trials), the target remained visible, which permitted identification of delay activity related to vision. We found that 77% (51/66) of the FEF output neurons had delay activity. In 53% (27/51) of these neurons, delay activity was modulated by Go/Nogo instructions. The modulation preceded saccades made into only part of the visual field, indicating that the modulation was movement-related. In some neurons, delay activity was modulated by Go/Nogo instructions in both memory and visual trials and seemed to represent where to move in general. In other neurons, delay activity was modulated by Go/Nogo instructions only in memory trials, which suggested that it was a correlate of working memory, or only in visual trials, which suggested that it was a correlate of visual attention. In 47% (24/51) of FEF output neurons, delay activity was unaffected by Go/Nogo instructions, which indicated that the activity was related to the visual stimulus. In some of these neurons, delay activity occurred in both memory and visual trials and seemed to represent a coordinate in visual space. In others, delay activity occurred only in memory trials and seemed to represent transient visual memory. In the remainder, delay activity occurred only in visual trials and seemed to be a tonic visual response. In conclusion, the FEF sends diverse delay activity signals related to movement, memory, and vision to the SC, where the signals may be used for saccade generation. Downstream transmission of various delay activity signals may be an important, general way in which the prefrontal cortex contributes to the control of movement.     

Prefrontal neuronal activity encodes spatial target representations sequentially updated after nonspatial target-shift cues

We examined prefrontal neuronal activity while monkeys performed a sequential target-shift task, in which, after a positional cue indicated the initial saccade target among 8 peripheral positions, the monkeys were required to internally shift the target by one position on every flash of a target-shift cue. The target-shift cue appeared in the center 0 to 3 times within a single trial and was always the same in shape, size, and color. We found selective neuronal activity related to the target position: when the target-shift cue implied the target shift to particular peripheral positions, neurons exhibited early-dominant and late-dominant activity during the following delay period. The early-dominant target-selective activity emerged early in the delay just after the presentation of the target-shift cue, whereas the late-dominant activity gradually built up toward the end of the delay. Because the target-shift cue was not related to any specific target location, the early-dominant target-selective activity could not be a mere visual response to the target-shift cue. We suggest that the early-dominant activity reflects the transitory representation for the saccade target that was triggered by the nonspatial target-shift cue, whereas the late-dominant activity reflects the target representation in the spatial working memory or the preparatory set for the possible impending saccade, being repeatedly updated during sequential target shifts.     

Neuronal activity related to eye-hand coordination in the primate premotor cortex

To test the functional implications of gaze signals that we previously reported in the dorsal premotor cortex (PMd), we trained two rhesus monkeys to point to visual targets presented on a touch screen while controlling their gaze orientation. Each monkey had to perform four different tasks. To initiate a trial, the monkey had to put his hand on a starting position at the center of the touch screen and fixate a fixation point. In one task, the animal had to make a reaching movement to a peripheral target randomly presented at one of eight possible locations on a circle while maintaining fixation at the center of this virtual circle (central fixation + reaching). In the second task, the monkey maintained fixation at the location of the upcoming peripheral target and, later, reached to that location. After a delay, the target was turned on and the monkey made a reaching arm movement (target fixation + reaching). In the third task, the monkey made a saccade to the target without any arm movement (saccade). Finally, in the fourth task, the monkey first made a saccade to the target, then reached to it after a delay (saccade + reaching). This design allowed us to examine the contribution of the oculomotor context to arm-related neuronal activity in PMd. We analyzed the effects of the task type on neuronal activity and found that many cells showed a task effect during the signal (26/60; 43%), set (16/49; 33%) and/or movement (15/54; 28%) epochs, depending on the oculomotor history. These findings, together with previously published data, suggest that PMd codes limb-movement direction in a gaze-dependent manner and may, thus, play an important role in the brain mechanisms of eye-hand coordination during visually guided reaching. Received: 10 September 1998 / Accepted: 19 March 1999     

Direction-selective visual responses in macaque superior colliculus induced by behavioral training

In a previous report, we described a heretofore undetected population of neurons in the intermediate and deep layers of the monkey superior colliculus (SC) that yielded directionally selective visual responses to stimuli presented within the central 4 degrees of the visual field. We observed these neurons in three monkeys that had been extensively trained to perform a visual direction discrimination task in this region of the visual field. The task required the monkeys to report the perceived direction of motion by making a saccadic eye movement to one of two targets aligned with the two possible directions of motion. We hypothesized that these neurons reflect a learned association between visual motion direction and saccade direction formed through extensive training on the direction discrimination task. We tested this hypothesis by searching for direction-selective visual responses in two monkeys that had been trained to perform a similar motion discrimination task in which the direction of stimulus motion was dissociated from the direction of the operant saccade. Strongly directional visual responses were absent in these monkeys, consistent with the notion that extensive training can induce highly specific visual responses in a subpopulation of SC neurons.