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.

Saccades are rapid eye movements that orient gaze toward areas of interest in the visual scene. Neural activity correlated with saccade target selection has been identified in several brain regions, including the superior colliculus (SC), but it is not known whether the SC is directly involved in target selection, or whether the SC merely receives selection-related signals from cortex in preparation for the execution of eye movements. In monkeys, we used focal reversible inactivation to test the functional contributions of the SC to target selection during visual search, and found that inactivation resulted in clear deficits. When a target appeared in the inactivated field, saccades were often misdirected to distractor stimuli. Control tasks showed that this deficit was not caused by low-level visual or motor impairments. Our results indicate that, in addition to its well-established involvement in movement execution, the SC has an important functional role in target selection.

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.

We provide evidence that the saccadic system can simultaneously program two saccades to different goals. We presented subjects with simple visual search displays in which they were required to make a saccade to an odd-colored target embedded in an array of distractors. When there was strong competition between target and distractor stimuli (due to color priming from previous trials), subjects were more likely to make a saccade to a distractor. Such error saccades were often followed, after a very short inter-saccadic interval ( approximately 10-100 ms), by a second saccade to the target. The brevity of these inter-saccadic intervals suggests that the programming of the two saccades (one to a distractor and one to the target) overlapped in time. Using a saccade-contingent change in the search display, we show that new visual information presented during the initial saccade does not change the goal of the second saccade. This supports the idea that, by the end of the first saccade, programming of the second saccade is already well underway. We also elicited two-saccade responses (similar to those seen in search) using a double-step task, with the first saccade directed to the initial target step and the second saccade directed to the second target step. If the two saccades are programmed in parallel and programming of each saccade is triggered by one of the two target steps, the second saccade should occur at a relatively fixed time after the onset of the second target step, regardless of the timing of the initial saccade. This prediction was confirmed, supporting the idea that the two saccades are programmed in parallel. Finally, we observed that the shortest inter-saccadic intervals typically followed hypometric initial saccades, suggesting that the initial saccade may have been interrupted by the impending second saccade. Using predictions from physiological studies of interrupted saccades, we tested this hypothesis and found that the hypometric initial saccades did not appear to be interrupted in mid-flight. We discuss the significance of our findings for models of the saccadic system.

We performed two sets of experiments in which observers were instructed to make saccades to an odd colored target embedded in an array of distractors. First, we found that when the colors of the target and distractors switched unpredictably from trial to trial (the mixed condition), saccadic latencies decreased with increasing numbers of distractors. In contrast, saccadic latencies were independent of the number of distractors when the color of the target and distractors remained the same on each trial (the blocked condition). This pattern of results mirrors visual search tasks in which focal rather than distributed attention is required (Bravo, M.J., Nakayama, K. (1992). The role of attention in different visual search tasks. Perception and Psychophysics, 51, 465-472.). Second, we found that saccades to an odd target were made more quickly and accurately when the target was the same color as on previous trials than when it changed color. This priming of the target color accumulates across five to seven trials over a period of approximately 30 s. A similar priming effect has been previously shown for the deployment of focal attention (Maljkovic, V., Nakayama, K. (1994). Priming of popout: III. Role of features. Memory and Cognition, 22(6), 657-672.). Thus, we show a close congruence between the pattern of saccadic eye movement latencies and the deployment of focal attention. This supports the view that (1) the execution of saccades requires focal as opposed to distributed attention and that (2) this focal attention is guided by a short term memory system which facilitates the rapid refixation of gaze to recently foveated targets.