Target Selection for Saccadic Eye Movements: Direction-Selective Visual Responses in the Superior Colliculus

2001 ◽  
Vol 86 (5) ◽  
pp. 2527-2542 ◽  
Author(s):  
Gregory D. Horwitz ◽  
William T. Newsome
Keyword(s):  
Superior Colliculus ◽  
Eye Movement ◽  
Discrimination Task ◽  
Visual Motion ◽  
Target Selection ◽  
Small Population ◽  
Saccade Target ◽  
Visual Responses ◽  
Direction Discrimination ◽  
Deep Layers

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 ∼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.

Target Selection for Saccadic Eye Movements: Prelude Activity in the Superior Colliculus During a Direction-Discrimination Task

2001 ◽  
Vol 86 (5) ◽  
pp. 2543-2558 ◽  
Author(s):  
Gregory D. Horwitz ◽  
William T. Newsome
Keyword(s):  
Eye Movements ◽  
Superior Colliculus ◽  
Discrimination Task ◽  
Target Selection ◽  
Saccadic Eye Movements ◽  
Saccade Target ◽  
Visual Responses ◽  
Direction Discrimination ◽  
Motion Signal ◽  
Movement Field

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.

scholarly journals Reversal of a Distractor Effect on Saccade Target Selection After Superior Colliculus Inactivation

2008 ◽  
Vol 99 (5) ◽  
pp. 2694-2702 ◽  
Author(s):  
Robert M. McPeek
Keyword(s):  
Superior Colliculus ◽  
Search Task ◽  
Target Location ◽  
Target Selection ◽  
Saccade Target ◽  
Search Array ◽  
Distractor Effect ◽  
Normal Trend ◽  
Winner Take All ◽  
Take All

Recent evidence indicates that inactivation of the primate superior colliculus (SC) results in an increase in saccade target-selection errors. The pattern of errors suggests that a winner-take-all competition selects the saccade goal and that SC inactivation perturbs this process by biasing the competition against stimuli in the inactivated field. To investigate this idea, the difficulty of target selection was manipulated in a color-oddity search task by varying the number of homogeneous distractors in the search array. Previous studies have shown that target selection is easier when a greater number of homogeneous distractors is present, due to perceptual grouping of the distractors. These results were replicated when testing with the SC intact. Surprisingly, during SC inactivation, this normal trend was reversed: target-selection performance declined significantly with more distractors, resulting in a greater proportion of errant saccades to distractors. Examination of the saccade endpoints indicates that after SC inactivation, many errant saccades were directed to distractors adjacent to the target. This pattern of results suggests that the salience signal used by the SC for target selection is relatively broad in spatial scope. As a result, when the area of the SC representing the target location is inactivated, distractors near the target are at a competitive advantage relative to more distant distractors and, consequently, are selected more often as the saccade goal. This contributes to the trend of worse performance with more distractors due to the greater proximity of distractors to the target.

Representation of an Abstract Perceptual Decision in Macaque Superior Colliculus

2004 ◽  
Vol 91 (5) ◽  
pp. 2281-2296 ◽  
Author(s):  
Gregory D. Horwitz ◽  
Aaron P. Batista ◽  
William T. Newsome
Keyword(s):  
Superior Colliculus ◽  
A Priori ◽  
Small Population ◽  
Delay Period ◽  
Stimulus Motion ◽  
Electrical Microstimulation ◽  
Categorical Representation ◽  
Mnemonic Strategy ◽  
Deep Layers ◽  
Dot Motion

We recorded from neurons in the intermediate and deep layers of the superior colliculus (SC) while monkeys performed a novel direction discrimination task. In contrast to the task we used previously, the new version required the monkey to dissociate perceptual judgments from preparation to execute specific operant saccades. The monkey discriminated between 2 opposed directions of motion in a random-dot motion stimulus and was required to maintain the decision in memory throughout a delay period before the target of the required operant saccade was revealed. We hypothesized that perceptual decisions made in this paradigm would be represented in an “abstract” or “categorical” form within the brain, probably in the frontal cortex, and that decision-related neural activity would be eliminated from spatially organized preoculomotor structures such as the SC. To our surprise, however, a small population of neurons in the intermediate and deep layers of the SC fired in a choice-specific manner early in the trial well before the monkey could plan the operant saccade. Furthermore, the representation of the decision during the delay period appeared to be spatial: the active region in the SC map corresponded to the region of space toward which the perceptually discriminated stimulus motion flowed. Electrical microstimulation experiments suggested that these decision-related SC signals were not merely related to covert saccade planning. We conclude that monkeys may employ, in part, a spatially referenced mnemonic strategy for representing perceptual decisions, even when an abstract, categorical representation might appear more likely a priori.

The effect of a moving distractor on the initiation of smooth-pursuit eye movements

1997 ◽  
Vol 14 (2) ◽  
pp. 323-338 ◽  
Author(s):  
Vincent P. Ferrera ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Visual Motion ◽  
Target Selection ◽  
Motion Processing ◽  
Smooth Pursuit Eye Movements ◽  
Response Preparation ◽  
Pursuit Eye Movements ◽  
Visual Motion Processing

AbstractAs a step toward understanding the mechanism by which targets are selected for smooth-pursuit eye movements, we examined the behavior of the pursuit system when monkeys were presented with two discrete moving visual targets. Two rhesus monkeys were trained to select a small moving target identified by its color in the presence of a moving distractor of another color. Smooth-pursuit eye movements were quantified in terms of the latency of the eye movement and the initial eye acceleration profile. We have previously shown that the latency of smooth pursuit, which is normally around 100 ms, can be extended to 150 ms or shortened to 85 ms depending on whether there is a distractor moving in the opposite or same direction, respectively, relative to the direction of the target. We have now measured this effect for a 360 deg range of distractor directions, and distractor speeds of 5–45 deg/s. We have also examined the effect of varying the spatial separation and temporal asynchrony between target and distractor. The results indicate that the effect of the distractor on the latency of pursuit depends on its direction of motion, and its spatial and temporal proximity to the target, but depends very little on the speed of the distractor. Furthermore, under the conditions of these experiments, the direction of the eye movement that is emitted in response to two competing moving stimuli is not a vectorial combination of the stimulus motions, but is solely determined by the direction of the target. The results are consistent with a competitive model for smooth-pursuit target selection and suggest that the competition takes place at a stage of the pursuit pathway that is between visual-motion processing and motor-response preparation.

Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements

1995 ◽  
Vol 73 (5) ◽  
pp. 1988-2003 ◽  
Author(s):  
M. F. Walker ◽  
E. J. Fitzgibbon ◽  
M. E. Goldberg
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Receptive Fields ◽  
Saccadic Eye Movements ◽  
Superficial Layer ◽  
Saccade Target ◽  
Visual Response ◽  
Intermediate Layers ◽  
Movement Field

1. Previous experiments have shown that visual neurons in the lateral intraparietal area (LIP) respond predictively to stimuli outside their classical receptive fields when an impending saccade will bring those stimuli into their receptive fields. Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. 2. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. 3. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. Each of these neurons did not respond to the stimulus unless an eye movement brought it into its receptive field, nor did it discharge in association with the eye movement unless it brought a stimulus into its receptive field. 4. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. 5. The predictive responses of most of these neurons (16/18, 89%) did not require that the stimulus be relevant to the monkey's rewarded behavior. However, for some neurons the predictive response was enhanced when the stimulus was the target of a subsequent saccade into the neuron's movement field. 6. Most neurons with predictive responses responded with a similar magnitude and latency to a continuous stimulus that remained on after the saccade, and to the same stimulus when it was only flashed for 50 ms coincident with the onset of the saccade target and thus never appeared within the cell's classical receptive field. 7. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Neurons that showed predictive responses began to discharge before the saccade, were suppressed during the saccade, and usually resumed discharging after the saccade. 8. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst. These neurons responded predictively to a stimulus that was going to be the target for a second saccade, but not to an irrelevant flashed stimulus. 9. No superficial layer neuron (0/27) responded predictively when a stimulus would not be brought into their receptive fields by a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

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