Inhibitory tagging both speeds and strengthens saccade target selection in the superior colliculus during visual search.

It has been suggested that, during difficult visual search tasks involving time pressure and multiple saccades, inhibitory tagging helps to facilitate efficient saccade target selection by reducing responses to objects in the scene once they have been searched and rejected. The superior colliculus (SC) is a midbrain structure involved in target selection, and recent findings suggest an influence of inhibitory tagging on SC activity. Precisely how, and by how much, inhibitory tagging influences target selection by SC neurons, however, is unclear. The purpose of this study, therefore, was to characterize and quantify the influence of inhibitory tagging on target selection in the SC. Rhesus monkeys performed a visual search task involving time pressure and multiple saccades. Early in the fixation period between saccades in the context of this task, a subset of SC neurons reliably discriminated the stimulus selected as the next saccade goal, consistent with a role in target selection. Discrimination occurred earlier and was more robust, however, when unselected stimuli in the search array had been previously fixated on the same trial. This indicates that inhibitory tagging both speeds and strengthens saccade target selection in the SC during multisaccade search. The results provide constraints on models of target selection based on SC activity.NEW & NOTEWORTHY An important aspect of efficient behavior during difficult, time-limited visual search tasks is the efficient selection of sequential saccade targets. Inhibitory tagging, i.e., a reduction of neural activity associated with previously fixated objects, may help to facilitate such efficient selection by modulating the selection process in the superior colliculus (SC). In this study, we characterized and quantified this modulation and found that, indeed, inhibitory tagging both speeds and strengthens target selection in the SC.

Inhibitory tagging both speeds and strengthens saccade target selection in the superior colliculus during visual search.

It has been suggested that, during difficult visual search tasks involving time pressure and multiple saccades, inhibitory tagging helps to facilitate efficient saccade target selection by reducing responses to objects in the scene once they have been searched and rejected. The superior colliculus (SC) is a midbrain structure involved in target selection, and recent findings suggest an influence of inhibitory tagging on SC activity. Precisely how, and by how much, inhibitory tagging influences target selection by SC neurons, however, is unclear. The purpose of this study, therefore, was to characterize and quantify the influence of inhibitory tagging on target selection in the SC. Rhesus monkeys performed a visual search task involving time pressure and multiple saccades. Early in the fixation period between saccades, a subset of SC neurons reliably discriminated the stimulus selected as the next saccade goal, consistent with a role in target selection. Discrimination occurred earlier and was more robust, however, when unselected stimuli in the search array had been previously fixated on the same trial. This indicates that inhibitory tagging both speeds and strengthens saccade target selection in the SC during multisaccade search. The results provide constraints on models of target selection based on SC activity.

Inhibitory tagging in the superior colliculus during visual search.

Inhibitory tagging is an important feature of many models of saccade target selection, in particular those that are based on the notion of a neural priority map. The superior colliculus (SC) has been suggested as a potential site of such a map, yet it is unknown whether inhibitory tagging is represented in the SC during visual search. In this study, we tested the hypothesis that SC neurons represent inhibitory tagging during search, as might be expected if they contribute to a priority map. To do so, we recorded the activity of SC neurons in a multisaccade visual-search task. On each trial, a single reward-bearing target was embedded in an array of physically identical, potentially reward-bearing targets and physically distinct, non-reward-bearing distractors. The task was to fixate the reward-bearing target. We found that, in the context of this task, the activity of many SC neurons was greater when their response field stimulus was a target than when it was a distractor and was reduced when it had been previously fixated relative to when it had not. Moreover, we found that the previous-fixation-related reduction of activity was larger for targets than for distractors and decreased with increasing time (or number of saccades) since fixation. Taken together, the results suggest that fixated stimuli are transiently inhibited in the SC during search, consistent with the notion that inhibitory tagging plays an important role in visual search and that SC neurons represent this inhibition as part of a priority map used for saccade target selection.NEW & NOTEWORTHY Searching a cluttered scene for an object of interest is a ubiquitous task in everyday life, which we often perform relatively quickly and efficiently. It has been suggested that to achieve such speed and efficiency an inhibitory-tagging mechanism inhibits saccades to objects in the scene once they have been searched and rejected. Here, we demonstrate that the superior colliculus represents this type of inhibition during search, consistent with its role in saccade target selection.

Motor control: Ready, steady, go!

Neurons governing saccadic eye movements typically multiplex sensory, cognitive, and movement-related signals. How is a reliable 'go' signal extracted from this mixture? A new study reveals that saccade initiation is gated by the temporal stability of rising population activity.

Contextual saccade adaptation induced by sequential saccades.

Saccade adaptation is the gradual adjustment of saccade end point to maintain spatial accuracy. Contextual adaptation refers to a situation in which the adaptation-related change in saccade end point is contingent on the behavioral context in which the saccade is made. For example, in some situations, the same saccade to the same retinotopic location can be simultaneously adapted in opposite directions depending on the context in which it is made. Saccade adaptation has traditionally been studied in isolated movements, but in everyday life, saccades are often planned and executed in sequences. The oculomotor system may therefore have adaptive mechanisms specific to sequential saccades. Here, in five experiments, we investigated contextual saccade adaptation in sequences of saccades. In the first experiment, we demonstrate that saccades to a given retinotopic location can be simultaneously adapted in opposite directions depending on whether they occur in isolation or in a sequence. In the other experiments, we measured the extent to which properties of the previous and following saccades in a sequence can induce contextual saccade adaptation. Overall, we find that the existence, direction, and amplitude of previous and subsequent saccades, as well as the order of the current saccade within a movement sequence, can all induce contextual adaptation. These novel findings demonstrate the surprising flexibility of the system in maintaining end point accuracy, and support the idea that saccades made in a movement sequence are planned concurrently rather than independently.NEW & NOTEWORTHY This study reveals a new type of contextual saccade adaptation: sequential saccades are able to induce contextual saccade adaptation when direction, amplitude, or the existence of preceding and following saccades are used as contexts. These novel findings are also consistent with the idea that saccades made in a sequence are planned concurrently rather than independently.

Role of the Superior Colliculus in Guiding Movements Not Made by the Eyes.

The superior colliculus (SC) has long been associated with the neural control of eye movements. Over seventy years ago, the orderly topography of saccade vectors and corresponding visual field locations were discovered in the cat SC. Since then, numerous high-impact studies have investigated and manipulated the relationship between visuotopic space and saccade vector across this topography to better understand the physiological underpinnings of the sensorimotor signal transformation. However, less attention has been paid to the other motor responses that may be associated with SC activity, ranging in complexity from concerted movements of skeletomotor muscle groups, such as arm-reaching movements, to behaviors that involve whole-body movement sequences, such as fight-or-flight responses in murine models. This review surveys these more complex movements associated with SC (optic tectum in nonmammalian species) activity and, where possible, provides phylogenetic and ethological perspective.

Microsaccades and attention in a high-acuity visual alignment task.

While aiming and shooting, we make tiny eye movements called microsaccades that shift gaze between task-relevant objects within a small region of the visual field. However, in the brief period before pressing the trigger, microsaccades are suppressed. This might be due to the lack of a requirement to shift gaze as the retinal images of the two objects begin to overlap on the fovea. Alternatively, we might actively suppress microsaccades to prevent any disturbances in visual perception caused by microsaccades around the time of their occurrence and their subsequent effect on shooting performance. In this study we looked at microsaccade rates while participants performed a simulated shooting task under two conditions: a normal condition in which they moved their eyes freely, and an eccentric condition in which they maintained gaze on a fixed target while performing the shooting task at 5° eccentricity. As expected, microsaccade rate dropped near the end of the task in the normal viewing condition. However, we also found the same decrease for the eccentric condition in which microsaccades did not shift gaze between the task objects. Microsaccades are also produced in response to shifts in covert attention. To test whether disengagement of covert attention from the eccentric shooting location caused the drop in microsaccade rate, we monitored the location of participants' spatial attention by using a Rapid Serial Visual Presentation (RSVP) task simultaneously at a location opposite to the shooting task. Target letter detection at the RSVP location did not improve during the drop in microsaccade rate, suggesting that covert attention was maintained at the shooting task location. We conclude that in addition to their usual gaze-shifting function, microsaccades during fine-acuity tasks might be modulated by cognitive processes other than spatial attention.

Modulation of saccade trajectories during sequential saccades.

The planning and execution of sequential saccades can overlap in time, and abrupt changes in neural activity in the oculomotor system can alter the normal trajectory of saccades. In this study, we analyzed saccade trajectories to assess the combined programming of sequential saccades. In two separate psychophysical experiments, subjects were instructed to make a sequence of two saccades. The results showed modulation of saccade curvature by the direction and amplitude of both the preceding and following saccade: saccade curvature is modulated in the direction of preceding saccades and away from the direction of following saccades. Moreover, larger preceding and following saccades have stronger effects on curvature. These results support the idea that sequential saccades are programmed concurrently. Finally, the amount of saccade curvature is correlated with the deviation of saccade start and end points, and the time of maximum deviation of saccade trajectories is highly consistent in both experiments. Based on this, we propose a novel benefit for the modulation of saccade trajectories by the oculomotor system: minimizing the saccadic error in sequential saccades.NEW & NOTEWORTHY We show that in saccade sequences, saccade trajectory is modulated in the direction of the preceding saccade and away from the following saccade. The magnitude of this effect is correlated with preceding and following saccade amplitude. This confirms that programming of sequential saccades overlaps. Curvature is also correlated with the deviation of saccade start and end points. Thus, we propose a novel benefit for the modulation of saccade trajectories: minimizing end point error in sequential saccades.

Effects of a pretarget distractor on saccade reaction times across space and time in monkeys and humans.

Previous studies have shown that the influence of a behaviorally irrelevant distractor on saccade reaction times (SRTs) varies depending on the temporal and spatial relationship between the distractor and the saccade target. We measured distractor influence on SRTs to a subsequently presented target, varying the spatial location and the timing between the distractor and the target. The distractor appeared at one of four equally eccentric locations, followed by a target (either 50 ms or 200 ms after) at one of 136 different locations encompassing an area of 20° square. We extensively tested two humans and two monkeys on this task to determine interspecies similarities and differences, since monkey neurophysiology is often used to interpret human behavioral findings. Results were similar across species; for the short interval (50 ms), SRTs were shortest to a target presented close to or at the distractor location and increased primarily as a function of the distance from the distractor. There was also an effect of distractor-target direction and visual field. For the long interval (200 ms) the results were inverted; SRTs were longest for short distances between the distractor and target and decreased as a function of distance from distractor. Both SRT patterns were well captured by a two-dimensional dynamic field model with short-distance excitation and long-distance inhibition, based upon known functional connectivity found in the superior colliculus that includes wide-spread excitation and inhibition. Based on these findings, we posit that the different time-dependent patterns of distractor-related SRTs can emerge from the same underlying neuronal mechanisms common to both species.

Neural correlates of target selection for reaching movements in superior colliculus.

We recently demonstrated that inactivation of the primate superior colliculus (SC) causes a deficit in target selection for arm-reaching movements when the reach target is located in the inactivated field (Song JH, Rafal RD, McPeek RM. Proc Natl Acad Sci USA 108: E1433-E1440, 2011). This is consistent with the notion that the SC is part of a general-purpose target selection network beyond eye movements. To understand better the role of SC activity in reach target selection, we examined how individual SC neurons in the intermediate layers discriminate a reach target from distractors. Monkeys reached to touch a color oddball target among distractors while maintaining fixation. We found that many SC neurons robustly discriminate the goal of the reaching movement before the onset of the reach even though no saccade is made. To identify these cells in the context of conventional SC cell classification schemes, we also recorded visual, delay-period, and saccade-related responses in a delayed saccade task. On average, SC cells that discriminated the reach target from distractors showed significantly higher visual and delay-period activity than nondiscriminating cells, but there was no significant difference in saccade-related activity. Whereas a majority of SC neurons that discriminated the reach target showed significant delay-period activity, all nondiscriminating cells lacked such activity. We also found that some cells without delay-period activity did discriminate the reach target from distractors. We conclude that the majority of intermediate-layer SC cells discriminate a reach target from distractors, consistent with the idea that the SC contains a priority map used for effector-independent target selection.

Reprint of: The effects of distractors and spatial precues on covert visual search in macaque. Vision Research, 76, pp. 43-9.

Covert visual search has been studied extensively in humans, and has been used as a tool for understanding visual attention and cueing effects. In contrast, much less is known about covert search performance in monkeys, despite the fact that much of our understanding of the neural mechanisms of attention is based on these animals. In this study, we characterize the covert visual search performance of monkeys by training them to discriminate the orientation of a briefly-presented, peripheral Landolt-C target embedded within an array of distractor stimuli while maintaining fixation. We found that target discrimination performance declined steeply as the number of distractors increased when the target and distractors were of the same color, but not when the target was an odd color (color pop-out). Performance was also strongly affected by peripheral spatial precues presented before target onset, with better performance seen when the precue coincided with the target location (valid precue) than when it did not (invalid precue). Moreover, the effectiveness of valid precues was greatest when the delay between precue and target was short (∼80-100 ms), and gradually declined with longer delays, consistent with a transient component to the cueing effect. Discrimination performance was also significantly affected by prior knowledge of the target location in the absence of explicit visual precues. These results demonstrate that covert visual search performance in macaques is very similar to that of humans, indicating that the macaque provides an appropriate model for understanding the neural mechanisms of covert search.

The effects of distractors and spatial precues on covert visual search in macaque.

Covert visual search has been studied extensively in humans, and has been used as a tool for understanding visual attention and cueing effects. In contrast, much less is known about covert search performance in monkeys, despite the fact that much of our understanding of the neural mechanisms of attention is based on these animals. In this study, we characterize the covert visual search performance of monkeys by training them to discriminate the orientation of a briefly-presented, peripheral Landolt-C target embedded within an array of distractor stimuli while maintaining fixation. We found that target discrimination performance declined steeply as the number of distractors increased when the target and distractors were of the same color, but not when the target was an odd color (color pop-out). Performance was also strongly affected by peripheral spatial precues presented before target onset, with better performance seen when the precue coincided with the target location (valid precue) than when it did not (invalid precue). Moreover, the effectiveness of valid precues was greatest when the delay between precue and target was short (∼80-100 ms), and gradually declined with longer delays, consistent with a transient component to the cueing effect. Discrimination performance was also significantly affected by prior knowledge of the target location in the absence of explicit visual precues. These results demonstrate that covert visual search performance in macaques is very similar to that of humans, indicating that the macaque provides an appropriate model for understanding the neural mechanisms of covert search.

Deficits in reach target selection during inactivation of the midbrain superior colliculus.

Purposive action requires the selection of a single movement goal from multiple possibilities. Neural structures involved in movement planning and execution often exhibit activity related to target selection. A key question is whether this activity is specific to the type of movement produced by the structure, perhaps consisting of a competition among effector-specific movement plans, or whether it constitutes a more abstract, effector-independent selection signal. Here, we show that temporary focal inactivation of the primate superior colliculus (SC), an area involved in eye-movement target selection and execution, causes striking target selection deficits for reaching movements, which cannot be readily explained as a simple impairment in visual perception or motor execution. This indicates that target selection activity in the SC does not simply represent a competition among eye-movement goals and, instead, suggests that the SC contributes to a more general purpose priority map that influences target selection for other actions, such as reaches.

Attentional modulation of fMRI responses in human V1 is consistent with distinct spatial maps for chromatically defined orientation and contrast.

Attending to different stimulus features such as contrast or orientation can change the pattern of neural responses in human V1 measured with fMRI. We show that these pattern changes are much more distinct for colored stimuli than for achromatic stimuli. This is evidence for a classic model of V1 functional architecture in which chromatic contrast and orientation are coded in spatially distinct neural domains, while achromatic contrast and orientation are not.

The eye dominates in guiding attention during simultaneous eye and hand movements.

Prior to the onset of a saccade or a reach, attention is directed to the goal of the upcoming movement. However, it remains unknown whether attentional resources are shared across effectors for simultaneous eye and hand movements. Using a 4-AFC shape discrimination task, we investigated attentional allocation during the planning of a saccade alone, reach alone, or combined saccade and reach to one of five peripheral locations. Target discrimination was better when the probe appeared at the goal of the impending movement than when it appeared elsewhere. However, discrimination performance at the movement goal was not better for combined eye-hand movements compared to either effector alone, suggesting a shared limited attentional resource rather than separate pools of effector-specific attention. To test which effector dominates in guiding attention, we then separated eye and hand movement goals in two conditions: (1) cued reach/fixed saccade--subjects made saccades to the same peripheral location throughout the block, while the reach goal was cued and (2) cued saccade/fixed reach--subjects made reaches to the same location, while the saccade goal was cued. For both conditions, discrimination performance was consistently better at the eye goal than the hand goal. This indicates that shared attentional resources are guided predominantly by the eye during the planning of eye and hand movements.

Attentional cueing at the saccade goal, not at the target location, facilitates saccades.

Presenting a behaviorally irrelevant cue shortly before a target at the same location decreases the latencies of saccades to the target, a phenomenon known as exogenous attention facilitation. It remains unclear whether exogenous attention interacts with early, sensory stages or later, motor planning stages of saccade production. To distinguish between these alternatives, we used a saccadic adaptation paradigm to dissociate the location of the visual target from the saccade goal. Three male and four female human subjects performed both control trials, in which saccades were made to one of two target eccentricities, and adaptation trials, in which the target was shifted from one location to the other during the saccade. This manipulation adapted saccades so that they eventually were directed to the shifted location. In both conditions, a behaviorally irrelevant cue was flashed 66.7 ms before target appearance at a randomly selected one of seven positions that included the two target locations. In control trials, saccade latencies were shortest when the cue was presented at the target location and increased with cue-target distance. In contrast, adapted saccade latencies were shortest when the cue was presented at the adapted saccade goal, and not at the visual target location. The dynamics of adapted saccades were also altered, consistent with prior adaptation studies, except when the cue was flashed at the saccade goal. Overall, the results suggest that attentional cueing facilitates saccade planning rather than visual processing of the target.

Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production.

Most visual scenes are complex and crowded, with several different objects competing for attention and action. Thus a complete understanding of the production of goal-directed actions must incorporate the higher-level process of target selection. To examine the neural substrates of target selection for visually guided reaching, we recorded the activity of isolated neurons in the dorsal premotor area (PMd) of monkeys performing a reaction-time visual search task. In this task, monkeys reached to an odd-colored target presented with three distractors. We found that PMd neurons typically discriminate the target before movement onset, ∼150-200 ms after the appearance of the search array. In one subset of neurons, discrimination occurred at a consistent time after search array onset regardless of when the reaching movement occurred, suggesting that these neurons are involved in target selection. In a second group of neurons, discrimination time depended on reach reaction time, consistent with involvement in movement production but not in target selection. To look for physiological corroboration of these two functionally defined groups, we analyzed the extracellular spike waveforms of recorded neurons. This analysis showed a population of neurons with narrow action potentials that carried signals related to target selection. A second population with broader action potentials was more heterogeneous, with some neurons showing activity related to target selection and others showing only movement production activity. These results suggest that PMd contains signals related to target selection and movement execution and that different signals are carried by distinct neural subpopulations.

Eye-hand coordination during target selection in a pop-out visual search.

We examined the coordination of saccades and reaches in a visual search task in which monkeys were rewarded for reaching to an odd-colored target among distractors. Eye movements were unconstrained, and monkeys typically made one or more saccades before initiating a reach. Target selection for reaching and saccades was highly correlated with the hand and eyes landing near the same final stimulus both for correct reaches to the target and for incorrect reaches to a distractor. Incorrect reaches showed a bias in target selection: they were directed to the distractor in the same hemifield as the target more often than to other distractors. A similar bias was seen in target selection for the initial saccade in correct reaching trials with multiple saccades. We also examined the temporal coupling of saccades and reaches. In trials with a single saccade, a reaching movement was made after a fairly stereotyped delay. In multiple-saccade trials, a reach to the target could be initiated near or even before the onset of the final target-directed saccade. In these trials, the initial trajectory of the reach was often directed toward the fixated distractor before veering toward the target around the time of the final saccade. In virtually all cases, the eyes arrived at the target before the hand, and remained fixated until reach completion. Overall, these results are consistent with flexible temporal coupling of saccade and reach initiation, but fairly tight coupling of target selection for the two types of action.

Differential influence of attention on gaze and head movements.

A salient peripheral cue can capture attention, influencing subsequent responses to a target. Attentional cueing effects have been studied for head-restrained saccades; however, under natural conditions, the head contributes to gaze shifts. We asked whether attention influences head movements in combined eye-head gaze shifts and, if so, whether this influence is different for the eye and head components. Subjects made combined eye-head gaze shifts to horizontal visual targets. Prior to target onset, a behaviorally irrelevant cue was flashed at the same (congruent) or opposite (incongruent) location at various stimulus-onset asynchrony (SOA) times. We measured eye and head movements and neck muscle electromyographic signals. Reaction times for the eye and head were highly correlated; both showed significantly shorter latencies (attentional facilitation) for congruent compared with incongruent cues at the two shortest SOAs and the opposite pattern (inhibition of return) at the longer SOAs, consistent with attentional modulation of a common eye-head gaze drive. Interestingly, we also found that the head latency relative to saccade onset was significantly shorter for congruent than that for incongruent cues. This suggests an effect of attention on the head separate from that on the eyes.

Reversal of a distractor effect on saccade target selection after superior colliculus inactivation.

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.