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 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.

Neurons in FEF Keep Track of Items That Have Been Previously Fixated in Free Viewing Visual Search.

When searching a visual scene for a target, we tend not to look at items or locations we have already searched. It is thought that this behavior is driven by an inhibitory tagging mechanism that inhibits responses on priority maps to the relevant items. We hypothesized that this inhibitory tagging signal should be represented as an elevated response in neurons that keep track of stimuli that have been fixated. We recorded from 231 neurons in the frontal eye field (FEF) of 2 male animals performing a visual foraging task, in which they had to find a reward linked to one of five identical targets (Ts) among five distractors. We identified 38 neurons with activity that was significantly greater when the stimulus in the receptive field had been fixated previously in the trial than when it had not been fixated. The response to a fixated object began before the saccade ended, suggesting that this information is remapped. Unlike most FEF neurons, the activity in these cells was not suppressed during active fixation, had minimal motor responses, and did not change through the trial. Yet using traditional classifications from a memory-guided saccade, they were indistinguishable from the rest of the FEF population. We propose that these neurons keep track of any items that have been fixated within the trial and this signal is propagated by remapping. These neurons could be the source of the inhibitory tagging signal to parietal cortex, where a neuronal instantiation of inhibitory tagging is seen.SIGNIFICANCE STATEMENT When we search a scene for an item, we rarely examine the same location twice. It is thought that this is due to a neural mechanism that keeps track of the items at which we have looked. Here we identified a subset of neurons in the frontal eye field that preferentially responded to items that had been fixated earlier in the trial. These responses were remapped, appearing before the saccade even ended, and were not suppressed during maintained fixation. We propose that these neurons keep track of which items have been examined in search and could be the source of feedback that creates the inhibitory tagging seen in parietal cortex.

Remapping of the environment without corollary discharges: evidence from scene-based IOR.

Previous studies suggested that in order to perceive a stable image of the visual world despite constant eye movements, an efference copy of the oculomotor command is used to remap the representation of the environment in the brain. In two experiments, an inhibitory attentional component (inhibition of return-IOR) was used to examine whether remapping can occur also in the absence of eye movements. Participants were asked to maintain fixation while an unpredictive, attention-grabbing cue appeared and was then followed by a movement of the background image which was artificial (random dots, Experiment 1) or composed of natural scenes (Experiment 2). The participants were then required to respond to a target stimulus that was presented either at the same location as the cue relative to fixation (retinotopic), or at a matching location relative to the background (scene based). In both experiments, an IOR effect was found in scene-based locations immediately after the movement of the background. We suggest that remapping of the inhibitory tagging, which might be a proxy for remapping of the visual scene, could be accomplished rapidly even without the use of an efference copy; the inhibitory tag seems to be anchored to the background image and to move together with it.

Inhibition of return as a foraging facilitator in visual search: Evidence from long-term training.

Inhibition of return (IOR) discourages visual attention from returning to previously attended locations, and has been theorized as a mechanism to facilitate foraging in visual search by inhibitory tagging of inspected items. Previous studies using visual search and probe-detection tasks (i.e., the probe-following-search paradigm) found longer reaction times (RTs) for probes appearing at the searched locations than probes appearing at novel locations. This IOR effect was stronger in serial than parallel search, favoring the foraging facilitator hypothesis. However, evidence for this hypothesis was still lacking because no attempt was made to study how IOR would change when search efficiency gradually improves. The current study employed the probe-following-search paradigm and long-term training to examine how IOR varied following search efficiency improvements across training days. According to the foraging facilitator hypothesis, inhibitory tagging is an after-effect of attentional engagement. Therefore, when attentional engagement in a visual search task is reduced via long-term training, the strength of inhibitory tagging decreases, thus predicting a reduced IOR effect. Consistent with this prediction, two experiments consistently showed that IOR decreased while search efficiency improved through training, although IOR reached the floor more quickly than search efficiency. These findings support the notion that IOR facilitates search performance via stronger inhibitory tagging in more difficult visual search.

The role of the parietal cortex in inhibitory processing in the vertical meridian: Evidence from elderly brain damaged patients.

We explored the effects of parietal damage on inhibitory effects of visuospatial attention, inhibition of return (IOR) and inhibitory tagging (IT), in the vertical meridian. We combined a vertical spatial cue paradigm with a Stroop task employing three different temporal intervals between the spatial cue and the target (700, 1200 and 2000 ms) in two groups of patients, one with damage to the parietal cortex and underlying white matter (the parietal patients group) and the other with damage in other brain areas not including the parietal lobe (the control patient group), and a healthy control group. Healthy controls showed the expected inhibitory effects, IOR at the 700 and 1200 intervals and IT at the 1200 interval (as evidenced in a reduction in the magnitude of Stroop interference at the cued location). On the other hand, only the group of parietal patients showed delayed onset of inhibitory effects, IOR and IT appeared at the 1200 ms and 2000 ms intervals, respectively. These findings provide evidence for a role of the parietal cortex, and the underlying fibre tracts, in inhibitory processing in the vertical meridian, with damage to the parietal cortex altering the time course of attention-dependent inhibition.

Searching Through Alternating Sequences: Working Memory and Inhibitory Tagging Mechanisms Revealed Using the MILO Task.

We used the Multi-Item Localisation (MILO) task to examine search through two sequences. In Sequential blocks of trials, six letters and six digits were touched in order. In Mixed blocks, participants alternated between letters and digits. These conditions mimic the A and B variants of the Trail Making Test (TMT). In both block types, targets either vanished or remained visible after being touched. There were two key findings. First, in Mixed blocks, reaction times exhibited a saw-tooth pattern, suggesting search for successive pairs of targets. Second, reaction time patterns for vanish and remain conditions were identical in Sequential blocks-indicating that participants could ignore past targets-but diverged in Mixed blocks. This suggests a breakdown of inhibitory tagging. These findings may help explain the elevated completion times observed in TMT-B, relative to TMT-A.

Time course of the inhibitory tagging effect in ongoing emotional processing. A HD-tDCS study.

When a cueing procedure that usually triggers inhibition of return (IOR) effects is combined with tasks that tap semantic processing, or involve response-based conflict, an inhibitory tagging (IT) emerges that disrupts responses to stimuli at inhibited locations. IT seems to involve the executive prefrontal cortex, mainly the left dorsolateral prefrontal cortex (DLPFC), in cognitive conflict tasks. Contrary to other inhibitory effects, IT has been observed with rather short intervals, concretely when the stimulus onset asynchrony (SOA) between the prime presented at the cued location, and the subsequent target is 250 ms. Here we asked whether IT is also applied to ongoing emotional processing, and whether the left DLPFC plays a causal role in IT using HD-tDCS. In two experiments with an emotional conflict task, we observed reduced conflict effects, the signature of IT, when the prime word was presented at the cued location, and once again when the prime-target SOA was just 250 ms. Also, the IT effect was eliminated when cathodal stimulation was applied to the left DLPFC. These findings suggest that the IT effect involves areas of the executive attention network and cooperates with IOR to favor attentional allocation to novel unexplored objects/locations, irrespective of their emotional content.

Influence of inhibitory tagging (IT) on emotional and cognitive conflict processing: Evidence from event-related potentials.

Inhibitory tagging (IT), a flexible central control mechanism based on the current task goals, reduces the cognitive conflict effect at the cued location by blocking the incompatible stimulus-response (S-R) code. However, it is unknown whether IT has a similar effect on emotional conflict. Thus, we combined the face-word Stroop task with the manipulation of inhibition of return (IOR) and used event-related potential (ERP) technology to simultaneously examine the modulation effect of IT on emotional and cognitive conflict processing. At the cued location, we found that the two types of conflict effect were significantly reduced and that the conflict processing-related N450 effect was absent. Our data further revealed that IT had similar effects on emotional and cognitive conflict processing. Although a negative difference wave (Nd) was found in the time window of 160 and 220ms, which may reflect the impaired early perceptual processing of the target at the cued location, the effect of Nd was not affected by stimulus congruency. These results illustrate that the cueing effect of conflict processing does not arise from the early stage of perceptual processing, but rather results from the blocked S-R code of the distractors due to IT functioning during the later stage of processing.