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.