The term priority map is commonly used to describe a map of the visual scene, in which objects and locations are represented by their attentional priority, which itself is a combination of low-level salience and top-down control. The aim of this review is to examine how such a map may be represented at the neuronal level. We propose that there is not a single, common map in the brain, but that a number of cortical areas work together to generate the resultant behavior. Specifically, we suggest that the lateral intraparietal area (LIP) of posterior parietal cortex provides a simple representation of attentional priority, which remaps across saccades, so that there is an apparent allocentric map in a region with retinocentric encoding scheme. We propose that the frontal eye field (FEF) of prefrontal cortex receives the responses from LIP, but can suppress them to control the flow of eye movement behavior, and that the intermediate layers of the superior colliculus (SCi) reflect the final saccade goal. Together, these areas function to guide eye movements and may play a similar role in allocating covert visual attention.

As our eyes move, we have a strong percept that the world is stable in space and time; however, the signals in cortex coming from the retina change with each eye movement. It is not known how this changing input produces the visual percept we experience, although the predictive remapping of receptive fields has been described as a likely candidate. To explain how remapping accounts for perceptual stability, we examined responses of neurons in the lateral intraparietal area while animals performed a visual foraging task. When a stimulus was brought into the response field of a neuron that exhibited remapping, the onset of the postsaccadic representation occurred shortly after the saccade ends. Whenever a stimulus was taken out of the response field, the presaccadic representation abruptly ended shortly after the eyes stopped moving. In the 38% (20/52) of neurons that exhibited remapping, there was no more than 30 ms between the end of the presaccadic representation and the start of the postsaccadic representation and, in some neurons, and the population as a whole, it was continuous. We conclude by describing how this seamless shift from a presaccadic to postsaccadic representation could contribute to spatial stability and temporal continuity.

The decision of where to make an eye movement is thought to be driven primarily by responses to stimuli in neurons' receptive fields (RFs) in oculomotor areas, including the frontal eye field (FEF) of prefrontal cortex. It is also thought that a saccade may be generated when the accumulation of this activity in favor of one location or another reaches a threshold. However, in the reading and scene perception fields, it is well known that the properties of the stimulus at the fovea often affect when the eyes leave that stimulus. We propose that if FEF plays a role in generating eye movements, then the identity of the stimulus at fixation should affect the FEF responses so as to reduce the probability of making a saccade when fixating an item of interest. Using a visual foraging task in which animals could make multiple eye movements within a single trial, we found that responses were strongly modulated by the identity of the stimulus at the fovea. Specifically, responses to the stimulus in the RF were suppressed when the animal maintained fixation for longer durations on a stimulus that could be associated with a reward. We suggest that this suppression, which was predicted by models of eye movement behavior, could be a mechanism by which FEF can modulate the temporal flow of saccades based on the importance of the stimulus at the fovea.

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.

The enhancement of neuronal responses in many visual areas while animals perform spatial attention tasks has widely been thought to be the neural correlate of visual attention, but it is unclear whether the presence or absence of this modulation contributes to our striking inability to notice changes in change blindness examples. We asked whether neuronal responses in visual area V4 and the lateral intraparietal area (LIP) in posterior parietal cortex could explain the limited ability of subjects to attend multiple items in a display. We trained animals to perform a change detection task in which they had to compare 2 arrays of stimuli separated briefly in time and found that each animal's performance decreased as function of set-size. Neuronal discriminability in V4 was consistent across set-sizes, but decreased for higher set-sizes in LIP. The introduction of a reward bias produced attentional enhancement in V4, but this could not explain the vast improvement in performance, whereas the enhancement in LIP responses could. We suggest that behavioral set-size effects and the marked improvement in performance with focused attention may not be related to response enhancement in V4 but, instead, may occur in or on the way to LIP.