Adam N. Phillips

Predictive Activity in Macaque Frontal Eye Field Neurons During Natural Scene Searching

Generating sequences of multiple saccadic eye movements allows us to search our environment quickly and efficiently. Although the frontal eye field cortex (FEF) has been linked to target selection and making saccades, little is known about its role in the control and performance of the sequences of saccades made during self-guided visual search. We recorded from FEF cells while monkeys searched for a target embedded in natural scenes and examined the degree to which cells with visual and visuo-movement activity showed evidence of target selection for future saccades. We found that for about half of these cells, activity during the fixation period between saccades predicted the next saccade in a sequence at an early time that precluded selection based on current visual input to a cells response field. In addition to predicting the next saccade, activity during the fixation prior to two successive saccades also predicted the direction and goal of the second saccade in the sequence. We refer to this as advanced predictive activity. Unlike activity indicating the upcoming saccade, advanced predictive activity occurred later in the fixation period, mirroring the order of the saccade sequence itself. The remaining cells without advanced predictive activity did not predict future saccades but reintroduced the signal for the upcoming saccade at an intermediate time in the fixation period. Together these findings suggest that during natural visual search the timing of FEF cell activity is consistent with a role in specifying targets for one or more future saccades in a search sequence.

Saliency and Saccade Encoding in the Frontal Eye Field During Natural Scene Search

The frontal eye field (FEF) plays a central role in saccade selection and execution. Using artificial stimuli, many studies have shown that the activity of neurons in the FEF is affected by both visually salient stimuli in a neurons receptive field and upcoming saccades in a certain direction. However, the extent to which visual and motor information is represented in the FEF in the context of the cluttered natural scenes we encounter during everyday life has not been explored. Here, we model the activities of neurons in the FEF, recorded while monkeys were searching natural scenes, using both visual and saccade information. We compare the contribution of bottom-up visual saliency (based on low-level features such as brightness, orientation, and color) and saccade direction. We find that, while saliency is correlated with the activities of some neurons, this relationship is ultimately driven by activities related to movement. Although bottom-up visual saliency contributes to the choice of saccade targets, it does not appear that FEF neurons actively encode the kind of saliency posited by popular saliency map theories. Instead, our results emphasize the FEFs role in the stages of saccade planning directly related to movement generation.

Feature-based attention and spatial selection in frontal eye fields during natural scene search

When we search for visual objects, the features of those objects bias our attention across the visual landscape (feature-based attention). The brain uses these top-down cues to select eye movement targets (spatial selection). The frontal eye field (FEF) is a prefrontal brain region implicated in selecting eye movements and is thought to reflect feature-based attention and spatial selection. Here, we study how FEF facilitates attention and selection in complex natural scenes. We ask whether FEF neurons facilitate feature-based attention by representing search-relevant visual features or whether they are primarily involved in selecting eye movement targets in space. We show that search-relevant visual features are weakly predictive of gaze in natural scenes and additionally have no significant influence on FEF activity. Instead, FEF activity appears to primarily correlate with the direction of the upcoming eye movement. Our result demonstrates a concrete need for better models of natural scene search and suggests that FEF activity during natural scene search is explained primarily by spatial selection.