Induction of Shape Selectivity in Macaque Frontal Eye Field Dissociates Perceptual and Motor Processing Stages of Visual Search

Abstract

Neurons in frontal eye field (FEF) respond to visual stimulation, before eye movements, and both. These responses differentiate whether or not a stimulus is a saccade target. This differentiation, or target selection, is stimulus-locked for many neurons. Importantly, this target selection does not usually depend on the features that define a target as such, because most neurons in FEF do not exhibit intrinsic feature selectivity. However, consistent mapping of a stimulus feature and reward can elicit feature selectivity. Whether this feature selectivity is similarly stimulus-locked or if it is related to the selection of a saccade endpoint is unknown. We developed a search pro-/anti-saccade task in which shape varies among stimuli but does not define the saccade target. One monkey tested in this task developed a strategy that exploits an incidental shape-response association as opposed to the intended rule. We identified visual neurons in FEF that exhibited shape selectivity. The timing of this selectivity followed visual onset but was coincident with saccade target selection. Further, we found that these neurons showed an additional increase in firing rate when a stimulus of the preferred shape was also chosen via saccade. This occurred after feature selection and was coincident with additional temporal measures of saccade endpoint selection. These findings together suggest that feature selectivity, when induced, is tantamount to target selection which is then followed by saccade endpoint selection. In this way, we can exploit feature selectivity in FEF neurons to dissociate the perceptual and motor stages of a complex visual search task.