Graded Neuronal Modulations Related to Visual Spatial Attention

Studies of visual attention in monkeys typically measure neuronal activity when the stimulus event to be detected occurs at a cued location versus when it occurs at an uncued location. But this approach does not address how neuronal activity changes relative to conditions where attention is unconstrained by cueing. Human psychophysical studies have used neutral cueing conditions and found that neutrally cued behavioral performance is generally intermediate to that of cued and uncued conditions (Posner et al., 1978; Mangun and Hillyard, 1990; Montagna et al., 2009). To determine whether the neuronal correlates of visual attention during neutral cueing are similarly intermediate, we trained macaque monkeys to detect changes in stimulus orientation that were more likely to occur at one location (cued) than another (uncued), or were equally likely to occur at either stimulus location (neutral). Consistent with human studies, performance was best when the location was cued, intermediate when both locations were neutrally cued, and worst when the location was uncued. Neuronal modulations in visual area V4 were also graded as a function of cue validity and behavioral performance. By recording from both hemispheres simultaneously, we investigated the possibility of switching attention between stimulus locations during neutral cueing. The results failed to support a unitary “spotlight” of attention. Overall, our findings indicate that attention-related changes in V4 are graded to accommodate task demands. SIGNIFICANCE STATEMENT Studies of the neuronal correlates of attention in monkeys typically use visual cues to manipulate where attention is focused (“cued” vs “uncued”). Human psychophysical studies often also include neutrally cued trials to study how attention naturally varies between points of interest. But the neuronal correlates of this neutral condition are unclear. We measured behavioral performance and neuronal activity in cued, uncued, and neutrally cued blocks of trials. Behavioral performance and neuronal responses during neutral cueing were intermediate to those of the cued and uncued conditions. We found no signatures of a single mechanism of attention that switches between stimulus locations. Thus, attention-related changes in neuronal activity are largely hemisphere-specific and graded according to task demands.