Visual Attention: Bottom-Up Versus Top-Down Dispatch

To mangle a well-known Wordsworth line, the world istoo much for us — it contains far too much informa-tion for us to perceive at once. We typically payattention to individual items, one after another. Butwhich items? That depends on two distinct types ofattentional mechanism. Bottom-up mechanisms arethought to operate on raw sensory input, rapidly andinvoluntarily shifting attention to salient visual featuresof potential importance — the spot of red against afield of green that could be a piece of fruit, the suddenmovement that could be a predator. Top-downmechanisms implement our longer-term cognitivestrategies, biasing attention toward colored spots ifwe are hungry or toward sudden movements andquadrupedal shapes if we fear a predator.Psychologists have investigated how these twoattentional processes function in human perception,both individually and — as is usual under naturalconditions — together [1]. In a typical experiment [2],on some trials subjects were asked to search for andidentify a color singleton, such as a single red target ina search display containing several white distractorstimuli, while on other trials the target was an onsetsingleton — the only item in the display with an abruptonset. The search display was immediately precededby a ‘cue’ display, also containing a color or onset sin-gleton. Even though subjects were instructed that thepreceding cue display was irrelevant and should beignored, the cue singleton attracted attention in aninvoluntary, bottom-up fashion, affecting how quicklysubjects could respond to the upcoming targets. When a color-singleton cue appeared at the samelocation as the upcoming color target, for example,attention was drawn to the target location in advanceand responses were faster. When a color-singletoncue appeared at a different location, attention wastemporarily drawn away from the target location andresponses were slower. However, this bottom-upattention effect was modulated by the subject’s top-down attentional state: color-singleton cues onlyaffected response times when the subject wassearching for a color target; likewise, onset-singletoncues only mattered during search for onset targets.Thus, bottom-up attention alerts us to salient items inour environment, but top-down attention modulatesbottom-up signals when we need to look for some-thing specific.A new paper by Ogawa and Komatsu [3] provides aglimpse at the neural processes underlying suchinteractions between bottom-up and top-downattention. These investigators trained monkeys on twotop-down behavioral strategies: color-singleton searchand shape-singleton search. The search displays(Figure 1, red and green boxes) always contained sixstimuli, including one color singleton and one shapesingleton. At the beginning of the trial, the monkey hadto fix its gaze at the center of the screen. Then thedisplay appeared, and the monkey had to saccade(shift its gaze; arrows in Figure 1) to the correct targetto receive a reward. In the color search task (the twoboxes on the right), the correct target was the colorsingleton; in the shape search task (left-hand boxes)the correct target was the shape singleton. While the monkey performed these tasks, Ogawaand Komatsu [3] recorded the electrical spike activityof individual neurons in area V4, an intermediate stagein the visual object-processing pathway of the brain,where neural activity is known to be affected byattention [4–8]. The display was arranged so that onestimulus fell inside the V4 neuron’s receptive field(gray circles in Figure 1). On a given trial, the receptivefield stimulus could be the shape singleton (red boxesin Figure 1), the color singleton (green boxes) or one ofthe four non-singleton stimuli (not shown). Dependingon the search condition, a receptive field singletonstimulus could either be a target (solid outline boxes)or a non-target (dashed outline boxes). The firing rate