Top-down and bottom-up mechanisms in biasing competition in the human brain

Abstract

The biased competition theory of selective attention has been an influential neural theory of attention, motivating numerous animal and human studies of visual attention and visual representation. There is now neural evidence in favor of all three of its most basic principles: that representation in the visual system is competitive; that both top-down and bottom-up biasing mechanisms influence the ongoing competition; and that competition is integrated across brain systems. We review the evidence in favor of these three principles, and in particular, findings related to six more specific neural predictions derived from these original principles.

Figure 1. Competitive interactions and attentional modulation in visual cortex

A: Suppressive interactions in V1 and V4. Simultaneously presented stimuli evoked less activity than sequentially presented stimuli in V4, but not in V1, suggesting that suppressive interactions were scaled to the RF size of neurons in visual cortex. B: Attentional modulation of suppressive interactions. The suppression effect in V4 was replicated in the unattended condition of this experiment, when the subjects’ attention was directed away from the stimulus display (unshaded time series). Spatially directed attention (shaded time series) increased responses to simultaneously presented stimuli to a larger degree than to sequentially presented ones in V4. Adapted from Kastner et al. (1998).

Figure 2. Modulation of sensory suppression in areas V4 and TEO

Time series of fMRI signals in V4 and TEO with display sizes of 2 × 2 degrees (A) and 7 × 7 degrees (B). Displays consisting of four stimuli were presented within the same quadrant and in the sequential and simultaneous conditions. Data are from a single subject. When stimuli were presented with the 2 × 2 degrees display, response differences to sequentially and simultaneously presented stimuli were found in V4 and TEO. When stimuli were presented with the 7 × 7 degrees display, the response differences were abolished in V4, but unchanged in TEO.

Figure 3. Increases of baseline activity in the absence of visual stimulation

A: Time series of fMRI signals in V4. Directing attention to a peripheral target location in the absence of visual stimulation led to an increase of baseline activity (textured blocks), which was followed by a further increase after the onset of the stimuli (gray shaded blocks). Baseline increases were found in both striate and extrastriate visual cortex. B: Time series of fMRI signals in FEF. Directing attention to the peripheral target location in the absence of visual stimulation led to a stronger increase in baseline activity than in visual cortex; the further increase of activity after the onset of the stimuli was not significant.

Figure 4. Time series of fMRI signals for heterogeneous and pop-out displays in visual cortex

Group analysis (N=6). Solid curves indicate activity evoked by sequential presentations and dashed curves that evoked by simultaneous presentations. A: For heterogeneous displays, sequentially presented stimuli evoked more activity than simultaneously presented stimuli in areas V2/VP and V4. In V1, there was no difference between sequentially and simultaneously presented heterogeneous stimuli. B: Pop-out displays did not induce significant response differences between simultaneously and sequentially presented stimuli in areas V2/VP and V4. In area V1, the difference in responses evoked by sequential and simultaneous presentations was reversed.

Figure 5. Effects of pop-out, stimulus similarity and directed attention on competitive interactions in human visual cortex

SSIs [SSI = (R_SEQ − R_SIM)/(R_SEQ + R_SIM); R, response computed as mean signal change; SEQ, sequential presentation condition; SIM, simultaneous presentation condition] obtained for areas V1 (squares), V2/VP (triangles), and V4 (circles) are plotted for the study investigating competitive interactions in the presence of top-down spatially directed attention (Kastner et al. 1998; black symbols) and in the presence of the bottom-up factors of pop-out (Beck & Kastner, 2005; open symbols) and stimulus similarity (Beck & Kastner, 2007; gray symbols). The horizontal axis represents the SSIs obtained for heterogeneous display conditions from the three studies, when the peripheral stimuli were unattended. The vertical axis represents the SSIs obtained for the pop-out display condition, the homogeneous display condition from the stimulus similarity study, and the directed attention condition, in order to directly compare the top-down and bottom-up effects on the competition. The dashed line represents the points at which the two indices are equal (i.e. equivalent competitive interactions with and without the bias). Although all points fall below the dashed line indicating that all three manipulations reduced competitive interactions, this effect was larger for the pop-out study (filled symbols) than the directed attention study (open symbols).

Figure 6. A fronto-parietal network for spatial attention

Axial slice through frontal and parietal cortex. A: When the subject directed attention to a peripheral target location and performed a discrimination task, a distributed fronto-parietal network was activated including the SEF, the FEF and the SPL. B: The same network of frontal and parietal areas was activated when the subject directed attention to the peripheral target location in expectation of the stimulus onset. L indicates left hemisphere.