Independence of anticipatory signals for spatial attention from number of nontarget stimuli in the visual field

Abstract

Covertly attending to a location modulates the activity of visual areas even in the absence of visual stimulation. These effects are widespread, being found in the cortical representations of both attended and unattended portions of the visual field. It is not clear, however, whether preparatory modulations depend on subjects' expectation regarding the presence of additional nontarget stimuli in the visual field. Here, we asked subjects to endogenously direct attention to a peripheral location in the upper visual field, to identify the orientation of a low-contrast target stimulus, and we manipulated the number and behavioral relevance of other low-contrast nontarget stimuli in the visual field. Anticipatory (i.e., prestimulus) blood oxygenation level-dependent (BOLD) signal increments in visual cortex were strongest at the contralateral attended location, whereas signal decrements were strongest at the unattended mirror-opposite ipsilateral location/region of visual cortex. Importantly, these strong anticipatory decrements were not related to the presence/absence of nontarget low-contrast stimuli and did not correlate with either weaker target-evoked responses or worse performance. Second, the presence of other low-contrast stimuli in the visual field, even when potential targets, did not modify the anticipatory signal modulation either at target or nontarget locations. We conclude that the topography of spatial attention-related anticipatory BOLD signal modulation across visual cortex, specifically decrements at unattended locations, is mainly determined by processes at the cued location and not by the number or behavioral relevance of distant low-contrast nontarget stimuli elsewhere in the visual field.

FIG. 1.

The visuospatial attention task used in the practice sessions and the functional magnetic resonance imaging (fMRI) experiment. A: trial structure for the 3 versions of the task (“zero-NT,” “one-NT,” or “three-NT,” where NT is nontarget). During the 2 practice sessions stimulus-onset asynchrony (SOA) was kept constant at 2 s, whereas in the fMRI task it varied among 6, 8, and 10 s. B: the association between spoken numbers and the peripheral locations where target or nontarget stimuli could have been presented.

FIG. 2.

Regions of interest (ROIs) in the visual cortex. A: the result of the retinotopy scans is superimposed on the flattened left hemisphere surface of a representative subject. The stimuli (vertical and horizontal meridians) used to obtain borders of visual areas are shown in the top right corner. B: an example of the results from the localizer scan in the same subject, which illustrates the portion of the ventral visual cortex of the left hemisphere activated by the presentation of a flickering high-contrast patch in the upper right visual field. C: the definition of the 3 ROIs in each hemisphere. The different colors correspond to the different peripheral locations in the visual field.

FIG. 3.

Behavioral performance, averaged across the 5 subjects, for the 3 experimental conditions. Accuracy (A) and reaction times (B) for valid and invalid trials calculated using only trials with the longest SOA that were used for the fMRI statistical analysis. Accuracy (C) and reaction times (D) for valid trials (Uvf cued) and invalid trials presented at the other upper field location (Uvf unc.), at the lower field location of the cued side (Lvf cued side), and, finally, at the lower field location of the uncued side (Lvf unc. Side), for the “three-NT” condition only. Vertical bars represent SEs. *P < 0.05; **P < 0.01. Lvf, lower visual field; Uvf, upper visual field; unc., uncued.

FIG. 4.

Average blood oxygenation level–dependent (BOLD) signal time courses corresponding to the 13 time points following cue onset during valid correct trials with the longest SOA (10 s). Time courses were extracted from the ROIs representing the 4 possible target locations plus a foveal location, independently identified by the localizer. The 3 ROIs in the left and right hemispheres are highlighted in different colors and superimposed on the flattened hemisphere surfaces of a representative subject (located in the left and the right sides of the picture). Region colors correspond to the specific peripheral locations, illustrated above the left hemisphere representation. For display purposes, time courses have been collapsed for the different display conditions and left and right hemisphere ROIs. The two red vertical lines represent cue and target onset, respectively. Time courses from dorsal cortical regions (indicated by green and yellow areas on the flattened surface), corresponding to the lower visual field locations, are displayed in the top row. Ventral cortical regions (red and blue areas), corresponding to the upper visual field locations, are displayed in the bottom row. Time courses from ROIs representing the foveal regions (black areas) are shown in between. Black and gray time courses indicate BOLD responses for contralateral and ipsilateral cues, respectively. Vertical bars of the time courses represent SEs.

FIG. 5.

BOLD signal time courses (valid correct trials only) during the preparatory period from the 4 peripheral ROIs [upper visual field (v.f.) cued location (thick black line), upper v.f. uncued (thick gray line), lower v.f. on the cued side (thin black line), and lower v.f. location on the uncued side (thin gray line)], each of of the 3 display conditions displayed separately. The time courses from the 2 hemispheres are collapsed.

FIG. 6.

Histogram of the receiver-operator-characteristic (ROC) values obtained in the predictive analysis of cue direction, “zero-NT” and “three-NT” conditions displayed separately. The bars correspond to (from the left): the single regions representing the upper v.f. locations, the single regions representing the lower v.f. locations, the subtraction of signals between regions representing the upper and the contralateral lower location, the subtraction between the 2 lower locations, and, finally, the subtraction between the 2 upper locations.

FIG. 7.

BOLD signal time courses evoked by valid (thick black line) and invalid (thick gray line) target presentation from the corresponding ROIs representing the upper v.f. locations, in the 3 conditions. BOLD signal time courses evoked by invalid targets presented at lower v.f. locations (“three-NT” condition) obtained in the corresponding ROIs [lower v.f. location in the cued side (thin black line) and lower v.f. location in the uncued side (think gray line)]. The time courses from the 2 hemispheres are collapsed.