Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: supramodal or sensory-specific control mechanisms?

Abstract

Oscillatory alpha-band activity (8-15 Hz) over parieto-occipital cortex in humans plays an important role in suppression of processing for inputs at to-be-ignored regions of space, with increased alpha-band power observed over cortex contralateral to locations expected to contain distractors. It is unclear whether similar processes operate during deployment of spatial attention in other sensory modalities. Evidence from lesion patients suggests that parietal regions house supramodal representations of space. The parietal lobes are prominent generators of alpha oscillations, raising the possibility that alpha is a neural signature of supramodal spatial attention. Furthermore, when spatial attention is deployed within vision, processing of task-irrelevant auditory inputs at attended locations is also enhanced, pointing to automatic links between spatial deployments across senses. Here, we asked whether lateralized alpha-band activity is also evident in a purely auditory spatial-cueing task and whether it had the same underlying generator configuration as in a purely visuospatial task. If common to both sensory systems, this would provide strong support for "supramodal" attention theory. Alternately, alpha-band differences between auditory and visual tasks would support a sensory-specific account. Lateralized shifts in alpha-band activity were indeed observed during a purely auditory spatial task. Crucially, there were clear differences in scalp topographies of this alpha activity depending on the sensory system within which spatial attention was deployed. Findings suggest that parietally generated alpha-band mechanisms are central to attentional deployments across modalities but that they are invoked in a sensory-specific manner. The data support an "interactivity account," whereby a supramodal system interacts with sensory-specific control systems during deployment of spatial attention.

Figure 1.

A schematic of the experimental paradigm illustrates the sequence of events and their timing within a trial, for each of the auditory (A) and visual (B) tasks. The spoken phoneme (/ba/ or /da/) served to cue participants to attend right or to attend left for the occurrence of a possible target. These auditory cues were followed 1000 ms later by the imperative stimulus (S2: Gabors in the visual task and a noise burst in the auditory task). In the depiction of the visual task (B), a target ring is present in the left Gabor. C and D delineate the stimulus probabilities at cued and uncued locations for auditory and visual tasks.

Figure 2.

Performance on the auditory and visual tasks. Accuracy as a function of task and cue direction is illustrated in a, and reaction time as a function of task and cue direction is illustrated in b.

Figure 3.

Scalp topographic maps of alpha power (from 600 to 940 ms) for cue-left and cue-right conditions, for each of the auditory and visual tasks. In the bottom row, cue right is subtracted from cue left to illustrate the parietal distribution of the cue-specific alpha-power topographies that is seen in both the auditory and visual tasks.

Figure 4.

Alpha power in each ROI dependent on cue direction. Comparing left and right ROIs for each of the auditory and visual tasks, alpha power is greater over the parieto-occipital cortex ipsilateral to the direction of attention for several post-S1 time windows, for both visual and auditory tasks.

Figure 5.

Scalp topographies of alpha power averaged over cue condition for the auditory and visual tasks. For each time interval from 600 to 940 ms (a–d), topographies are displayed separately for auditory and visual tasks. To illustrate differences in the scalp distribution of alpha power between the sensory conditions, these are accompanied by a composite display of the same auditory and visual scalp topographies and their centers of maximal activity. The bottom row (e, f) displays the electrodes used for the stage 2 analysis. The gray circle shaded electrode represents the midline occipital electrode as a bearing, as the scalp has been rotated to depict mainly right hemisphere electrodes.

Figure 6.

Paired t tests of all electrodes and all time points across auditory and visual conditions (corrected for multiple comparisons). Parieto-occipital electrodes outlined in white show significant (p < 0.05) difference across the two conditions from 780 to 940 ms after S1. Significant differences were also observed for a few parietal electrodes from 400 to 700 ms, but distinct topographical shifts were not observed for this time period.