The neural mechanisms for minimizing cross-modal distraction

Abstract

The neural circuitry that increases attention to goal-relevant stimuli when we are in danger of becoming distracted is a matter of active debate. To address several long-standing controversies, we asked participants to identify a letter presented either visually or auditorily while we varied the amount of cross-modal distraction from an irrelevant letter in the opposite modality. Functional magnetic resonance imaging revealed three novel results. First, activity in sensory cortices that processed the relevant letter increased as the irrelevant letter became more distracting, consistent with a selective increase of attention to the relevant letter. In line with this view, an across-subjects correlation indicated that the larger the increase of activity in sensory cortices that processed the relevant letter, the less behavioral interference there was from the irrelevant letter. Second, regions of the dorsolateral prefrontal cortex (DLPFC) involved in orienting attention to the relevant letter also participated in increasing attention to the relevant letter when conflicting stimuli were present. Third, we observed a novel pattern of regional specialization within the cognitive division of the anterior cingulate cortex (ACC) for focusing attention on the relevant letter (dorsal ACC) versus detecting conflict from the irrelevant letter (rostral ACC). These findings indicate novel roles for sensory cortices, the DLPFC, and the ACC in increasing attention to goal-relevant stimulus representations when distracting stimuli conflict with behavioral objectives. Furthermore, they potentially resolve a long-standing controversy regarding the key contribution of the ACC to cognitive control.

Figure 1.

A schematic of the experimental task showing sample trials and response options. Participants were cued from the visual modality (top left) or from the auditory modality (top right) to attend for a target letter in one sensory modality (visual or auditory; only visual is shown) while ignoring a simultaneous distracter letter in the unattended modality. The distracter letter was equally likely to be mapped to the same response as the target (congruent target-distracter pair; bottom left) or to a different response (incongruent target-distracter pair; bottom right). ISI, Interstimulus interval.

Figure 2.

Target-related activity in visual and auditory sensory cortices. Regions of the left middle temporal gyrus (MTG) and right middle occipital gyrus (MOG) identified by voxel-wise and ROI analyses, respectively, overlaid on an axial slice (z = -7) of the SPM'99 normalized anatomical template. Each figure plots the average BOLD response (in units of percentage change from baseline) in either the left MTG or right MOG for incongruent (red) and congruent (green) target-distracter pairs. When participants identified a visual letter, the presence of an incongruent versus a congruent auditory letter selectively increased activity in the right MOG (top left). In contrast, when participants identified an auditory target, the presence of an incongruent versus a congruent visual letter selectively increased activity in the left MTG (bottom right).

Figure 3.

Correlation between fMRI activity in the right middle occipital gyrus (MOG) and behavior. Across participants, greater conflict-related fMRI activity in the right MOG during the identification of visual targets predicted reduced behavioral interference from auditory distracters (r = -0.49; p < 0.05). In other words, participants with a relatively large difference between peak percentage change for incongruent versus congruent target-distracter pairs in the right MOG (x-axis) exhibited a relatively small difference between reaction time for incongruent versus congruent target-distracter pairs (y-axis).

Figure 4.

Cue- and target-related activity in the DLPFC. The left and right DLPFC are overlaid on an axial slice (z = +28) of the SPM'99 normalized anatomical template. Each figure plots the average BOLD response (in units of percentage change from baseline) in either the left or the right DLPFC for incongruent target-distracter pairs (red), congruent target-distracter pairs (green), cues to orient attention to the auditory modality (blue), and cues to orient attention to the visual modality (purple). In both the left and right DLPFC, there was significantly greater activity for (1) cues to orient attention to the auditory versus the visual modality (solid circles) and (2) incongruent versus congruent target-distracter pairs (dashed circles). LH, Left hemisphere; RH, right hemisphere.

Figure 5.

Cue- and target-related activity in midline frontal cortices. Five ROIs are overlaid on a sagittal slice (x = +4) of the SPM'99 normalized anatomical template. Each figure plots the average BOLD response (in units of percentage change from baseline) in a particular ROI for incongruent target-distracter pairs (red), congruent target-distracter pairs (green), cues to orient attention to the auditory modality (blue), and cues to orient attention to the visual modality (purple). Significantly greater activity for cues to orient attention to the auditory versus the visual modality was observed in dorsal and ventral regions within the cognitive division of the ACC (solid circles). In these same regions, there was also significantly greater activity for incongruent versus congruent target-distracter pairs (dashed circles). Rostral regions within the cognitive division of the ACC exhibited significantly greater activity for incongruent versus congruent target-distracter pairs in the absence of differential cue activity.