The neural circuitry underlying the executive control of auditory spatial attention

Abstract

Although a fronto-parietal network has consistently been implicated in the control of visual spatial attention, the network that guides spatial attention in the auditory domain is not yet clearly understood. To investigate this issue, we measured brain activity using functional magnetic resonance imaging while participants performed a cued auditory spatial attention task. We found that cued orienting of auditory spatial attention activated a medial-superior distributed fronto-parietal network. In addition, we found cue-triggered increases of activity in the auditory sensory cortex prior to the occurrence of an auditory target, suggesting that auditory attentional control operates in part by biasing processing in sensory cortex in favor of expected target stimuli. Finally, an exploratory cross-study comparison further indicated several common frontal and parietal regions as being involved in the control of both visual and auditory spatial attention. Thus, the present findings not only reveal the network of brain areas underlying endogenous spatial orienting in the auditory modality, but also suggest that the control of spatial attention in different sensory modalities is enabled in part by some common, supramodal neural mechanisms.

Figure 1. Brain activity for cues and targets, plotted using F-values, overlaid on several slices of the MNI normalized anatomical brain

Shown is activity related to (a) cue interpretation processes (Interpret-cue-only trials vs. Nostim trials), (b) cue interpretation processes plus attentional orienting processes (Attend-cue-only trials vs. Nostim trials), (c) attentional orienting processes (Attend-cue-only trials vs. Interpret-cue-only trials), and (d) target-related process (Attend-cue-plus-target vs. Attend-cue-only trials). Nine sample slices are shown for each contrast with the Talairach Z-coordinate (mm) labeled under each slice. The color bars under each row refer to the F-values that are plotted in each of the brain slices.

Figure 2. Attention-orienting activity in (a) dorsal brain areas and (b) ventral brain areas

These regions were identified by contrasting Attend-cue only with Interpret-cue-only trials, after correcting for overlap using the no-stim subtraction (see Methods). Each plot depicts the average BOLD response (in units of percentage change from the corresponding baseline) across time. Note that the extracted hemodynamic responses for the Attend-cue-only trials (red solid lines) are larger than those for the Interpret-cue-only trials (gray solid line) in these regions.

Figure 3. Cue-triggered activity within the left and right auditory cortices

Plotted is the difference in peak amplitude (percent change of BOLD response) between responses to right and left Attend-cue-only trials within the left and right auditory cortices (i.e., superior temporal gyrus). One sample slice (Z = 15mm) of the brain activation is shown to indicate the ROIs being drawn. The relative contralaterality of the cue response in auditory cortex was reflected in a significant interaction in an ANOVA (F(1,12) = 7.12, p < 0.025). Note. STG = superior temporal gyrus

Figure 4. Conjunction analysis revealing areas involved in spatial orienting in both the visual and the auditory modalities

(A) Auditory-study ROIs (red), visual-study ROIs (blue) and conjunction (yellow) brain areas (supramodal regions) are indicated. The numbered light green dot-circled regions in the figure refer to 1, the superior parietal lobe, 2, the frontal eye fields, 3 the anterior cingulate cortex, and 4, the anterior insula. (B) Plots of fMRI responses in supramodal areas. Each plot depicts the average BOLD response (in units of percentage change from the corresponding baseline) across time for Attend-cue-only (red) and Interpret-cue-only (gray) trials. These responses are shown in areas that were supramodal (yellow) including the superior parietal lobe, the frontal eye fields, the anterior cingulate cortex, and the anterior insula. Note that the responses from the visual and auditory studies are plotted on different scales, due to differences in the magnetic field strength used in the two studies (i.e., 1.5 T versus 4 T, respectively).

Figure 5. Timeline of cue and target presentation in each trial

The structure of a trial in (a) the auditory spatial attention study and (b) the closely corresponding visual spatial attention study of Woldorff et al. (2004)