Auditory attention activates peripheral visual cortex

Abstract

Background: Recent neuroimaging studies have revealed that putatively unimodal regions of visual cortex can be activated during auditory tasks in sighted as well as in blind subjects. However, the task determinants and functional significance of auditory occipital activations (AOAs) remains unclear.

Methodology/principal findings: We examined AOAs in an intermodal selective attention task to distinguish whether they were stimulus-bound or recruited by higher-level cognitive operations associated with auditory attention. Cortical surface mapping showed that auditory occipital activations were localized to retinotopic visual cortex subserving the far peripheral visual field. AOAs depended strictly on the sustained engagement of auditory attention and were enhanced in more difficult listening conditions. In contrast, unattended sounds produced no AOAs regardless of their intensity, spatial location, or frequency.

Conclusions/significance: Auditory attention, but not passive exposure to sounds, routinely activated peripheral regions of visual cortex when subjects attended to sound sources outside the visual field. Functional connections between auditory cortex and visual cortex subserving the peripheral visual field appear to underlie the generation of AOAs, which may reflect the priming of visual regions to process soon-to-appear objects associated with unseen sound sources.

Figure 1. Stimuli and task.

Subjects attended to either auditory or visual stimuli in 21 s blocks to detect repeated stimulus events in the modality cued by a letter at fixation (top row). Auditory and visual stimuli occurred asynchronously at mean stimulus onset intervals of 1.5 s within each modality. Auditory targets (asterisk) were repeated tone triplets (250 ms/tone = 750 ms, red rectangles). Visual stimuli were presented for 700 ms (blue rectangles).

Figure 2. Cortical surface analysis display method.

Schematic diagram showing the transformation of a cortical hemisphere partially inflated using FreeSurfer to the equal-area Mollweide projection flat map used to display the data in this study. Clockwise from top left: Views of the medial and lateral surface of a semi-inflated model of the cortical surface (gray matter/white matter boundary) of the left hemisphere averaged over 60 individual brains. Shading indicates average cortical curvature (light: convex; dark: concave) with an overlaid functional activation map showing the effects of attention (see Figure 4 for more details). Next, the hemisphere is fully inflated to a sphere using FreeSurfer, and rotated to place the posterior occipital lobe at the equator. Finally, the surface of the sphere is visualized using an equal-area Mollweide projection, with the occipital pole at the map's center.

Figure 3. Stimulus-dependent activations.

Stimulus-dependent activations (SDAs) to unattended stimuli projected on a map of mean curvature across both hemispheres (darker gray = sulcus). A circled cross indicates the occipital pole. The calcarine sulcus is indicated by the yellow arrow pointing away from the foveal towards the peripheral visual field regions. HG Heschl's gyrus, STG superior temporal gyrus, IPS intraparietal sulcus, CentS central sulcus, TP temporal pole, FG fusiform gyrus, LG lingual gyrus, cun cuneus, POS parietal-occipital sulcus, CC corpus callosum. Data from sessions using sparse image acquisition. All activation maps are triple-thresholded (z>3/p<0.001, signal change >0.1%, cluster size >20 voxels).

Figure 4. Attention-related modulations.

Visual attention-related modulations (ARMs, blue) were seen in posterior occipitotemporal areas and the IPS. Auditory ARMs (red) were found in auditory cortex along the superior temporal plane with additional foci in the lingual gyrus and cuneus (auditory occipital activations: AOAs). The color scale shows mean percent signal change. Insets (right): mean occipital activations from sparse and continuous image acquisition sessions.

Figure 5. Occipital regions activated by auditory attention.

(A) Left: average cortical surface anatomy showing occipital regions (box). AOAs in all 9 subjects, depicted on maps of their individual occipital cortex surface curvature. Bottom right: the activation map from one subject who underwent retinotopic mapping of the horizontal and vertical meridians (green lines) and two eccentric annuli (white and yellow lines). (B) Cortical surface projections of the Talairach coordinates reported by Stenbacka et al. (2007) for visual checkerboard patterns presented at 12–30° and 30–49° in the peripheral visual field, superimposed on the mean AOA map averaged across subjects. Dots represent the reported Talairach coordinates (white, 12–30°, green, 30–49°) projected to the closest corresponding location on the cortical surface for each of 60 brains in the anatomical database.

Figure 6. Region of interest (ROI) analyses.

(A) Left: ARM activation maps from the sparse imaging data, plotted on the mean curvature map of the left hemisphere. The color scale and statistical thresholds are the same as in Figure 3. All significant voxels circumscribed by the yellow and green lines were designated as the AOA and central vision ROIs, respectively. Right: activation map from the continuous imaging data set used to analyze the ROIs, illustrated using identical thresholds. (B) Mean percent signal change for the four main task conditions in continuous imaging sessions: bimodal auditory (BA), unimodal auditory (UA), bimodal visual (BV) and unimodal visual (UV). A significant BA-BV difference indicates an ARM; a significant BV-UV difference indicates an auditory SDA; a BA-BV difference represents a visual SDA. The AOA ROI response was greatest when subjects attended to sounds in the absence of visual stimuli (UA condition), and showed no auditory SDA. Bars show standard errors of the mean.

Figure 7. Task-related processes and auditory occipital activations.

(A) Task-switching. Event-related time course regressors modeled activations associated with block termination and switching between auditory and visual tasks. Shown is the left hemisphere map from the continuous imaging data. Significant AOA regions (white outlines) overlapped very little with regions activated by task switching (red voxels). (B) Auditory target detection. Event-related time course regressors modeled button presses to targets during auditory attention blocks (red/yellow) as well as the intervals during which no responses were made (blue/cyan). Left hemisphere map is shown. AOA regions were not activated by target detection. (C) Inhibition by foveal visual cortex. Mixed-effects z-scores for the average correlation coefficient between the time course of each surface voxel and the mean time course of the AOA ROI, during unimodal visual conditions. Note the absence of significant correlations with central visual field voxels (region surrounding the circled cross). Left hemisphere map is shown.