Attention Modulates the Auditory Cortical Processing of Spatial and Category Cues in Naturalistic Auditory Scenes

Abstract

This combined fMRI and MEG study investigated brain activations during listening and attending to natural auditory scenes. We first recorded, using in-ear microphones, vocal non-speech sounds, and environmental sounds that were mixed to construct auditory scenes containing two concurrent sound streams. During the brain measurements, subjects attended to one of the streams while spatial acoustic information of the scene was either preserved (stereophonic sounds) or removed (monophonic sounds). Compared to monophonic sounds, stereophonic sounds evoked larger blood-oxygenation-level-dependent (BOLD) fMRI responses in the bilateral posterior superior temporal areas, independent of which stimulus attribute the subject was attending to. This finding is consistent with the functional role of these regions in the (automatic) processing of auditory spatial cues. Additionally, significant differences in the cortical activation patterns depending on the target of attention were observed. Bilateral planum temporale and inferior frontal gyrus were preferentially activated when attending to stereophonic environmental sounds, whereas when subjects attended to stereophonic voice sounds, the BOLD responses were larger at the bilateral middle superior temporal gyrus and sulcus, previously reported to show voice sensitivity. In contrast, the time-resolved MEG responses were stronger for mono- than stereophonic sounds in the bilateral auditory cortices at ~360 ms after the stimulus onset when attending to the voice excerpts within the combined sounds. The observed effects suggest that during the segregation of auditory objects from the auditory background, spatial sound cues together with other relevant temporal and spectral cues are processed in an attention-dependent manner at the cortical locations generally involved in sound recognition. More synchronous neuronal activation during monophonic than stereophonic sound processing, as well as (local) neuronal inhibitory mechanisms in the auditory cortex, may explain the simultaneous increase of BOLD responses and decrease of MEG responses. These findings highlight the complimentary role of electrophysiological and hemodynamic measures in addressing brain processing of complex stimuli.

Keywords: auditory attention; auditory cortex (AC); auditory scene analysis; fMRI BOLD; magnetoencephalography (MEG).

Figure 1

Examples of the experimental stimuli. The original sounds (“baby babbling” and “Washing machine”) are depicted for both left and right auditory channel (top); the combined sounds used in the experiment, in both stereophonic and monophonic forms, are shown below.

Figure 2

Results from cortex-based aligned random effect analysis in stereophonic and monophonic experimental conditions (LH, left hemisphere; RH, right hemisphere). (A) All conditions vs. baseline (F-map; the color ranges from yellow to reddish with increasing f-value). (B) “Stereophonic” vs. “Monophonic” stimuli (merged attention conditions; light blue: Stereophonic > Monophonic). (C) “Stereophonic” vs. “Monophonic” stimuli in the “Voice” condition (red: Stereophonic-Voice > Monophonic-Voice) and in the “Environment” condition (blue: Stereophonic-Environment > Monophonic-Environment); the overlapping area common for both these contrasts is highlighted in yellow. (D) The statistically significant interaction maps of the activations depicted in (C). Green: “Stereophonic-Environment”—“Monophonic-Environment” > “Stereophonic-Voice”—“Monophonic-Voice”; orange: “Stereophonic-Voice”—Monophonic- Voice” > “Stereophonic-Environment”—“Monophonic-Environment.”

Figure 3

MEG group-level data. The locations and orientations of individual ECDs used to model the 100-ms, sustained (white dots), and 250-ms (black dots) responses superimposed on an average brain, and the corresponding averaged ECD time courses from −200 to 1000 ms with respect to the stimulus onset, grouped across the two attention conditions. The asterisk indicates the 100-ms time window with statistically significant difference (P < 0.04) between the conditions.

Figure 4

Time courses of the ECDs used to model the 100-ms and sustained responses to stereo- vs. monophonic sounds in both attentional conditions. (Top: attention to voice; bottom: attention to environmental sounds). The asterisks indicate the 50-ms (LH) and 100-ms time windows (RH) with statistically significant differences between the conditions.