Attentional modulation of the inner ear: a combined otoacoustic emission and EEG study

Abstract

Attending to a single stimulus in a complex multisensory environment requires the ability to select relevant information while ignoring distracting input. The underlying mechanism and involved neuronal levels of this attentional gain control are still a matter of debate. Here, we investigated the influence of intermodal attention on different levels of auditory processing in humans. It is known that the activity of the cochlear amplifier can be modulated by efferent neurons of the medial olivocochlear complex. We used distortion product otoacoustic emission (DPOAE) measurements to monitor cochlear activity during an intermodal cueing paradigm. Simultaneously, central auditory processing was assessed by electroencephalography (EEG) with a steady-state paradigm targeting early cortical responses and analysis of alpha oscillations reflecting higher cognitive control of attentional modulation. We found effects of selective attention at all measured levels of the auditory processing: DPOAE levels differed significantly between periods of visual and auditory attention, showing a reduction during visual attention, but no change during auditory attention. Primary auditory cortex activity, as measured by the auditory steady-state response (ASSR), differed between conditions, with higher ASSRs during auditory than visual attention. Furthermore, the analysis of cortical oscillatory activity revealed increased alpha power over occipitoparietal and frontal regions during auditory compared with visual attention, putatively reflecting suppression of visual processing. In conclusion, this study showed both enhanced processing of attended acoustic stimuli in early sensory cortex and reduced processing of distracting input, both at higher cortical levels and at the most peripheral level of the hearing system, the cochlea.

Keywords: DPOAE; alpha oscillation; auditory steady-state responses; cochlea; selective attention.

Figure 1.

Schematic illustration of the task and the EEG layout. A, Paradigm: Simultaneous acoustic (40 Hz amplitude modulated two-tone stimulus) and visual (Gabor patch) stimulation. After 3 s, a visual cue indicated the to-be-attended modality (visual or auditory). The target (stimulus deviation) occurred in the time range of 3–5 s after the cue and had to be responded to by an immediate button press. B, EEG electrode layout with 41 electrodes. C, Exemplary frequency spectrum of the DPOAE measurement including the primary tones (f1: 1390 Hz; f2: 1682 Hz) and the 2f1–f2 DPOAE. The noise level is marked by the gray line.

Figure 2.

Impact of intermodal attention on DPOAEs. A, Averaged time course of DPOAE level across the task duration (n = 23, mean ± SE). Red solid line, auditory task; blue dotted line, visual task. The DPOAE level is depicted relative to baseline. B, Mean DPOAE level change during attention compared with the time window before attention (n = 23, ± SE. The time windows are indicated by gray boxes in A. There was a significant difference between the auditory and visual conditions (t test, p = 0.01).

Figure 3.

Correlation between attention effect and individual DPOAE base level. The individual difference of the DPOAE level change in auditory versus visual trials and the subjects' preattentional DPOAE level was negatively correlated (r = −0.77; p < 0.001).

Figure 4.

Auditory steady-state responses during auditory and visual attention. A, Topographical distribution of the 40 Hz ASSR during the period of focused attention averaged across all subjects for auditory (left) and visual (right) trials relative to the baseline period before the cue. B, Statistical contrast between conditions (t values). Electrodes of the significant cluster (p = 0.03) are marked with crosses. C, Time course of the ASSR power at cluster electrodes, mean ± SE. Red solid line, auditory trials; blue dotted line, visual trials.

Figure 5.

Attentional modulation of alpha activity (8–14 Hz). A, Topographic representation of statistical differences (t values) between alpha activity during auditory and visual attention in the period 0.5–2.5 s after cue presentation. Electrodes of the two significant clusters are marked (first cluster at occipitoparietal sites: *p < 0.01, second cluster at left frontal electrodes; +p < 0.01). B, Time course of alpha power during the task. Averaged values are depicted for the occipitoparietal cluster electrodes for all subjects (n = 23, mean ±SE). Red solid line, auditory trials; blue dotted line, visual trials.