Prior expectation mediates neural adaptation to repeated sounds in the auditory cortex: an MEG study

Abstract

Repetition suppression, the phenomenon that the second presentation of a stimulus attenuates neural activity, is typically viewed as an automatic consequence of repeated stimulus presentation. However, a recent neuroimaging study has suggested that repetition suppression may be driven by top-down expectations. Here we examined whether and when repetition suppression can be modulated by top-down expectation. Participants listened to auditory stimuli in blocks where tone repetitions were either expected or unexpected, while we recorded ongoing neural activity using magnetoencephalography. We found robust repetition suppression in the auditory cortex for repeated tones. Interestingly, this reduction was significantly larger for expected than unexpected repetitions, both in terms of evoked activity and gamma-band synchrony. These findings indicate a role of top-down expectation in generating repetition suppression and are in line with predictive coding models of perception, in which the difference between expected and actual input is propagated from lower to higher cortical areas.

Figures

Figure 1.

Localization of auditory activation. A, Topographic representation of average MEG channel activation for all tones, in the 50–150 ms interval after tone onset. The 10 maximally activated channels in each hemisphere are highlighted. B, Average auditory evoked field for all tones in selected channels that are highlighted in A. C, Time–frequency representation of average activity for all tones in selected channels. D, Source localization of activity to the first tone, in the 50–150 ms interval after tone onset. The power of the source reconstruction was thresholded at half-maximum.

Figure 2.

Effect of expectation on auditory repetition. A, Auditory evoked fields for expected (in blue) and unexpected (in red) tone repetitions. B, Time–frequency representations for expected (left panel) and unexpected (middle panel) tone repetitions, as well as their difference (right panel). Black rectangular boxes indicate temporal (evoked activity) or spectrotemporal (oscillatory activity) clusters of significant differences between conditions of expectation.

Figure 3.

Effect of expectation on auditory omission. A, Auditory evoked fields for expected (in blue) and unexpected (in red) tone omissions. B, Time–frequency representations for expected (left panel) and unexpected (middle panel) tone omissions, as well as their difference (right panel). Black rectangular boxes indicate temporal (evoked activity) or spectrotemporal (oscillatory activity) clusters of significant differences between conditions of expectation.

Figure 4.

Correlation between expectation effects on tone repetition and tone omission. The activity difference between expected and unexpected repetitions (averaged over the 100–500 ms window following the second tone, see Fig. 2A) is plotted (on the x-axis), against the activity difference between expected and unexpected omissions (on the y-axis; averaged over the same temporal window, see Fig. 3A).