Repetition suppression and expectation suppression are dissociable in time in early auditory evoked fields

Abstract

Repetition of a stimulus, as well as valid expectation that a stimulus will occur, both attenuate the neural response to it. These effects, repetition suppression and expectation suppression, are typically confounded in paradigms in which the nonrepeated stimulus is also relatively rare (e.g., in oddball blocks of mismatch negativity paradigms, or in repetition suppression paradigms with multiple repetitions before an alternation). However, recent hierarchical models of sensory processing inspire the hypothesis that the two might be separable in time, with repetition suppression occurring earlier, as a consequence of local transition probabilities, and suppression by expectation occurring later, as a consequence of learnt statistical regularities. Here we test this hypothesis in an auditory experiment by orthogonally manipulating stimulus repetition and stimulus expectation and, using magnetoencephalography, measuring the neural response over time in human subjects. We found that stimulus repetition (but not stimulus expectation) attenuates the early auditory response (40-60 ms), while stimulus expectation (but not stimulus repetition) attenuates the subsequent, intermediate stage of auditory processing (100-200 ms). These findings are well in line with hierarchical predictive coding models, which posit sequential stages of prediction error resolution, contingent on the level at which the hypothesis is generated.

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 (dashed line). The 10 maximally activated channels in each hemisphere are highlighted. B, Average auditory evoked field for all tones in selected channels highlighted in A. The two tones occurred in succession, but are displayed in the same time window here to highlight neuronal suppression for the second tone.

Figure 2.

Effect of pitch repetition on neuronal suppression. A, Auditory evoked fields for repeated (green) and alternating (black) tones. Temporal windows are denoted on the x-axis. Significant effects are in gray. Dashed line represents tone onset. B, Average topography over time for repeated tones (top), alternating tones (middle), and their difference (bottom). Dots represent analyzed channels.

Figure 3.

Effect of pitch expectation on neuronal suppression. A, Auditory evoked fields for expected (blue) and unexpected (red) tones. Temporal windows are denoted on the x-axis. Significant effects are in gray. Dashed line represents tone onset. B, Average topography over time for expected tones (top), unexpected tones (middle), and their difference (bottom). Dots represent analyzed channels.

Figure 4.

Stability of expectation suppression throughout the experiment. Average evoked fields 100–200 ms after tone onset for expected trials (blue) and unexpected trials (red). Each point represents an average of 10 successive trials.