Neural repetition suppression reflects fulfilled perceptual expectations

Abstract

Stimulus-evoked neural activity is attenuated on stimulus repetition (repetition suppression), a phenomenon that is attributed to largely automatic processes in sensory neurons. By manipulating the likelihood of stimulus repetition, we found that repetition suppression in the human brain was reduced when stimulus repetitions were improbable (and thus, unexpected). Our data suggest that repetition suppression reflects a relative reduction in top-down perceptual 'prediction error' when processing an expected, compared with an unexpected, stimulus.

Figure 1

Main experiment: protocol and results. (a) Faces were presented in successive pairs, with each face presented for 250ms, separated by a blank screen for 500ms, and a jittered interval of 2–4 seconds between pairs. Pairs comprised either the same face (repetition [rep] trials) or two different faces (alternation [alt] trials). Subjects monitored the stimulus stream for occasional inverted faces (target trials), occurring on 20% of all trials. Targets occurred equally often as the first or second stimulus within a pair. Trials were presented within two contexts (blocks of trials), one in which the probability of encountering rep trials was high (75% of non-target trials, REP BLOCKS), and one in which this probability was low (25% of non-target trials, ALT BLOCKS ). (b) In the left panels, center-of-mass locations for individual FFAs (see also Supplementary Table 1 online) are shown in different colors, rendered onto a standard brain (MNI y – 53, z – 21). The right panels display results from a random effects group analyses, thresholded at a whole-brain corrected false discovery rate of P < 0.05 (left FFA peak: MNI x – 44, y – 50, z – 20; right FFA peak: MNI x 46, y – 50, z – 18). (c) Average parameter estimates (± within-subject s.e.m.) obtained from individual FFAs are displayed for non-target rep trials (white bars) and alt trials (grey bars) in REP and ALT BLOCKS.

Figure 2

Control experiment: protocol and results. (a) Task parameters were identical to the main experiment (Fig. 1a), except that face images in each pair were subject to a variation in size. In standard alt and rep trials, either the first (in 50% of trials) or the second image in a pair of faces was reduced in size by 15%. Subjects monitored the stimulus stream for occasional targets, consisting of a face reduced by 60% in size, which occurred on 20% of all trials. The target face occurred equally often as the first or second stimulus within a pair, and half of the target trials showed the same face twice, while the other half showed two different faces. Trials were presented in blocks where the probability of encountering rep trials was either high (75% of non-target trials, REP BLOCKS), or low (25% of non-target trials, ALT BLOCKS). (b) In the left panels, center-of-mass locations for individual FFAs (see also Supplementary Table 1 online) are shown in different colors, rendered onto a standard brain (MNI y – 56, z – 21). The right panels display results from a random effects group analyses, thresholded at an uncorrected P < 0.005 (left FFA peak: MNI x – 44, y – 44, z – 20; right FFA peak: MNI × 46, y – 50, z – 24). (c) Average parameter estimates (± within-subject s.e.m.) obtained from individual FFAs are displayed for non-target rep trials (white bars) and alt trials (grey bars) in REP and ALT BLOCKS.