Abstract
Repeated exposure to a stimulus leads to reduced responses of stimulus-selective sensory neurons, an effect known as repetition suppression or stimulus-specific adaptation. Several influential models have been proposed to explain repetition suppression within hierarchically-organised sensory systems, with each specifying different mechanisms underlying repetition effects. We manipulated temporal expectations within a face repetition experiment to test a critical prediction of the predictive coding model of repetition suppression: that repetition effects will be larger following stimuli that appear at expected times compared to stimuli that appear at unexpected times. We recorded event-related potentials from 18 participants and mapped the spatiotemporal progression of repetition effects using mass univariate analyses. We then assessed whether the magnitudes of observed face image repetition effects were influenced by temporal expectations. In each trial participants saw an adapter face, followed by a 500 ms or 1000 ms interstimulus interval (ISI), and then a test face, which was the same or a different face identity to the adapter. Participants’ expectations for whether the test face would appear after a 500 ms ISI were cued by the sex of the adapter face. Our analyses revealed multiple repetition effects with distinct scalp topographies, extending until at least 800 ms from stimulus onset. An early (158–203 ms) repetition effect was larger for stimuli following surprising, rather than expected, 500 ms ISI durations, contrary to the model predictions of the predictive coding model of repetition suppression. During this time window temporal expectation effects were larger for alternating, compared to repeated, test stimuli. Statistically significant temporal expectation by stimulus repetition interactions were not found for later (230–609 ms) time windows. Our results provide further evidence that repetition suppression can reduce neural effects of expectation and surprise, indicating that there are multiple interactive mechanisms supporting sensory predictions within the visual hierarchy.
Highlights
Living organisms exhibit a remarkable ability to exploit statistical regularities and recurring patterns that occur within sensory environments
To provide a more specific test of temporal expectation effects on RS, we presented pairs of repeated and alternating faces separated by 500 ms and 1000 ms interstimulus intervals (ISIs)
Accuracy did not differ for targets following expected compared to surprising ISIs
Summary
Living organisms exhibit a remarkable ability to exploit statistical regularities and recurring patterns that occur within sensory environments. Repetition suppression (RS) refers to a reduction in a recorded signal of neuronal activity (e.g. firing rate, local field potential amplitude, fMRI BOLD signal change) to repeated compared to unrepeated stimuli (Henson et al, 2004; De Baene and Vogels, 2010; for reviews see Grill-Spector et al, 2006; Kohn, 2007; Vogels, 2016; Larsson et al, 2016). Repetition effects have been reported when recording EEG/MEG (e.g., Caharel et al, 2015; Feuerriegel et al, 2018a) These effects are widely believed to index RS, due to almost ubiquitous findings of suppression (rather than enhancement) of neural responses when using similar experimental designs combined with different recording modalities (e.g., single unit firing rates: Sawamura et al, 2006; local field potentials: De Baene and Neuropsychologia 122 (2019) 76–87
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