Abstract
According to predictive accounts of perception, visual cortical regions encode sensory expectations about the external world, and the violation of those expectations by inputs (surprise). Here, using multi-voxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data, we asked whether expectations and surprise activate the same pattern of voxels, in face-sensitive regions of the extra-striate visual cortex (the fusiform face area or FFA). Participants viewed pairs of repeating or alternating faces, with high or low probability of repetitions. As in previous studies, we found that repetition suppression (the attenuated BOLD response to repeated stimuli) in the FFA was more pronounced for probable repetitions, consistent with it reflecting reduced surprise to anticipated inputs. Secondly, we observed that repetition suppression and repetition enhancement responses were both consistent across scanner runs, suggesting that both have functional significance, with repetition enhancement possibly indicating the build up of sensory expectation. Critically, we also report that multi-voxels patterns associated with probability and repetition effects were significantly correlated within the left FFA. We argue that repetition enhancement responses and repetition probability effects can be seen as two types of expectation signals, occurring simultaneously, although at different processing levels (lower vs. higher), and different time scales (immediate vs. long term).
Highlights
Understanding the mechanisms by which visual objects, faces and scenes are recognized is a key question for psychologists and neuroscientists (Logothetis and Sheinberg, 1996)
When participants viewed sequences of 3–4 presentations of a unique face, fusiform face area” (FFA) voxels exhibiting decreasing and increasing responses along the sequence constituted two populations that were segregated consistently across runs, responded at differing latencies, and exhibited different patterns of connectivity. These results suggested that repetition suppression and repetition enhancement responses may have distinct functional roles, and perhaps map onto distinct populations of neurons that encode surprise and expectation, respectively
For both region of interest (ROI), we extracted peri-stimulus time histograms (PSTHs) of the BOLD response for our four trial types (Figure 2B), and conducted an ANOVA on the amplitudes of the peak of these responses, with repetition and repetition probability manipulations as within participants factors. This analysis confirmed that both the left and right FFA regions of interest were sensitive to repetition [left: F(1, 15) = 16.71, p = 0.001; right: F(1, 15) = 24.78, p = 0.0001] and to the interaction between repetition and repetition probability [left: F(1, 15) = 6.93, p = 0.019; right: F(1, 15) = 5.38, p = 0.035], with a marginal trend for a main effect of repetition probability in the right FFA [F(1, 15) = 3.79, p = 0.07]
Summary
Understanding the mechanisms by which visual objects, faces and scenes are recognized is a key question for psychologists and neuroscientists (Logothetis and Sheinberg, 1996). According to one proposal known as “predictive coding” (Friston, 2005), perceptual inference depends on two distinct classes of signal: top-down signals encode predictions about the forthcoming stimulus, while feedforward signals convey the difference between the predicted and observed inputs, a “surprise” signal not dissimilar to the “prediction error” observed for rewards in dopaminergic neurons of the midbrain (Schultz et al, 1997) and the anterior cingulate cortex (Matsumoto et al, 2007) This scheme emphasizes the dual role of expectation and surprise signals in sensory processing, and predicts that these two types of signals should be distinguishable in the visual brain
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