Neural mechanisms of repetition priming of familiar and globally unfamiliar visual objects

Abstract

Functional magnetic resonance imaging (fMRI) studies have shown that repetition priming of visual objects is typically accompanied by a reduction in activity for repeated compared to new stimuli (repetition suppression). However, the spatial distribution and direction (suppression vs. enhancement) of neural repetition effects can depend on the pre-experimental familiarity of stimuli. The first goal of this study was to further probe the link between repetition priming and repetition suppression/enhancement for visual objects and how this link is affected by stimulus familiarity. A second goal was to examine whether priming of familiar and unfamiliar objects following a single stimulus repetition is supported by the same processes as priming following multiple repetitions within the same task. In this endeavor, we examined both between and within-subject correlations between priming and fMRI repetition effects for familiar and globally unfamiliar visual objects during the first and third repetitions of the stimuli. We included reaction time of individual trials as a linear regressor to identify brain regions whose repetition effects varied with response facilitation on a trial-by-trial basis. The results showed that repetition suppression in bilateral fusiform gyrus, was selectively correlated with priming of familiar objects that had been repeated once, likely reflecting facilitated perceptual processing or the sharpening of perceptual representations. Priming during the third repetition was correlated with repetition suppression in prefrontal and parietal areas for both familiar and unfamiliar stimuli, possibly reflecting a shift from top-down controlled to more automatic processing that occurs for both item types.

Figure 1

Examples of the types of stimuli used in this study.

Figure 2

Behavioral Results. Mean reaction time (on y-axis) for classifying familiar and unfamiliar objects as a function of presentation number (on x-axis). Error bars represent the standard error of the mean.

Figure 3

Brain regions showing between-subjects correlations between repetition suppression from presentation 1 to 2 and priming. For familiar objects, such correlations were detected in the right fusiform gyrus (A) and left fusiform gyrus (B). For unfamiliar objects, no such correlations were detected. The left panel shows areas demonstrating significant repetition suppression (contrast presentation 1 – 2, p < 0.001) for familiar objects. Areas showing the maximum correlation between repetition suppression and priming are circled in blue. Scatterplots of these correlations are displayed in the right panel. The middle panel shows mean fMRI activation for both types of objects at presentations 1, 2, and 4 at the coordinates displayed in the left panel. Note that both correlations were significant at the same threshold (right fusiform) or slightly lower threshold (left fusiform, p < 0.008) when the potential outlier was excluded from the GLM analysis.

Figure 4

Brain regions showing between-subjects correlations between repetition suppression from presentation 1 to 4 and priming. Such correlations were detected in the right inferior frontal gyrus/anterior insula for both familiar (A) and unfamiliar objects (D) and in the left precuneus (B) and right inferior parietal lobule (C), for the familiar objects only. The left panel shows areas demonstrating significant repetition suppression (contrast presentation 1 – 4, p < 0.001) for the familiar items. Areas showing the maximum correlation between repetition suppression and priming are indicated by the blue arrow. Scatterplots of these correlations are displayed in the right panel. The middle panel shows mean fMRI activation for the familiar objects at presentations 1 and 4 at the corresponding coordinates displayed in the left panel.

Figure 5

Brain regions where the magnitude of repetition suppression (thresholded at p < 0.001) for familiar (A) and unfamiliar (B) objects was modulated by reaction time priming on a within-subjects basis are displayed. For familiar objects, we detected voxels in the right fusiform gyrus (A, left panel) where repetition suppression from presentation 1 to 2 correlated with priming at presentation 2 across subjects (at p < 0.05) and within subjects (at p < 0.05), combined probability p < 0.0000025. From presentation 1 to 4, repetition suppression in the left precentral gyrus (A, right panel) correlated with priming of familiar objects (at p < 0.005) and repetition suppression in the right precuneus (B, left panel) and left inferior frontal gyrus (B, right panel) correlated with priming of unfamiliar objects (at p < 0.005).