Repetition suppression of faces is modulated by emotion

Abstract

Single-unit recordings and functional brain imaging studies have shown reduced neural responses to repeated stimuli in the visual cortex. By using event-related functional MRI, we compared the activation evoked by repetitions of neutral and fearful faces, which were either task relevant (targets) or irrelevant (distracters). We found that within the inferior occipital gyri, lateral fusiform gyri, superior temporal sulci, amygdala, and the inferior frontal gyri/insula, targets evoked stronger responses than distracters and their repetition was associated with significantly reduced responses. Repetition suppression, as manifested by the difference in response amplitude between the first and third repetitions of a target, was stronger for fearful than neutral faces. Distracter faces, regardless of their repetition or valence, evoked negligible activation, indicating top-down attenuation of behaviorally irrelevant stimuli. Our findings demonstrate a three-way interaction between emotional valence, repetition, and task relevance and suggest that repetition suppression is influenced by high-level cognitive processes in the human brain.

Fig. 1.

A network of face-responsive regions. Shown from left to right are coronal sections illustrating activation in the inferior occipital gyri (IOG, y = -75), FG and STS (y = -55), the amygdala (y = -8), and the IFG/insula (y = 22). The far right image shows vertical lines on whole-brain image indicate location of these sections. Data were averaged across all 13 subjects.

Fig. 2.

Activation evoked by targets. The mean amplitudes of the fMRI signal were averaged across all subjects and all repetitions of each event in each subject. In this and subsequent graphs, error bars indicate SEM. Response to neutral and fearful faces is color coded in blue and red, respectively. E indicates target encoding.

Fig. 3.

Target repetition suppression index in face-responsive regions. The index was calculated by subtracting the response amplitude during the third repetition of a target from its first repetition divided by their sum. L, left hemisphere; R, right hemisphere; AMG, amygdala.

Fig. 4.

Activation evoked by distracters. The mean amplitudes of the fMRI signal were averaged across all subjects and all repetitions of novel, neutral distracters (N, black bars), repeated neutral (blue), and repeated fearful (red) distracters.

Fig. 5.

Comparison between activations evoked by repetition of targets and distracters. Mean amplitudes were averaged across both hemispheres of all face-responsive regions in all subjects. Solid and broken lines indicate targets and distracters, respectively. N, neutral; F, fearful; T, targets; D, distracters.