Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge

Abstract

Functional magnetic resonance imaging (fMRI) of the human brain was used to study whether the amygdala is activated in response to emotional stimuli, even in the absence of explicit knowledge that such stimuli were presented. Pictures of human faces bearing fearful or happy expressions were presented to 10 normal, healthy subjects by using a backward masking procedure that resulted in 8 of 10 subjects reporting that they had not seen these facial expressions. The backward masking procedure consisted of 33 msec presentations of fearful or happy facial expressions, their offset coincident with the onset of 167 msec presentations of neutral facial expressions. Although subjects reported seeing only neutral faces, blood oxygen level-dependent (BOLD) fMRI signal in the amygdala was significantly higher during viewing of masked fearful faces than during the viewing of masked happy faces. This difference was composed of significant signal increases in the amygdala to masked fearful faces as well as significant signal decreases to masked happy faces, consistent with the notion that the level of amygdala activation is affected differentially by the emotional valence of external stimuli. In addition, these facial expressions activated the sublenticular substantia innominata (SI), where signal increases were observed to both fearful and happy faces--suggesting a spatial dissociation of territories that respond to emotional valence versus salience or arousal value. This study, using fMRI in conjunction with masked stimulus presentations, represents an initial step toward determining the role of the amygdala in nonconscious processing.

Fig. 1.

Masked fearful faces versus masked happy faces. Areas of significant activation (p < 6.6 × 10⁻⁴) across whole brain, presented here as 57, 3 mm coronal slices for the masked fear versus masked happy contrast, for the eight subjects who reported not having seen the fearful or happy target faces. All figures are displayed according to radiological convention (i.e., left = right; right = left; top = superior; bottom = inferior). The most anterior slice is in the top left corner, and slices proceed in a posterior direction from left to rightand then down. The colorized statistical map is superimposed over the averaged high-resolution structural data for these eight subjects. Both functional and structural data have been placed in a normalized space according to the coordinate system ofTalairach and Tournoux (1988). All figures were smoothed by using a Hamming nine voxel 1:2:1 kernel filter, although activations were significant on unsmoothed maps. Significant activation within the amygdaloid region is evident within two slices in the third row (yellow brackets). These two slices represent Talairach coordinates in the y-plane of 0 (see Fig. 3) and −6 (see Fig. 2), respectively. Note also the relative lack of activation across all other brain regions. There is an activation of the inferior prefrontal cortex (first row, slice nine) that met the significance level set a priori for the amygdala. Note that, although our 15 original horizontal slice acquisitions covered “whole brain,” susceptibility from the sinus space causes signal dropout in portions of some brain regions (see Results).

Fig. 2.

Top. Amygdala activation to masked fearful versus masked happy faces. A, Coronal display of the most posterior slice depicting activation within the region of the amygdala from Figure 1. Image parameters are as in Figure 1. Activation depicted here in the right amygdala includes four contiguous voxels that significantly increased in response to masked fearful faces when compared with masked happy faces (p < 6.6 × 10⁻⁴). B, Bar graph depicting changes in BOLD signal intensity as a function of repeated stimulus presentations. Bars represent the mean percentage change of signal intensity per epoch in response to masked fearful and masked happy faces (counterbalanced), as compared with the preceding and following low-level fixation conditions. Values reflect only the four voxels that exceeded the Bonferroni-corrected significance threshold (depicted within A) for the masked fearful versus masked happy contrast.