Neural processing of emotional faces requires attention

Abstract

Attention gates the processing of stimuli relatively early in visual cortex. Yet, existing data suggest that emotional stimuli activate brain regions automatically, largely immune from attentional control. To resolve this puzzle, we used functional magnetic resonance imaging to first measure activation in regions that responded differentially to faces with emotional expressions (fearful and happy) compared with neutral faces. We then measured the modulation of these responses by attention, using a competing task with a high attentional load. Contrary to the prevailing view, all brain regions responding differentially to emotional faces, including the amygdala, did so only when sufficient attentional resources were available to process the faces. Thus, the processing of facial expression appears to be under top-down control.

Fig 1.

Experimental paradigm. While subjects fixated the faces, they indicated in alternating blocks of trials either whether the face was male or female (attended trials) or whether the bars were or were not of similar orientations (unattended trials). The dashed lines indicate the display regions attended on alternating blocks (not shown on actual displays). Stimuli are not drawn to scale.

Fig 2.

Attention and valence effects in the amygdala. (A) Arrows point to the amygdala. Attended faces compared with unattended faces evoked significantly greater activations for all facial expressions. The level of the coronal section is indicated on the small whole-brain inset. L, left; R, right. (B) Estimated responses for the left and right amygdala ROIs as a function of attention and valence. FA, fearful attended; FU, fearful unattended; HA, happy attended; HU, happy unattended; NA, neutral attended; NU, neutral unattended. Coordinates (x, y, z) for peak sites in the amygdala were: neutral, left, −20, −8, −9, right, 21, −4, −10; fearful, left, −18, −6, −10, right, 20, −5, −9; happy, left, −18, −5, −9, right, 21, −5, −9.

Fig 3.

Attention and valence effects in ventral occipitotemporal cortex. (A) Fearful faces compared with neutral faces (pooled across attentional conditions) evoked significantly greater activations. Arrows point to the fusiform gyrus. L, left; R, right. (B) Estimated responses for the right fusiform gyrus ROI as a function of attention and valence.

Fig 4.

Stimulus valence by attention interaction effects. Maps indicate voxels in which the valence effect was greater for attended compared with unattended conditions. (A) STS: interaction between valence and attention for fearful compared with happy faces. (B) VMPFC/OFC: interaction between valence and attention for fearful compared with happy faces. (C) Calcarine fissure (V1/V2): interaction between valence and attention for fearful compared with neutral faces. L, left; R, right.

Fig 5.

Coupling of activity between the amygdala and other brain regions. (A) Increases in the coupling between amygdala and visual cortical activity (V1/V2 and fusiform gyrus; see arrows) on attended compared with unattended trials (see Materials and Methods). (B) Contrast of fearful and neutral faces during attended trials, demonstrating a significant effect of valence in the fusiform gyrus. A threshold of P < 0.00001 (uncorrected) was used for both A and B (which show the y = −52 plane). L, left; R, right.