Amygdala-prefrontal dissociation of subliminal and supraliminal fear

Abstract

Facial expressions of fear are universally recognized signals of potential threat. Humans may have evolved specialized neural systems for responding to fear in the absence of conscious stimulus detection. We used functional neuroimaging to establish whether the amygdala and the medial prefrontal regions to which it projects are engaged by subliminal fearful faces and whether responses to subliminal fear are distinguished from those to supraliminal fear. We also examined the time course of amygdala-medial prefrontal responses to supraliminal and subliminal fear. Stimuli were fearful and neutral baseline faces, presented under subliminal (16.7 ms and masked) or supraliminal (500 ms) conditions. Skin conductance responses (SCRs) were recorded simultaneously as an objective index of fear perception. SPM2 was used to undertake search region-of-interest (ROI) analyses for the amygdala and medial prefrontal (including anterior cingulate) cortex, and complementary whole-brain analyses. Time series data were extracted from ROIs to examine activity across early versus late phases of the experiment. SCRs and amygdala activity were enhanced in response to both subliminal and supraliminal fear perception. Time series analysis showed a trend toward greater right amygdala responses to subliminal fear, but left-sided responses to supraliminal fear. Cortically, subliminal fear was distinguished by right ventral anterior cingulate activity and supraliminal fear by dorsal anterior cingulate and medial prefrontal activity. Although subcortical amygdala activity was relatively persistent for subliminal fear, supraliminal fear showed more sustained cortical activity. The findings suggest that preverbal processing of fear may occur via a direct rostral-ventral amygdala pathway without the need for conscious surveillance, whereas elaboration of consciously attended signals of fear may rely on higher-order processing within a dorsal cortico-amygdala pathway.

Figure 1

Mean and standard error for the amplitude of skin conductance responses (SCRs) in microsiemens for supraliminal presentations of fear (F‐Supra) and neutral (N‐Supra) and for subliminal presentations of fear (F‐Sub) and neutral (N‐Sub). ANOVA showed that SCRs were higher for fear relative to neutral for both supraliminal and subliminal conditions, although SCRs were generally greater in the supraliminal condition. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

A–D: Statistical parameter maps (SPMs at P < 0.05_{small volume corrected}), overlaid on the canonical T1 images, derived from the Montreal Neurological Institute. Images are in neurological orientation (left hemisphere = left of image). SPMs are for within‐ and between‐condition contrasts of supraliminal and subliminal fear, relative to a neutral baseline, for the regions of interest: amygdala, ventral (vACC) and dorsal anterior cingulate cortex (dACC), and connected ventral (vMPFC) and dorsal (dMPFC) portions of the medial prefrontal cortex. The within‐condition contrast of supraliminal fear relative to neutral elicited significant responses in the left amygdala (A, image on left) and left dACC/dMPFC (A, image on right). The contrast of subliminal fear relative to neutral elicited significant activity in the bilateral amygdala (B, image on left) and vACC (B, image on right). In between‐condition contrasts, supraliminal fear was distinguished by significantly greater responses in the bilateral amygdala, most pronounced in the left amygdala, and in the dACC and dMPFC (C), whereas subliminal fear was distinguished by relatively greater activity in the vACC (D). The 3D images (bottom row) illustrate further the distinction between conditions in prefrontal responses: whereas supraliminal fear was distinguished by greater responses in the dorsal ACC, supraliminal fear was distinguished by greater responses in the ventral ACC. The standardized anatomical coordinates for these regions of activity are presented in Table I.

Figure 3

The percentage blood oxygenation level‐dependent (BOLD) signal change and standard error for supraliminal and subliminal fear, relative to a neutral baseline, for the regions of interest: left (A) and right (B) amygdala, and both left (C) and right (D) dorsal portions of the anterior cingulate cortex (ACC) and left (E) and right (F) ventral portions of the ACC. In each graph, bars depict signal change for the full experimental time course (total), and for the early and late phases of the time course. The total percentage signal change is included as a frame of reference to findings from image analyses. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]