The effect of threat on novelty evoked amygdala responses

Abstract

A number of recent papers have suggested that the amygdala plays a role in the brain's novelty detection circuit. In a recent study, we showed that this role may be specific to certain classes of biologically-relevant stimuli, such as human faces. The purpose of the present experiment was to determine whether other biologically-relevant stimuli also evoke novelty specific amygdala responses. To test this idea, we presented novel and repeated images of snakes and flowers while measuring BOLD. Surprisingly, we found that novel images of snakes and flowers evoke more amygdala activity than repeated images of snakes and flowers. Our results further confirm the robustness of the novelty evoked amygdala responses, even when compared with effects more traditionally associated with the amygdala. In addition, our results suggest that threatening stimuli may prime the amygdala to respond to other types of stimuli as well.

Figure 1. We presented novel and repeated images of snakes and flowers while measuring BOLD activity.

(a) We presented images sequentially for 8 seconds each in an event related design. All participants saw 5 presentations of novel snake (NS) and 5 presentations of novel flower (NF) images indicated by the light green and light purple outlines, respectively. In addition all saw 5 repetitions of one snake (RS) and one flower (RF) image, shown in dark green and dark purple respectively.

Figure 2. We sampled BOLD activity in the amygdala and hippocampus using anatomical regions of interest.

We defined the amygdala and hippocampus for each individual using Freesurfer, and sampled BOLD in native space activity using these regions of interest. The images in this figure show the axial, sagittal, coronal, and rendered view of the amygdala and hippocampus in Talairach space, collapsed across subjects.

Figure 3. Novel snakes and novel flowers drive BOLD activity in the amygdala and hippocampus.

(a,c) Line graphs represent BOLD timecourse in the amygdala (a) and hippocampus (c). (b,d) Bar graphs represent the percent signal change in the amygdala (b) and hippocampus (d) during the last two seconds of the stimulus period. All data points represent mean±SEM. (NS = novel snake, RS = repeated snake, NF = novel flower, RF = repeated flower).

Figure 4. Images of snakes and flowers evoke distinct patterns of activity in visual cortical areas.

(a) Series of axial sections displaying the results from the whole brain Snake>Flower comparison. Colors indicate size and direction of F-statistic depicted on brain slice, and correspond to the colors on the scale to the left. (b) Flowers evoke more activity than snakes in lower-level visual processing areas. (c) Snakes evoke more activity than flowers in higher-level visual processing areas. Bar graphs represent the percent signal change in the structures marked by the colored arrows.

Figure 5. Snakes were perceived as more threatening, and evoked larger SCRs than flowers.

(a) Participants rated snakes as more likely to predict an electrical stimulation than flowers. (b) Participants showed larger SCRs to snake images than flower images. Participants also showed larger SCRs to novel images than to repeated images. (SCR = skin conductance response, NS = novel snake, RS = repeated snake, NF = novel flower, RF = repeated flower).