Resting-state connectivity of the amygdala is altered following Pavlovian fear conditioning

Abstract

Neural plasticity in the amygdala is necessary for the acquisition and storage of memory in Pavlovian fear conditioning, but most neuroimaging studies have focused only on stimulus-evoked responses during the conditioning session. This study examined changes in the resting-state functional connectivity (RSFC) of the amygdala before and after Pavlovian fear conditioning, an emotional learning task. Behavioral results from the conditioning session revealed that participants learned normally and fMRI data recorded during learning identified a number of stimulus-evoked changes that were consistent with previous work. A direct comparison between the pre- and post-conditioning amygdala connectivity revealed a region of dorsal prefrontal cortex (PFC) in the superior frontal gyrus that showed a significant increase in connectivity following the conditioning session. A behavioral measure of explicit memory performance was positively correlated with the change in amygdala connectivity within a neighboring region in the superior frontal gyrus. Additionally, an implicit autonomic measure of conditioning was positively correlated with the change in connectivity between the amygdala and the anterior cingulate cortex (ACC). The resting-state data show that amygdala connectivity is altered following Pavlovian fear conditioning and that these changes are also related to behavioral outcomes. These alterations may reflect the operation of a consolidation process that strengthens neural connections to support memory after the learning event.

Keywords: amygdala; fMRI; fear conditioning; functional connectivity; resting-state.

Figure 1

Diagram of the phases in the experiment.

Figure 2

Participants demonstrate differential conditioning with UCS expectancy ratings and SCR. (A) Mean UCS expectancy ratings on CS+ and CS− trials during the conditioning task. (B) Mean SCR on CS+ and CS− trials during the conditioning task.

Figure 3

The left and right amygdala both demonstrate differential responses to the CSs in the conditioning phase of the experiment. (A) An amygdala probability mask created by combining each participant's anatomical amygdala ROI. The color scale corresponds to the probability that the region is included in any of the participants' amygdala ROIs. Black indicates a low probability and bright green indicates high probability. (B) Bar graph depicting the AUC values for both the CS+ and CS− evoked BOLD response in the right amygdala during the conditioning task. (C) Bar graph depicting the AUC values for both the CS+ and CS− evoked BOLD response in the left amygdala during the conditioning task.

Figure 4

Amygdala functional connectivity before and after the conditioning task shows some similarities and some differences. Brain images depict the pre- and post-conditioning connectivity maps as well as where those maps overlap.

Figure 5

The dorsal medial prefrontal cortex (superior frontal gyrus) [Talairach coordinates: 24, 30, 45] shows a significant increase in its connectivity with the amygdala following the conditioning task. The colors on the brain map correspond to the t-values on the color scale.

Figure 6

Changes in amygdala connectivity are related to behavioral performance. (A) Connectivity changes between the amygdala and the superior frontal gyrus [Talairach coordinates: 11, 48, 9] are positively correlated with UCS expectancy performance during the conditioning task. (B) Scatter plot depicting UCS expectancy performance and change in connectivity between the amygdala and superior frontal gyrus. (C) Connectivity changes between the amygdala and the ACC [Talairach coordinates: 3, 13, −5] are positively correlated with SCR performance during the conditioning task. (D) Scatter plot depicting SCR performance and change in connectivity between the amygdala and the ACC.