Dissociable contributions of the amygdala to the immediate and delayed effects of emotional arousal on memory

Abstract

Emotional arousal enhances memory encoding and consolidation leading to better immediate and delayed memory. Although the central noradrenergic system and the amygdala play critical roles in both effects of emotional arousal, we have recently shown that these effects are at least partly independent of each other, suggesting distinct underlying neural mechanisms. Here we aim to dissociate the neural substrates of both effects in 70 female participants using an emotional memory paradigm to investigate how neural activity, as measured by fMRI, and a polymorphism in the α_2B-noradrenoceptor vary for these effects. To also test whether the immediate and delayed effects of emotional arousal on memory are stable traits, we invited back participants who were a part of a large-scale behavioral memory study ∼3.5 yr ago. We replicated the low correlation of the immediate and delayed emotional enhancement of memory across participants (r = 0.16) and observed, moreover, that only the delayed effect was, to some degree, stable over time (r = 0.23). Bilateral amygdala activity, as well as its coupling with the visual cortex and the fusiform gyrus, was related to the preferential encoding of emotional stimuli, which is consistent with affect-biased attention. Moreover, the adrenoceptor genotype modulated the bilateral amygdala activity associated with this effect. The left amygdala and its coupling with the hippocampus was specifically associated with the more efficient consolidation of emotional stimuli, which is consistent with amygdalar modulation of hippocampal consolidation.

Figure 1.

Behavioral results. (Left panel) Corrected hit rates in the immediate and delayed memory test for negative (black) and neutral (gray) pictures from the current study and from the previous large-scale behavioral study of the same participants (solid bars—current fMRI study, contour bars—large-scale behavioral study). (Middle panel) Correlations between the immediate and delayed emotional enhancement of memory (iEEM and dEEM, respectively) across participants in the current study. Exclusion of the outlier changes correlation to r = 0.14. (Right panel) Correlations of iEEMs and of dEEMs between the current study and the previous large-scale behavioral study of the same participants.

Figure 2.

Mean amygdala and hippocampal activity associated with iEEM and dEEM: Results of the ROI-based analyses. Mean activity across all voxels in the left and right amygdala and side-matched hippocampus ROIs. Immediate and delayed EEM are shown.

Figure 3.

Amygdala activity associated with iEEM and dEEM: Results of the peak voxel-based analyses. (Upper panel) Activity in the bilateral amygdala correlated with iEEM. (Lower panel) Activity in the left amygdala/anterior hippocampus correlated with dEEM. Negative and neutral SMEs, i.e., activity during subsequent hits minus misses, in the immediate (iSMEs) and delayed (dSMEs) tests are shown. Importantly, parameter estimates are shown only for the peaks that survived the exclusive masking with the opposing EEM contrast and therefore represent the largest observed differences between activities associated with iEEM and dEEM in the given brain areas. The solid bars represent the effect (iEEM or dEEM) that was significant in the area plotted, the contour bars the effects used as exclusive mask.

Figure 4.

Amygdala coupling related to iEEM and dEEM. (Left panel) The cluster in the left amygdala identified by the main effect of emotion (white circle) served as seed region for the connectivity analyses. (Middle panel) The amygdala was more strongly coupled with the bilateral fusiform, lingual, and middle occipital gyri during successful encoding related to iEEM. (Right panel) The amygdala was more strongly coupled with the bilateral hippocampi, fusiform, lingual, middle occipital, and inferior frontal during processing of negative than neutral pictures that were successfully consolidated. Importantly, the parameter estimates are shown for the peaks that survived the exclusive masking with the opposing EEM contrast and therefore represent the largest observed difference between activities associated with iEEM and dEEM in the given brain areas. The solid bars represent the effect (iEEM or dEEM) that was significant in the given area, the contour bars the effects used as exclusive mask.

Figure 5.

Interaction of α_2B-adrenocepor genotype and amygdala activity associated with iEEM. Activity in the bilateral amygdala correlated more strongly with iEEM in wild-type than with α_2B-adrenocepor deletion carriers. Negative and neutral SMEs for iEEM are shown for both genotype groups.