Opposing effects of negative emotion on amygdalar and hippocampal memory for items and associations

Abstract

Although negative emotion can strengthen memory of an event it can also result in memory disturbances, as in post-traumatic stress disorder (PTSD). We examined the effects of negative item content on amygdalar and hippocampal function in memory for the items themselves and for the associations between them. During fMRI, we examined encoding and retrieval of paired associates made up of all four combinations of neutral and negative images. At test, participants were cued with an image and, if recognised, had to retrieve the associated (target) image. The presence of negative images increased item memory but reduced associative memory. At encoding, subsequent item recognition correlated with amygdala activity, while subsequent associative memory correlated with hippocampal activity. Hippocampal activity was reduced by the presence of negative images, during encoding and correct associative retrieval. In contrast, amygdala activity increased for correctly retrieved negative images, even when cued by a neutral image. Our findings support a dual representation account, whereby negative emotion up-regulates the amygdala to strengthen item memory but down-regulates the hippocampus to weaken associative representations. These results have implications for the development and treatment of clinical disorders in which diminished associations between emotional stimuli and their context contribute to negative symptoms, as in PTSD.

Keywords: amygdala; associative memory; hippocampus; item memory.

Fig. 1

Encoding involved presentation of image pairs followed by a simple judgement of whether participants thought the two images went well together. At retrieval, participants were shown one image and instructed to try and remember the image that originally appeared with the cue image. Participants were then shown six options, including four descriptions for the possible target associate, a ‘new’ response and a ‘don’t know’ response. This was followed by a confidence rating on the participant’s response.

Fig. 2

Behavioural results showing proportions correct for (A) item recognition and (B) associative memory for each type of association collapsed across tests 1 and 2. Note that mixed associations (neutral-negative and negative-neutral) switch from test 1 (testing associations in one direction inside the scanner) to test 2 testing associations in the opposite direction performed outside the scanner). See Supplementary Figure S1 for memory data split by tests 1 and 2. Bars represent SE, *P < 0.05, **P < 0.01, ***P < 0.001.

Fig. 3

Encoding activity showing subsequent memory effects across emotional valence conditions. (A) A contrast of subsequent item hits vs misses identified the left amygdala (P <  0.001 uncorrected; −33, −6, −21). (B) Activations in the left anterior hippocampus predicted subsequent associative hits compared with misses (P < 0.05 FWE SVC; −21, −18, −15). Effects displayed on group average brains and thresholded at P < 0.005 uncorrected for display purposes.

Fig. 4

Retrieval activity related to item and associative memory (percent signal change figures show associative hits minus misses for each condition) across cue and target conditions. (A) Activity in the amygdala was increased for negative item memory (hits minus misses) compared with neutral item memory (P < 0.05 FWE SVC; −18, 0, −15). (B) We saw a significant activation in the left hippocampus (P = 0.07 FWE SVC; −27, −24, −9) for associative memory (associative hits minus misses) when cued with a neutral item vs a negative item. (C) Activity in the right amygdala increased during successful associative memory (associative hits minus misses) when retrieving a negative target associate compared with a neutral target (P < 0.05 FWE SVC; +30, +3, −15). Effects displayed on group average brains and thresholded at P < 0.005 uncorrected for display purposes.