Differential effects of negative emotion on memory for items and associations, and their relationship to intrusive imagery

Abstract

A crucial aspect of episodic memory formation is the way in which our experiences are stored within a coherent spatio-temporal context. We review research that highlights how the experience of a negative event can alter memory encoding in a complex manner, strengthening negative items but weakening associations with other items and the surrounding context. Recent evidence suggests that these opposing effects can occur through amygdala up-modulation to facilitate item encoding, while the hippocampal provision of contextual binding is down-modulated. We consider how these characteristics of memory for negative events might contribute to the development and maintenance of distressing intrusive imagery in posttraumatic stress disorder, and how they should influence therapeutic interventions.

Figure 1

(a) To assess, item and item–context memory, participants studied neutral and negative items presented on neutral background contexts. Memory was tested for the items and the associations between the items and their context. (b) Whilst memory for negative items is enhanced, memory for associations between the negative items and their neutral context is impaired. (c and d) To rule out the effect of attentional capture by the negative item itself, participants were instructed that certain contexts were predictive of a mild electrical shock. Whilst recognition memory for neutral and negative items was unaffected by safe and threatening contexts, associative memory for the context of neutral items was disrupted in the threatening context [27].

Figure 2

(a) Participants encoded paired associates of neutral and negative images. Memory was tested by presenting one item from each pair and asking participants if they recognized the item and if so, to identify the image it was paired with from a list of descriptions. (b) Recognition of negative item cues was better than for neutral items. (c) Associative memory was reduced by the presence of negative items at encoding. (d) Increased amygdala activity at encoding was predictive of subsequent item memory, whereas the hippocampus supported associative memory (e). Hippocampal activity was reduced by the presence of negative items at encoding. (f) At retrieval, increases in amygdala activity predicted negative item recognition. (g) The presence of a negative item cue reduced hippocampal activity during associative retrieval. (h) Amygdala activity increased when retrieving a negative associate from memory even when the cue was neutral, corresponding to a boost in retrieval of negative associates (c) [32^•].

Figure 3

Schematic dual representation model. Green lines: In memory for neutral events items represented in perirhinal cortex (PRC) are bound together with the corresponding context (parahippocampal gyrus, PHG) in the hippocampus (HPC). Voluntary retrieval can be initiated by ‘top-down’ input from prefrontal cortex (PFC), reconstructing an allocentric representation of the scene of the event via pattern completion in the medial temporal lobe (MTL, dashed green line), translated via retrosplenial cortex (RSC) to produce egocentric imagery in the Precuneus (following [59•, 60•]). The resulting scene is consistent with the viewpoint indicated by HPC place cells and the view direction indicated by head-direction cells. Red lines: For traumatic events, strong sensory/affective item representations are also formed in the Insula, PRC and Sensory areas via processing in the amygdala. In healthy memory, voluntary retrieval of a traumatic event occurs via the hippocampal system under control from PFC (green lines). However, following a traumatic event, intrusive imagery may occur due to an imbalance between strongly represented negative content, boosted by the amygdala (red lines), and contextual representations rendered weak and fragmented by reduced associative processing in the rest of the MTL (green dashed lines). This allows reactivation of negative content to be triggered via environmental cues and experienced as distressing imagery in precuneus, outside of its associated context [6^••].