Level of Processing Modulates the Neural Correlates of Emotional Memory Formation

Abstract

Emotion is known to influence multiple aspects of memory formation, including the initial encoding of the memory trace and its consolidation over time. However, the neural mechanisms whereby emotion impacts memory encoding remain largely unexplored. The present study employed a levels-of-processing manipulation to characterize the impact of emotion on encoding with and without the influence of elaborative processes. Participants viewed emotionally negative, neutral, and positive scenes under two conditions: a shallow condition focused on the perceptual features of the scenes and a deep condition that queried their semantic meaning. Recognition memory was tested 2 days later. Results showed that emotional memory enhancements were greatest in the shallow condition. FMRI analyses revealed that the right amygdala predicted subsequent emotional memory in the shallow more than deep condition, whereas the right ventrolateral prefrontal cortex demonstrated the reverse pattern. Furthermore, the association of these regions with the hippocampus was modulated by valence: the amygdala-hippocampal link was strongest for negative stimuli, whereas the prefrontal-hippocampal link was strongest for positive stimuli. Taken together, these results suggest two distinct activation patterns underlying emotional memory formation: an amygdala component that promotes memory during shallow encoding, especially for negative information, and a prefrontal component that provides extra benefits during deep encoding, especially for positive information.Memories tinged with emotional salience tend to be remembered better and with greater vividness than emotionally neutral memories (Dolcos, Labar, & Cabeza, 2005;Ochsner, 2000). This influence of emotion on memory has been demonstrated to operate on multiple memory processes, including encoding--the initial formation of a memory trace (Dolcos, LaBar, & Cabeza, 2004a;Kensinger & Corkin, 2004)--and consolidation--the strengthening of this memory trace over time (LaBar & Phelps, 1998). Previous studies of emotional memory have tended to emphasize the role of consolidation processes in mediating these enhancements, driven by neurohormonal interactions between the amygdala and medial temporal lobe (MTL) memory system (McGaugh, 2004). Human neuroimaging has likewise demonstrated the importance of the amygdala and MTL memory system in promoting emotional memory formation. These regions tend to predict subsequent memory accuracy for emotional relative to neutral stimuli (Cahill, et al., 1996;Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000;Dolcos, LaBar, & Cabeza, 2004b;Hamann, Ely, Grafton, & Kilts, 1999;Kensinger & Corkin, 2004), and demonstrate enhanced functional coupling during emotional memory encoding (Dolcos, et al., 2004b;Hamann, et al., 1999;Richardson, Strange, & Dolan, 2004). Consistent with a consolidation account, interactions between the amygdala and MTL memory system increasingly predict emotional memory over time (Ritchey, Dolcos, & Cabeza, 2008 Despite this emphasis on consolidati...

Neural Correlates of Emotional Memories: A Review of Evidence From Brain Imaging Studies

“…2) (Dolcos et al, 2004b). Neuroimaging evidence also revealed that the increased AMY activation during memory formation may depend on the level-of processing during encoding (Ritchey, Labar, & Cabeza, 2011) and be related to the subjective vividness of subsequent memory regardless of arousal and valence (Kensinger, Addis, & Atapattu, 2011). The latter finding suggests that AMY's involvement may not be always a sign of encoding more details but rather seems to correspond to the subjective feeling of vivid memory.…”

“…This manipulation revealed that the AMY-MTL connectivity during encoding was greater for items retrieved after a longer delay, thus suggesting that AMY-MTL interactions underlie consolidation and persistence of emotional memories over time. Recent evidence also shows that although activity in AMY and MTL is driven primarily by arousal, their interaction may depend on valence (Ritchey et al, 2011). Namely, the study by Ritchey et al (2011) showed that the AMY-MTL interaction was stronger for encoding of negative stimuli, while the interaction between MTL and prefrontal cortex (PFC) was stronger for encoding of positive stimuli (see below.…”

“…Recent evidence also shows that although activity in AMY and MTL is driven primarily by arousal, their interaction may depend on valence (Ritchey et al, 2011). Namely, the study by Ritchey et al (2011) showed that the AMY-MTL interaction was stronger for encoding of negative stimuli, while the interaction between MTL and prefrontal cortex (PFC) was stronger for encoding of positive stimuli (see below. for a discussion on PFC and valence effect), although the basic activation pattern in these regions was not modulated by valence (Ritchey et al, 2011).…”

“…Namely, the study by Ritchey et al (2011) showed that the AMY-MTL interaction was stronger for encoding of negative stimuli, while the interaction between MTL and prefrontal cortex (PFC) was stronger for encoding of positive stimuli (see below. for a discussion on PFC and valence effect), although the basic activation pattern in these regions was not modulated by valence (Ritchey et al, 2011). These findings suggest that the effect of valence may not be always reflected in the overall activity of emotion-and memory-related regions, but it may emerge at the level of their interactions (Mickley Steinmetz, Addis, & Kensinger, 2010), thus revealing a more complex effect of valence on AMY activity and its interactions.…”

Memory for Emotional Picture Cues During Acute Alcohol Intoxication

“…Processing of emotionally laden memories has been associated with unique neural (Ritchey et al, 2011) and autonomic nervous system responses (Buchanan and Lovallo, 2001;Cahill and McGaugh, 1998;Garcia et al, 2011;Schwabe et al, 2008). These distinct brain and body responses to emotional stimuli result, at least in part, from the plicit memory).…”