Remembering one year later: Role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories
Florin Dolcos *, 
, 
, Kevin S. LaBar *, and Roberto Cabeza *
*Center for Cognitive Neuroscience, Duke University, Durham, NC 27708-0999; and Centre for Neuroscience, University of Alberta, Edmonton, AB, Canada T6G 2S2
Communicated by Dale Purves, Duke University Medical Center, Durham, NC, December 29, 2004 (received for review October 21, 2004)
The memory-enhancing effect of emotion can be powerful and long-lasting. Most studies investigating the neural bases of this phenomenon have focused on encoding and early consolidation processes, and hence little is known regarding the contribution of retrieval processes, particularly after lengthy retention intervals. To address this issue, we used event-related functional MRI to measure neural activity during the retrieval of emotional and neutral pictures after a retention interval of 1 yr. Retrieval activity for emotional and neutral pictures was separately analyzed for successfully (hits) vs. unsuccessfully (misses) retrieved items and for responses based on recollection vs. familiarity. Recognition performance was better for emotional than for neutral pictures, and this effect was found only for recollection-based responses. Successful retrieval of emotional pictures elicited greater activity than successful retrieval of neutral pictures in the amygdala, entorhinal cortex, and hippocampus. Moreover, in the amygdala and hippocampus, the emotion effect was greater for recollection than for familiarity, whereas in the entorhinal cortex, it was similar for both forms of retrieval. These findings clarify the role of the amygdala and the medial temporal lobe memory regions in recollection and familiarity of emotional memory after lengthy retention intervals.
affect | arousal | declarative memory | episodic memory | R-K paradigm
PNAS, February 15, 2005, vol. 102, no. 7, 2626-2631.
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Through evolution, the declarative memory system developed the ability to preferentially retain events that are relevant for survival, which are usually those associated with strong emotions and motivational goals (finding food, spotting a predator, etc.). Emotional arousal may enhance one or more of several memory stages, including the creation of new memory traces (encoding), the stabilization and persistence of these traces (consolidation and storage), and/or the final access to stored traces (retrieval). Yet, the vast majority of studies on the neural mechanisms of emotional memory have focused on early memory stages (encoding and consolidation), and very little information is available about retrieval, particularly after long retention intervals. Neurobiological theories of emotional memory will not be complete without an account of retrieval mechanisms. This issue also has implications for understanding dysfunctional accessibility of traumatic memory traces in affective disorders. To fill this void, we used event-related functional MRI (fMRI) to investigate the neural mechanisms underlying the long-term retrieval of emotional memories in healthy adults.
According to the modulation hypothesis, the memory-enhancing effect of emotional arousal reflects the influence of the amygdala (AMY) on the medial temporal lobe (MTL) memory system. Although much animal (1, 2) and functional neuroimaging (3–12) evidence links the memory-enhancing effect of emotional arousal to amygdalar modulation during encoding, it is not clear whether a similar mechanism operates also during retrieval. Evidence from the animal literature suggests that AMY is also involved during emotional memory retrieval (13), but the exact nature of this involvement is a matter of current debate (14, 15).
Similarly, a few functional neuroimaging studies in humans have found amygdalar activity during retrieval (16–20), but these studies have two main limitations: (i) they used short retention intervals (i.e., minutes), which do not allow a clear separation between the involvement of AMY in retrieval and early consolidation processes; and (ii) they did not demonstrate that AMY is differentially more involved in successful than in unsuccessful retrieval of emotional events relative to neutral events.
Thus, the first goal of the present fMRI study was to investigate the effect of emotional arousal on retrieval activity while addressing the two limitations of earlier studies: (i) to distinguish retrieval processes from early consolidation processes, we examined retrieval processes after a retention interval of 1 yr; and (ii) to specifically isolate activity associated with successful retrieval operations, we compared amygdalar and MTL memory system activity for successfully vs. unsuccessfully retrieved items, specifically contrasting old items classified as old (hits) to old items classified as new (misses).
The second goal of the study was to disentangle the effects of emotional arousal on two different forms of episodic memory retrieval: recollection and familiarity (21). Recollection refers to memory for an event (e.g., meeting someone) that is accompanied by the retrieval of contextual information and other associated elements (e.g., time, location, and sensory details), whereas familiarity refers to the feeling that an event happened in the past, but no associated information can be retrieved (e.g., knowing that a face was seen before but without remembering where or when). Distinguishing recollection and familiarity is critical, because there is behavioral evidence that the memory-enhancing effect of emotion specifically modulates recollection rather than familiarity processes (22, 23). However, the neural correlates of this differential effect are unknown. The fMRI studies that investigated recollection vs. familiarity either used neutral stimuli (24–26) or did not distinguish between successful and unsuccessful activity (20). Thus, the present study also investigated the effect of emotional arousal on the neural correlates of successful recollection vs. familiarity, an issue that has not been examined by previous studies.
In the present study, participants encoded high-arousing emotional (pleasant and unpleasant) and low-arousing neutral pictures by rating their valence, and 1 yr later, they were scanned while distinguishing between the pictures they previously saw and equivalent new pictures. Subjects performed a recognition task that distinguishes between recollection-based (R) and familiarity-based (K) responses (27). On the basis of behavioral evidence concerning the memory-enhancing effect of emotion (28, 29), we made a first prediction: (i) recognition would be better for emotional than for neutral pictures, and this effect would be driven mainly by recollection (22, 23). Concerning the neural basis of these effects, we made two additional predictions: (ii) on the basis of our encoding results (7), we predicted that emotion would enhance retrieval success activity (RS) in AMY and the MTL memory regions, specifically the hippocampus (HC) and the entorhinal cortex (EC); and (iii) we also predicted that R responses would be associated with greater activity than K response in AMY and HC but not in cortical MTL regions, such as EC. The AMY and HC were assumed to be the source of differential recollection vs. familiarity effects, because emotional arousal enhances recollective processes behaviorally, which have been more closely associated with hippocampal function than with other cortical MTL regions (21, 30).
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