Objectives
There is some discrepancy in the results regarding emotional enhancement of memory (EEM) in Alzheimer's disease (AD). Some studies report better retrieval of emotional information, especially positive, than neutral information. This observation is similar to the positivity effect reported in healthy older adults. It was suggested that this effect is due to privileged, deeper and more controlled processing of positive information. One way of testing this is to control both the intention to encode the information and the cognitive resources involved during encoding. Studies investigating EEM in AD patients did not systematically control the nature of encoding. Consequently, the purpose of our study was to examine EEM in AD while manipulating the nature of encoding.
Methods
Two experiments were conducted. In Experiment 1 the intention to encode stimuli was manipulated by giving or not giving instructions to participants about the subsequent retrieval. In Experiment 2 cognitive resources involved during encoding were varied (low vs high). In both experiments participants performed immediate recognition task of negative, positive and neutral pictures. 41 mild AD patients and 44 older healthy adults participated in Exp. 1, and 17 mild AD patients and 20 older healthy adults participated in Exp. 2.
Results
AD patients did not present EEM. Positivity effect, better performance for positive than neutral and negative pictures was observed with older healthy adults.
Conclusion
The data suggest that EEM is disturbed in mild AD patients, with respect to both negative and positive stimuli, at least concerning laboratory, not real-life material. They also suggest there is a positivity effect in healthy older adults and lend support to the idea that this effect is due to preferential cognitive processing of positive information in this population.
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Numerous studies have described better declarative memory for emotional stimuli (negative and positive) than for neutral stimuli in healthy young and older participants (see Reisberg & Heuer, 2004, for review). According to the evidences from both studies involving patients with amygdala lesions and neuroimaging studies, emotional enhancement of memory (EEM) is particularly reliant on the amygdala (Cahill et al., 1996 and Kensinger and Schacter, 2006). It has been suggested that EEM is based on not only the modulation the amygdala exerts on hippocampal memory consolidation processes, but also on the interaction between the amygdala and other brain regions (for review, see Canli et al., 2000, McGaugh, 2000 and Vuilleumier et al., 2004). Accordingly, it has been proposed that EEM may be based on two different mechanisms, one related to the influence of the amygdala on consolidation processes (consolidation-mediation hypothesis) and the other based on how the amygdala influences attention processes (attention-mediation hypothesis) (Talmi, Anderson, Riggs, Caplan, & Moscovitch, 2008). The latter hypothesis is particularly relevant when retrieval occurs immediately after encoding.
EEM was also investigated in patients with Alzheimer's disease (AD), given the neuropathological changes in the medial temporal lobes, including the amygdala, observed in the early stages of the disease. However, data regarding the presence of EEM in AD patients are fairly inconsistent (e.g., Kazui et al., 2003 and Kensinger et al., 2002). In the present study we investigated if encoding conditions may influence presence of EEM in AD patients, in immediate picture recognition task. In particular, we were interested in the influence of the intention to encode or not to encode the material and of the cognitive resources involved during encoding.
In the present study we tested emotional memory enhancement (EEM) in mild to moderate AD patients in the context of laboratory task with pictorial stimuli. We were particularly interested in the positivity effect, as some authors had suggested that this effect is characteristic of older adults. In Experiment 1 we used two types of encoding: intentional and incidental. We observed a positivity effect in older adults, regardless of intention to encode. Experiment 1 consequently confirms the positivity effect in older adults and backs the idea that it emerges because older adults focus more on positive than negative information and process this information more deeply. The data from Experiment 2 suggest that the intention to encode may play some part in this effect. Although the HR encoding task in Experiment 2 was identical to the incidental encoding task in Experiment 1, the positivity effect on memory recognition in older adults was not observed in Experiment 2. One explanation for this discrepancy in our results may be that the incidental encoding task was contaminated in some way by the intentional encoding task, given that our participants performed both encoding conditions. However, the order of the two tasks was counterbalanced between participants. The suggestion is that the positivity effect observed in Experiment 1 was principally driven by the intentional encoding task. Although we did not observe any significant interaction between encoding and valence in this experiment, the results regarding the recognition of previously seen positive, negative and neutral pictures after incidental encoding reveal almost no difference in performance for these stimuli (see Table 2). The difference is only apparent after intentional encoding.
We failed to show a positivity effect in AD patients. Our study therefore suggests there is no EEM in AD patients as regards negative and positive pictorial information. It is possible, however, that this enhancement could be observed with other types of stimuli (ex. Boller et al., 2002 and Fleming et al., 2003) or more ecological material (ex. Budson et al., 2004; Kazui et al., 2000), as demonstrated by some authors. Furthermore, it could also depend on the progression of the atrophy of mediotemporal structures, in particular the amygdala (Landré et al., 2013 and Perrin et al., 2012).
In conclusion, our data suggest that EEM is disturbed in mild to moderate AD patients, with respect to both negative and positive pictorial stimuli. Nonetheless, they do not rule out the possibility that this effect may be preserved, as tested with other types of material (words, stories or more ecological stimuli). Our study also suggests there is a positivity effect in healthy older adults and it is consistent with the idea that this effect is due to preferential cognitive processing of positive information in older adults.
