تجدید چاپ: مطالعات FMRI رمزگذاری حافظه هیجانی موفق: متا تجزیه و تحلیل کمی

Over the past decade, fMRI techniques have been increasingly used to interrogate the neural correlates of successful emotional memory encoding. These investigations have typically aimed to either characterize the contributions of the amygdala and medial temporal lobe (MTL) memory system, replicating results in animals, or delineate the neural correlates of specific behavioral phenomena. It has remained difficult, however, to synthesize these findings into a systems neuroscience account of how networks across the whole-brain support the enhancing effects of emotion on memory encoding. To this end, the present study employed a meta-analytic approach using activation likelihood estimates to assess the anatomical specificity and reliability of event-related fMRI activations related to successful memory encoding for emotional versus neutral information. The meta-analysis revealed consistent clusters within bilateral amygdala, anterior hippocampus, anterior and posterior parahippocampal gyrus, the ventral visual stream, left lateral prefrontal cortex and right ventral parietal cortex. The results within the amygdala and MTL support a wealth of findings from the animal literature linking these regions to arousal-mediated memory effects. The consistency of findings in cortical targets, including the visual, prefrontal, and parietal cortices, underscores the importance of generating hypotheses regarding their participation in emotional memory formation. In particular, we propose that the amygdala interacts with these structures to promote enhancements in perceptual processing, semantic elaboration, and attention, which serve to benefit subsequent memory for emotional material. These findings may motivate future research on emotional modulation of widespread neural systems and the implications of this modulation for cognition.

Emotion influences multiple aspects of cognition, and the impact of emotion on memory processes has been particularly well studied. Emotion is known to modulate both non-declarative and declarative forms of memory (see LaBar & Cabeza, 2006 for a review). In particular, declarative memories for emotionally salient information tend to be enhanced relative to their neutral counterparts, marked by both improved memory accuracy for emotional information (Burke et al., 1992, Cahill et al., 1996, Dolcos et al., 2004a and Dolcos et al., 2004b; Dolcos, LaBar, & Cabeza, 2004b; LaBar & Phelps, 1998) as well as increased vividness of these memories (Dolcos et al., 2005, Ochsner, 2000, Sharot et al., 2004 and Sharot and Yonelinas, 2008). These enhancements are thought to arise from the beneficial influence of emotion on the initial encoding of a memory trace (Canli et al., 2000, Dolcos et al., 2004a and Kensinger and Corkin, 2004) and its consolidation, or strengthening, over time (Hamann et al., 1999, Kleinsmith and Kaplan, 1963, LaBar and Phelps, 1998 and Ritchey et al., 2008). At the behavioral level, emotion has robust but complex effects on declarative memory. Memory enhancements can be driven by either the intensity of the stimulus’ valence (how emotionally positive or negative it is) or its induced emotional arousal (see Kensinger, 2004 for a review). Arousal has an inverted-U relationship with memory, in that moderate levels of arousal lead to memory enhancements whereas very high levels lead to impairments (Liang et al., 1990 and Roozendaal et al., 1999). The impact of emotion on memory may also change depending on which features of the memorandum are tested. For example, it has been suggested that emotion differentially impacts the gist versus details of a memory (Burke et al., 1992, Heuer and Reisberg, 1992, Kensinger et al., 2006 and Kensinger et al., 2007b). The influence of emotion on detailed memory may be further modulated by whether details are central versus peripheral to the emotionally salient features of the stimulus, leading to memory enhancements or impairments, respectively (Christianson and Loftus, 1991, Kensinger et al., 2007a and Loftus, 1979). Thus emotion influences memory encoding in a complex manner. For these reasons, further investigation into the cognitive and neural mechanisms that support these processes is warranted. At the neural level, a wealth of evidence supports the participation of the amygdala and medial temporal lobes (MTL) in promoting emotional memory enhancements in both animals (McGaugh, 2004) and humans (Kensinger, 2004 and LaBar and Cabeza, 2006) for reviews. Recently, human neuroimaging has afforded the opportunity to examine memory processes across the entire brain; thus, there is now emerging evidence regarding the distributed neural systems that support emotional memory encoding. These neuroimaging studies have largely focused on the enhancing effects of emotion on declarative memory formation. The present meta-analysis seeks to quantitatively integrate these results, with an emphasis on how transient activations during encoding predict enhanced memory for emotional information.

In this meta-analysis, we aimed to characterize the neural systems that have been consistently associated with emotional memory formation. To this end, we used Activation Likelihood Estimates to identify regions that reliably show greater ESA for emotional versus neutral stimuli. These regions included regions within bilateral amygdala, anterior hippocampus, parahippocampal gyrus, ventral visual stream, ventral parietal cortex, and PFC. Some of these regions, such as the amygdala, anterior hippocampus, and parahippoccampal gyrus, have been significantly highlighted in previous animal, patient, and neuroimaging studies of emotional memory. The specific roles of the PFC, parietal cortex, and ventral stream during emotional memory encoding, however, have been seldom investigated, even though these regions have been extensively studied within other domains of cognitive neuroscience. The consistency of findings in these cortical targets underscores the importance of generating hypotheses regarding their participation in emotional memory formation. In particular, we propose that the amygdala interacts with these structures to promote enhancements in perceptual processing, semantic elaboration, and attention, which serve to benefit subsequent memory for emotional material. Because of the complexities inherent in understanding the intersection of emotion and memory, more research is warranted that breaks down these gross constructs into more detailed analysis of cognitive subprocesses and corresponding neural mechanisms.