fMRI studies of successful emotional memory encoding: A quantitative meta-analysis

Abstract

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.

Event-Related Nociceptive Arousal Enhances Memory Consolidation for Neutral Scenes

“…The majority of human studies of the EEM explore differences during encoding of emotionally arousing and neutral stimuli. Enhanced amygdala activity is consistently observed for successful encoding of emotional stimuli, supporting the crucial role of this structure in the EEM (Murty et al, 2010), although single-cell recordings indicate that the amygdala also responds to neutral stimuli (Kreiman et al, 2000). Moreover, consistent with the proposed effect of arousal on consolidation, the memory benefit for emotional stimuli is more pronounced after longer retention intervals (Sharot et al, 2007).…”

“…However, because of the scenic stimulus material and the exclusive increase in familiarity-driven, acontextual recognition in the present setting, the parahippocampal activity presumably reflects scene processing (Doeller and Kaplan, 2011). An activity increase in this area has also been reported for successful encoding of emotionally arousing information (Murty et al, 2010). Therefore, this activity might reflect a common, arousal-induced process that does not depend on the initial processing based on the cognitive characteristics of emotional stimuli.…”

“…In contrast, fMRI studies consistently report greater amygdala activity during successful encoding of emotionally arousing stimuli and contexts (Erk et al, 2005;Murty et al, 2010). Also, autonomic measures are typically correlated with successful memory formation for emotionally arousing stimuli (Anderson et al, 2006;Buchanan et al, 2006;Abercrombie et al, 2008).…”

Functional organization of the hippocampal longitudinal axis

“…It should be noted that the origin of the homologous hippocampus-amygdala topographical projections in primates is more restricted in the sense that amygdala-projecting neurons are focally restricted to the most anterior (uncal) CA1 and prosubiculum 107 . This may explain why fMRI activations associated with emotional memory in humans are primarily anterior [108][109] (but see ref. 110 ).…”

Amygdala subnuclei response and connectivity during emotional processing

“…Through extensive interactions with cortical and other subcortical areas, the AG also modulates attention and perception (Adolphs et al, 2005;Pitkänen et al, 2000;Sah et al, 2003). Of particular interest is the AG's involvement in processing of emotionally relevant stimuli and encoding of emotionally salient memories (Dolcos et al, 2004;Kensinger, 2009;LeDoux and Schiller, 2009;Murty et al, 2010;Sergerie et al, 2008;Shafer and Dolcos, 2012).…”