Center for Cognitive Neuroscience
Department of Psychology and Neuroscience
Emotional memories dominate our life histories. How are emotionally-laden events prioritized in the brain and linked to neural systems that promote memory? This question has been at the forefront of affective neuroscience for decades but has received renewed attention as advances in imaging methodology have permitted more detailed accounts of neural interactions that contribute to complex human behaviors. A classic account of these brain mechanisms (the memory modulation hypothesis) postulated that emotionally-arousing episodes receive preferential consolidation into long-term storage through interactions between the amygdala and adjacent sectors of the medial temporal lobe, including the hippocampus and entorhinal cortex (McGaugh, 2004). This hypothesis was extensively supported by non-human animal research and provided a neural mechanism to explain how significant events like those that cause stress are promoted and selectively retained in long-term memory, relative to more mundane experiences. Human neuroimaging research has confirmed that these brain structures are more intensely engaged, and their activity is more tightly coupled, during the encoding of emotionally-arousing – relative to neutral – material in a manner that predicts long-term memory retention (for a meta-analysis, see Murty et al. 2010). For instance, when participants are shown pictures that vary in emotional content, those that are rated higher in arousal, such as erotic images or horror scenes, are better remembered than generic pictures of everyday events, such as people talking at a business meeting or walking down the street. Activity in and connectivity between the amygdala and adjacent medial temporal lobe structures in response to the emotional pictures predicts their retention advantage over neutral pictures on a subsequent memory test (Dolcos et al., 2005). Interestingly, these brain areas also predict subsequent memory even when their activity is spontaneously elicited in the resting baseline period before the stimulus appears (Mackiewicz et al., 2006), and when the amygdala activity is generated by a motivational threat cue that comes before the stimulus itself (Murty et al., 2012). Findings like these provided evidence for the brain-behavior relationships predicted by the memory modulation hypothesis and showed that the processes that consolidate emotional memories, originally discovered in rodents, are conserved in the human brain.
Failure to engage these brain systems can have detrimental consequences on emotional memory formation. Patients with amygdala damage due to epilepsy or congenital disorders (e.g., Urbach-Wiethe disease) do not exhibit the long-term retention advantages for arousing material, including emotionally intense portions of a story (Cahill et al., 1995) or emotionally evocative words (LaBar & Phelps, 1998). In another study, individuals with posttraumatic stress disorder (PTSD) exhibited reduced medial temporal lobe activity while encoding trauma-related scenes, particularly in individuals with high arousal symptoms (Hayes et al., 2011). Compared to trauma-exposed controls, those with PTSD had higher false alarm rates to trauma lures on the memory test. This pattern suggests that the material was encoded at a more superficial (gist-based) level, rather than a contextually rich, detailed level, which made the trauma lures on the memory test seem familiar. These functional alterations may contribute to the overgeneralized nature of traumatic memories in which autobiographical experiences get intertwined with other trauma-related material to exacerbate their negative impact.
At the same time, research has expanded the functional role of medial temporal lobe structures beyond enhanced memory consolidation to include processes related to memory retrieval accuracy and phenomenology. Notably, the same brain regions that promote memory consolidation at encoding work together to guide successful retrieval of emotionally arousing items from long-term storage (Botzung, Rubin, et al., 2010; Dolcos et al., 2005), including the recall of emotionally salient autobiographical events (Greenberg et al., 2005). The amygdala and hippocampus also contribute to the unique phenomenological experience of remembering that accompanies the retrieval of emotionally arousing events (Dolcos et al., 2005; Sharot et al., 2004), even when these memories are not more objectively accurate than neutral ones (Rimmele et al., 2011; Talarico & Rubin, 2003). The role of these brain regions thus extends beyond memory accuracy to include more subjective aspects of emotional remembering (how the memory feels when it is recalled rather than what is recalled). The subjective aspects of autobiographical memories, such as their emotional intensity and the visual imagery (reliving) that accompanies their re-experiencing, tend to be correlated (Talarico et al., 2004). Nonetheless, neuroimaging studies have shown that these features can be spatially and temporally segregated in the brain. When retrieving a specific autobiographical memory from a generic cue word like “wedding,” the amygdala signals the emotional intensity of the unfolding memory very early on in the process of its reconstruction, even before visual cortex activity emerges that signals the amount of reliving experienced while mentally traveling back in time to recall the event (Daselaar et al., 2008). In this way, the amygdala may bias memory selection from competing options (such as choosing one memory from among several life episodes involving a wedding), and it has access to the affective information associated with this event before the contextual details are fully retrieved from memory.
Neuroimaging meta-analyses have linked other brain systems to emotional memory processes beyond the medial temporal lobes, including regions of the frontal and parietal lobes involved in attentional and executive functions, and sensory processing areas, such as the fusiform gyrus (Murty et al., 2010). Theoretical accounts of emotional memory have expanded to incorporate these functions. The arousal-biased competition model (Mather & Sutherland, 2011) argues that high-priority stimuli compete with low-priority stimuli for access to limited cognitive resources, and that attentional factors and the goal-relevance of the stimuli will predict whether memory consolidation is enhanced or impaired. For instance, if a goal is to integrate emotionally salient stimuli with surrounding neutral information (as when learning facts about a potential medical treatment), then the neutral information may get incorporated into the emotional memory. Affective salience is signaled in part by the release of norepinephrine (NE) from the locus coeruleus, which fosters plasticity in the amygdala and prefrontal cortex and enhances sensory processing (Markovic et al., 2014). Pharmacologic manipulations of NE – a marker of sympathetic arousal – impact emotional memory consolidation by influencing neural activity in the amygdala and its interconnected brain regions (van Stegeren, 2008). Along with other neuromodulatory systems, NE may interact with glutamatergic-dependent long-term potentiation mechanisms to selectively support memory consolidation for high-priority stimuli in a competitive fashion (Mather et al., 2016).
The arousal-mediated memory consolidation and retrieval effects discussed above are not the only ways in which emotion impacts memory. The amount of attention paid to emotional stimuli at encoding, their distinctiveness relative to the surrounding context, and their semantic structure also bias memory processes, even at short time-scales before extensive consolidation occurs (Talmi, 2013). For instance, attentional and elaborative processes promote trade-offs in memory accuracy, particularly in aversive settings, whereby the central negative element of an emotional event tends to be overemphasized relative to peripheral contextual details (Mickley Steinmetz & Kensinger, 2013). Such accuracy trade-offs have important implications for eyewitness testimony in courtroom proceedings. Witnesses may selectively attend to and rehearse details focused on a weapon at a crime scene at the expense of important peripheral information, such as the identity of an accomplice (Mansour et al., 2017). By contrast, positive experiences often broaden attentional focus (Rowe et al., 2007), especially for lower-arousing events (Harmon-Jones et al., 2013), which can reduce central-peripheral trade-offs in memory (Chipchase & Chapman, 2013). Compared to positively valent memories, negatively valent memories exhibit greater recapitulation of sensory processing at retrieval, which confers greater vividness of the aversive visual elements of the memory (Bowen et al., 2018). Because this latter effect occurs even when arousal is equated across negative and positive memories, emotional valence is thought to have a specific role in memory processing. Thus valence (the positivity or negativity of the memory) can interact with attentional and sensory processing in different ways to bias memories for emotional material above and beyond the impact of arousal.
Through their influence on these various neurocognitive processes, emotional events can sometimes feel as though they are indelibly fixed in memory. However, researchers are now discovering that post-retrieval manipulations can, in some circumstances, alter the phenomenological characteristics of emotional memories. In one study, individuals used visual imagery to spatially distance themselves from reactivated memories of negative scenes by imagining that the scenes took place far away from them. Compared to individuals who didn’t reactivate the memory, reactivated the memory without regulating, or didn’t do anything, participants in the reactivate + regulate condition reported feeling less emotionally aroused when viewing the scenes several days later, despite having intact recognition memory for them (Parikh et al., 2019). Memories are thought to enter a labile state upon reactivation that provides a window of opportunity to therapeutically intervene by engaging specific regulatory strategies that have long-term benefits in mollifying emotional reactivity while maintaining memory accuracy (LaBar, 2015). Although the exact brain mechanisms remain unclear, cognitively mediated reappraisal strategies, like spatial distancing, may achieve their mnemonic effects by reducing amygdala activation to the emotional event while enhancing connectivity of the hippocampus and regulatory sectors of the prefrontal cortex (Hayes et al., 2010).
These advances in emotional memory research would not have been possible without integrating theoretical, behavioral, and neurobiological perspectives and the increased dialogue between basic scientists and clinicians who treat patients with affective and traumatic memory disorders. To provide an even stronger translational bridge, researchers should strive to increase the ecological validity of their experimental paradigms by incorporating complex facets of real-world emotional episodes, including their rich contextual details, social interactions, and temporal dynamics. In doing so, the laboratory paradigms will more closely approximate the real-life scenarios that the brain systems are designed to handle, which should improve an understanding of how emotional memories are impacted in mental health disorders. Validated databases of more complex emotional stimuli like movie clips (Cowen & Keltner, 2017) and news broadcasts (Samide et al., 2020) have been developed to aid researchers in these endeavors, along with virtual reality tools that present dynamic emotional stimuli in life-like 3-D worlds during neuroimaging (Åhs et al., 2015; Faul et al., 2020). Complementing these methodological advances, new data analytic tools have enabled neuroimaging researchers to extract more complex neural system interactions that unfold when subjects freely view real-world emotional events like televised sports games (Botzung, LaBar, et al., 2010). However, research on these fronts, particularly using socially interactive paradigms, is just beginning.
Research should also expand beyond the current emphasis on how valence and arousal benefit memory for brief emotional episodes. Mood and anxiety disorders are characterized by longer-term cognitive impacts of stress and other negative affective states, but how these states alter memory processes in the brain remains poorly understood. This is due, in part, to biases in neuroscience research toward investigating short-lived emotional reactions rather than sustained moods, which may exert a greater impact on memory function clinically. Increased focus on the neuroscience of the memory-impairing effects of emotion, rather than the memory benefits, will be particularly important to better understand the cognitive sequelae related to these syndromes. Finally, while most memory studies have experimentally manipulated emotional dimensions like arousal and valence, how specific emotions (anger, guilt, pride, etc.) impact memory function remains relatively unexplored. Recent empirical work has suggested that emotional experiences are best captured by theoretical models that incorporate both emotional dimensions and discrete emotions (Cowen & Keltner, 2017). Emotions like sadness and fear may differentiate memory alterations in disorders like unipolar depression and PTSD, respectively, better than (or in addition to) more general emotional dimensions. Moods and specific emotions may thus provide additional routes to memory modulation that are likely to be important contributors to cognitive dysfunction in affective disorders.
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