It has long been known that experiences that elicit arousal are more likely to be remembered than experiences that do not evoke an emotional response. This emotional memory enhancement
has been demonstrated across a range of paradigms and using a variety of stimuli (e.g., Bradley et al., 1992; Cahill & McGaugh, 1995
; Kensinger et al., 2002
). These enhancements are particularly pronounced for events that elicit arousal (e.g., Anderson et al., 2006
Buchanan et al., 2004; Kensinger & Corkin, 2003
; Talmi & Moscovitch, 2004
), and it is believed that the release of stress hormones may play an important role in modulating these mnemonic influences. In particular, it has been proposed that arousal-mediated enhancement of memory may occur when there is both an arousal-related enhancement in noradrenergic activation, leading to interactions between the basolateral nucleus of the amygdala and other regions important for sensory and mnemonic processing, and also the release of glucocorticoids (reviewed by McGaugh, 2004
; Wolf, 2008
). Though it might have been assumed that such effects would be too sluggish to modulate memory on a trial-by-trial basis, evidence is accumulating to suggest that arousal-mediated enhancement is likely to occur even when there is a relatively rapid fluctuation between emotional and neutral stimuli. For example, even when emotional and neutral stimuli are intermixed on a study list and are presented for a relatively short duration (e.g., a few seconds), arousal-related responses, such as galvanic skin conductance, are strong predictors of later memory (e.g., Anderson et al., 2006
), and noradrenergic blockade can remove the effects of emotion on memory (e.g., Strange & Dolan, 2007).
In order for a previous event to be remembered, at least three memory phases must occur successfully. First, the event must be recorded by sensory registers and encoded
. Second, the event must be consolidated
into a stable and lasting representation. Third, the event must be retrieved
. There is evidence to indicate that when an experience elicits an arousal response, there are emotion-specific processes that are engaged at each of these stages, enhancing the likelihood that information is encoded, consolidated, and retrieved. In brief, information eliciting arousal is more likely to be detected and attended (reviewed by Dolan & Vuilleumier, 2003
; Kensinger, 2004
; MacLeod & Matthews, 2004
), increasing the likelihood that the information is encoded. Arousing information also appears to be consolidated into memory more effectively than nonarousing information, as evidenced by the fact that the mnemonic benefit for arousing information (as compared to nonemotional information) tends to increase with longer retention delays. In other words, while nonarousing information is readily forgotten, once encoded, arousing information seems more likely to be established into a durable memory (LaBar & Phelps, 1998
). Once stored, arousing information also may be more likely to be retrieved, though there is less conclusive evidence regarding how emotion influences retrieval processes (see review by Buchanan, 2007
). Thus, when information is arousing, it is not remembered simply because of the engagement of the same sorts of processes that would enhance memory for more mundane experiences (e.g., enhanced semantic or autobiographical elaboration, additional rehearsal), but rather because of the engagement of processes not typically recruited unless an experience evokes an emotional reaction.
At a neural systems level, the memory enhancement seems to occur because, once active, regions within the affect processing system (e.g., the amygdala and the orbitofrontal cortex) modulate the processing of regions that facilitate the encoding of sensory detail (e.g., regions of the fusiform gyrus) and the consolidation of memory (e.g., the hippocampal formation; see ). There is extensive evidence that such modulation occurs in animals (reviewed by McGaugh, 2004
), and there is increasing support for a modulatory influence in humans as well. For example, neuroimaging studies have revealed that during the processing of emotional information, there are correlations between the strength of activity in the amygdala and in the hippocampus (e.g., Kensinger & Corkin, 2004
), and the strength of these correlations can correspond with the magnitude of the mnemonic boost for emotional information (e.g., Richardson et al., 2004
). There also are often correlations between the amount of activity in the amygdala and the fusiform gyrus (a region important for higher-level visual processing; Iidaka et al., 2001
; Vuilleumier et al., 2004
), and these interactions boost the likelihood that visual details are encoded into memory (e.g., Kensinger, Garoff-Eaton, & Schacter, 2007
; Talmi et al., 2008
). Neuroimaging studies, many investigating the retrieval of emotional autobiographical memories, have suggested that the amygdala may modulate retrieval processes as well (reviewed by Buchanan, 2007
), perhaps facilitating the mnemonic search process (Daselaar et al., 2007
). For example, during retrieval, there appears to be synchrony between the activity in the amygdala, the hippocampus, and the fusiform gyrus (e.g., Kensinger & Schacter, 2007
; Smith et al., 2006
). There also is increased strength of connectivity between the amygdala and the hippocampus during the retrieval of emotional information, modulated by activity within the orbitofrontal cortex (Smith et al., 2006
). These modulations may lead to an enhanced ability to retrieve the details associated with an episode.
These behavioral and neuroimaging results converge on the conclusion that memory for emotional events can benefit from the engagement of emotion-specific processes. However, the neuroimaging data emphasize that the emotion-specific processes do not replace the standard memory network. Rather, activity within emotion processing regions seems to functionally modulate the memory network that supports learning and retrieval of all experiences (even those void of emotion) and the visual processing regions that support the encoding of any event’s sensory details (see reviews by Phelps, 2004
; LaBar & Cabeza, 2006
These studies have provided evidence for memory-enhancing properties of emotional arousal; when an event is emotionally arousing, it is more likely to be remembered. However, if we examine not just whether an event is remembered, but also what types of details people remember about that event, then the literature suggests that emotional arousal does not enhance memory across-the-board and for all types of event details. Rather, emotional arousal appears to be associated with memory-narrowing effects. There are a number of related theories suggesting that the effects of emotional arousal on memory may be best characterized by focal enhancements (e.g., Buchanan & Adolphs, 2003; Reisberg & Heuer, 2004
; Mather, 2007
). Though the theories differ from one another in important ways, they all share the central tenet that some aspects of an emotional experience are remembered well because of their arousing nature, while other elements may receive no mnemonic benefit and in fact may be more likely to be forgotten.
The most widely discussed theory of arousal’s narrowing effects on memory arose from Easterbrook’s (1959)
proposal that arousal restricts the focus of attention, causing a person to notice information that elicits arousal but to fail to process other information. Though Easterbrook’s proposal was about attention focusing, proof of the concept has been derived from studies in which memory for “central” event aspects, directly tied to the emotion elicitor, is compared to memory for “peripheral” aspects, removed from the source of the emotion. Across a range of studies, researchers have demonstrated an emotion-induced memory trade-off, whereby individuals remember the central emotional content of a stimulus but often forget the other details (see Buchanan & Adolphs, 2002
; Reisberg & Heuer, 2004
for reviews). For example, after studying an image of a car accident on a street, participants tend to have good memory for the car accident but poor memory for the street. In fact, their memory for the street can be worse if they saw a car accident on the street than if they saw a nonemotional version of the scene, such as a taxi driving down the street. These sorts of trade-offs can occur not only for information presented in close spatial proximity to an emotional item but also for information presented in temporal proximity: For instance, after seeing an arousing word, participants are less likely to remember the word that immediately follows it (Hurlemann et al., 2005
Focal enhancements for emotional information occur not only when multiple items are shown in close temporal or spatial proximity, but also when memory is queried for multiple episodic details associated with a single arousing item’s presentation. For example, when a person is presented with an image of a snake and is asked to decide whether it depicts a living thing or whether it would fit in a shoebox, participants are quite good at remembering what the snake looked like but they do not remember which decision they were asked to make about the snake (Kensinger et al., 2007
). More generally, there seem to be some types of details that are reliably enhanced by emotion, including the perceptual details of a word (such as its font) or object (such as its shape, color, or orientation; Doerksen & Shimamura, 2001
; Kensinger & Corkin, 2003
; Kensinger, Garoff-Eaton, & Schacter, 2006
; D’Argembeau & Van der Linden, 2004
; MacKay et al., 2004
), well as the item’s spatial location (D’Argembeau & Van der Linden, 2004
; MacKay & Ahmetzanov, 2005
; Mather & Nesmith, in press
). By contrast, other details such as the temporal order in which an emotional item was presented, or the decision made about an item (Cook, Hicks, & Marsh, 2007
; Kensinger & Schacter, 2006a
; Kensinger, Garoff-Eaton, & Schacter, 2007
), are not remembered more reliably for emotional items than for nonemotional ones.
Based on the available evidence, my working hypothesis has been that arousal (and, as I will discuss later, arousal accompanying a negative
emotion in particular) enhances memory for “intrinsic” item features details but not “extrinsic” contextual details (see Kensinger & Schacter, 2006
; Kensinger, 2007
). This hypothesis can accommodate the central/peripheral trade-offs (where what is “intrinsic” is the emotional item whereas what is “extrinsic” is the information spatially, temporally, or conceptually removed from that item), and it also is consistent with the literature examining the effect of arousal on “source memory,” or the ability to remember the context in which a piece of information was learned (Johnson, Hashtroudi, & Lindsay, 1993
). The types of source details that have been reliably enhanced by emotion tend to be those that are integral to our ability to process the information, such as the sensory features associated with the information’s presentation.
This “intrinsic” vs. “extrinsic” dissociation is conceptually related to Mather’s (2007)
proposed distinction between memory binding for within-item features, which she purports is enhanced by arousal, and memory binding for between-item features, which she proposes receives no benefit from arousal. In most instances, what Mather would label a “within-object” feature I would label “intrinsic,” and what she would consider “between-object” I would consider to be “extrinsic.” However, I do not think there is a perfect mapping between our terminologies. For example, I would include as “extrinsic” characteristics even those event qualities that are not items per se (e.g., temporal order, the decision made about an item) and more generally, I do not consider the “intrinsic” vs. “extrinsic” distinction to be tied to object processing or even to the visual domain. I also conceive of “intrinsic” and “extrinsic” as dimensions that relate to how event features are processed in relation to the emotional aspect of an event rather than to fixed properties of the stimuli. For instance, if emotional and neutral words were presented sequentially and one at a time, but together formed a sentence (e.g., the - man - abused - children), I would expect memory to be enhanced for all of the words when compared to a word sequence that conveyed no emotional meaning. By contrast, if emotional and neutral words were presented in sequence but did not form a coherent statement, I would expect memory to be enhanced only for the emotional words within the stream (and see Kensinger et al., 2002
for some evidence to support this hypothesis). Thus, what is “intrinsic” vs. “extrinsic” need not be a fixed stimulus property but rather may be manipulated based on how the information is interpreted and processed.
Though there are conceptual differences between the central/peripheral, intrinsic/extrinsic, and within- vs. between-item binding theories, at the present time, I do not think there are sufficient data to adjudicate between these alternate theories (and they may not be mutually exclusive) or to elucidate the boundary conditions in which each may operate. Therefore, I want to focus on the conviction shared by each of these theories: that emotion leads to focal enhancements in memory and that these focal effects arise because of the way in which arousing information is attended and bound during encoding and consolidation. In the section below, I will review some of the behavioral and neuroimaging studies that have begun to shed light on the processes leading to these focal effects.
The Processes Leading to Arousal’s Focal Memory Enhancements
It is well known that arousing items can capture and sustain attention (reviewed by Dolan & Vuilleumier, 2003
; MacLeod & Matthews, 2004
), and it makes sense that if attention is devoted toward the processing of details that are intrinsic to an arousing item, this could leave fewer cognitive resources for the processing of other event details. Although changes in attention allocation have long been theorized to explain the focal effects of emotion on memory for detail (e.g., Easterbrook, 1959
), only recently have studies begun to address this hypothesis empirically.
Behavioral evidence for a role of attentional factors during encoding has come from studies indicating that the trade-offs in memory are far more likely to occur when there is an object that “grabs” attention than when there is only thematically-induced emotion, not tied to any particular aspect of a scene or story. For example, Laney et al (2004)
found that when participants listened to a story about either date rape or a successful first date, participants who heard about the date rape showed better memory for all aspects of the story than individuals who heard about the first date, with no tradeoff elicited. This finding suggests that trade-offs may occur only for the subset of emotional experiences in which there is an “attention magnet” (a term used by Laney et al., 2004
). Without such a magnet, the enhancing effects of emotion may be more widespread (see Reisberg & Heuer, 2004
for more discussion).
Additional behavioral evidence that the trade-off may be tied to the strength of the emotional “attention magnet” comes from studies that have manipulated participants’ encoding tasks, altering how their attention is directed toward the scenes. The logic behind these studies is that if the focal effects arise due to attention focusing during encoding, then it should be possible to alter the types of details that are remembered well by changing the way in which participants are asked to process the information. Indeed, my colleagues and I found that when we gave young adults intentional encoding instructions, informing them that they should remember all aspects of the scenes because their memory would be tested later, their ability to remember background details (e.g., the street) became as good as their ability to remember the negative details (e.g., the accident; Kensinger, Piguet, Krendl, & Corkin, 2005
). A similar dissipation of emotion-induced trade-off effects can occur if participants are asked to focus upon the visual details of the scene, describing the scene so that an artist could reproduce it acurately. With this type of focused encoding task, young adults became just as good at remembering the background details of a negative scene than of a neutral scene (Kensinger, Garoff-Eaton, & Schacter, 2007
These behavioral data suggest that the way in which the information is attended to and encoded has important consequences for what details later are remembered. In order to more directly examine what encoding processes may lead to these focal effects, my colleagues and I asked participants to undergo a functional magnetic resonance imaging (fMRI) scan. While in the fMRI scanner, we asked participants to view positive, negative, and neutral items. Participants made one of two decisions about each item. For some items, they decided whether the it was animate, and for other items they determined whether it was something commonly encountered. Later, outside of the scanner, participants saw some images that were exactly the same as the studied image, other images that shared the same theme as the studied image but differed in visual details (e.g., a different image of a snake) and other items that were unrelated to any studied image. Participants had to indicate whether each item was the “same” as the studied item, was “similar” but not identical to the studied item, or was “new” (Kensinger & Schacter, 2007
). By looking at how well participants could distinguish “same” from “similar” exemplars, we could examine how emotional valence influenced participants’ ability to remember the precise visual details of an object (Kensinger, Garoff-Eaton, & Schacter, 2007
). Using a subsequent-memory
paradigm (reviewed by Paller & Wagner, 2002
; see ), the neural activity during the encoding of each item was sorted based upon whether that item was later remembered with visual specificity, remembered without visual specificity, or forgotten. Neural activity during encoding also was sorted based on later memory for the decision made about the item (as a function of whether the decision was remembered correctly or incorrectly).
These neuroimaging analyses revealed that amygdala activity showed no correspondence with memory for the decision made about the item. Rather, amygdala activity was equally high during the encoding of all negative items that people later remembered studying, regardless of whether they were correct or incorrect about what decision they had made about the item. By contrast, amygdala activity showed a strong correspondence to memory for visual detail, as did activity within the fusiform gyrus. Activity in each of these regions was highest during the encoding of negative items that were remembered with accurate visual detail (i.e., same items accurately given a “same” response) and was less during the encoding of negative items that were remembered without visual detail (i.e., same items inaccurately given a “similar” response). There was a strong correlation between the level of activity in the right amygdala and in the right fusiform gyrus during the encoding of negative objects that would later be remembered with specific visual detail (i.e., later given a “same” response), suggesting that interactions between these regions are important for modulating the effect of negative emotion on the visual specificity of object memory (). These results highlight the fact that the relation between amygdala activity during encoding and memory for event details may depend on the particular type of detail that is assessed. Emotion does not enhance memory for all aspects of an encoding episode, and amygdala engagement at encoding does not ensure that all details will be accurately remembered. Rather, amygdala engagement during encoding can lead some aspects of an experience to be remembered well but can result in other aspects of an experience being forgotten.
Beyond the amygdala, there was a broader affective-attentional network whose activity increased the likelihood of remembering a negative item’s visual details but decreased the likelihood of remembering the task performed with the item. These regions included the orbitofrontal cortex, ventral striatum, and anterior cingulate gyrus, regions that have been implicated in the prioritized processing of emotional stimuli (Vuilleumier et al., 2001
) and in the motivational processing of affective stimuli (e.g., Robbins & Everitt, 1996
; Schultz, 2000
). The revelation of this network fits well with the hypothesis that at least some of the focal effects of emotion on memory arise from the prioritized processing and attentional focusing on arousing items during encoding. It makes sense that if participants are focused on the intrinsic attributes of an item (e.g., its visual features) they may fail to encode other details associated with the item’s presentation (e.g., the decision made about the item). In other words, activity within this affective attentional network may serve to focus and guide encoding processes, assuring that intrinsic details of negative items are encoded, but this focusing may come at the cost of encoding more extrinsic elements. Thus, these neuroimaging data suggest that it may be the same neural processes that lead to emotional enhancements that also lead to poorer memory for other types of details. The more affectively focused a person is during encoding, the more likely they are to remember some, but not all, aspects of an emotional experience.
The conclusion that heightened affective focus leads to memory trade-offs fits well with the behavioral data described earlier. Asking participants to describe the visual details of a scene rather than to determine whether they want to approach the scene, in essence manipulates how affectively focused participants are during the encoding episode. When they were affectively focused – deciding whether to approach a potentially threatening scene – they showed a robust memory trade-off, whereas when they were guided to be non-affectively focused – describing the scene for an artist - the magnitude of the trade-off was reduced (Kensinger, Garoff-Eaton, & Schacter, 2007