The selective effects of emotional arousal on memory
By Mara Mather and Matthew Sutherland
Mara Mather’s research focuses on how emotion and stress affect memory and decisions and how such influences differ depending on one’s age and gender. Her research elucidating the interaction of emotion, cognition, and aging has been recognized with the American Psychological Association’s Distinguished Scientific Award for Early Career Contribution to Psychology and the Springer Early Career Achievement Award in Research on Adult Development and Aging. She also received a National Institutes of Health K02 Career Development award and the Richard Kalish Innovative Publication Award from the Gerontological Society of America. She is associate professor of gerontology and psychology at the University of Southern California and holds an AB in psychology from Stanford University and a PhD in cognitive psychology from Princeton University.
Matthew Sutherland is a graduate student in psychology at the University of Southern California. His undergraduate training is in philosophy and psychology. His research focuses on how emotional responses change the way we attend to and remember visual objects and scenes. To this end he uses behavioral and psychophysiological methods. Moreover, his research has a strong focus on aging and is currently funded by a NIH multidisciplinary training grant at USC’s School of Gerontology. He is a member of the Emotion and Cognition Lab, where he works under the direct mentorship of Mara Mather.
Imagine that you are studying neuroanatomy one afternoon in the library. You are trying to learn the specific shape and location of the hippocampus. As you stare intently at an image of the brain, you suddenly hear a loud gunshot. You immediately stand and see several confused, shocked people, one of whom catches your eye because she is wearing a vibrant orange dress. The gun is nowhere in sight. After a few moments of commotion you learn that someone just committed suicide in the stacks.
Later, as you are packing up your books to leave, you see your notes on emotional memory from a recent psychology class. “Hmm,” you think, “Based on previous research, how should my memory for this afternoon differ from my typical study sessions at the library?” Well, past research shows that you will be more likely to remember this afternoon than most other afternoons in the library, and that you will have a vivid memory for the gunshot itself. But what would you predict about your memory for the information you were studying just before the gunshot, or what you saw immediately after? Will you remember the image of the hippocampus in your textbook any more or less clearly next week than you would have otherwise? Would your memory for people seated around you be better or worse than if you had not heard the gunshot?
The challenge of understanding arousal’s selective effects on memory
Researchers have investigated how experiencing an emotionally arousing event such as watching a comedy skit, a video of oral surgery, or a stress induction like immersing one’s hand in ice water might affect memory for what is seen just beforehand. These studies address the question of whether hearing the gunshot will affect your memory for the picture of the brain that you were carefully studying. But the challenge is that findings across studies differ and in some instances appear to contradict one another. In some studies an emotionally arousing event enhances later memory for neutral information presented beforehand (Nielson & Powless, 2007; Nielson & Bryant, 2005). In other studies manipulations of stress or emotional arousal either disrupt or have no effect on memory for neutral stimuli presented beforehand (Buchanan & Lovallo, 2001; Cahill, Gorski, & Le, 2003; Smeets, Otgaar, Candel, & Wolf, 2008).
Other experiments find that even just the presentation of an emotional picture or word can affect memory for neutral items shown just beforehand – but again, whether the emotional stimuli enhance or impair memory for information around them depends on the study, with many studies showing impairment (e.g., Detterman & Ellis, 1972; Knight & Mather, 2009; Strange, Hurlemann, & Dolan, 2003) but a couple demonstrating enhancement (Anderson, Wais, & Gabrieli, 2006; Knight & Mather, 2009).
Other findings related to the way that emotional arousal leads to selective memory also present some apparently conflicting findings. For instance, there is some evidence that emotional arousal enhances memory for generalized forms of information that lack detail, a type of memory known as ‘gist’ memory (Adolphs, Tranel, & Buchanan, 2005), whereas other studies show that emotional arousal enhances memory for the specific perceptual details of an item (Kensinger, Garoff-Eaton, & Schacter, 2006, 2007a, 2007b; Mather & Nesmith, 2008). How can we account for these seemingly contradictory effects of arousal on memory?
Across studies, one theme that emerges is that arousal has selective effects on memory. Whether arousal enhances or impairs memory depends on the experiment, and the type of information that the participant is tested on. But what determines what arousal will enhance in memory and what it will impair? One previous hypothesis is that emotional arousal leads to memory narrowing, in which arousal enhances memory for central details at the cost of peripheral details (Burke, Heuer, & Reisberg, 1992; Christianson, Loftus, Hoffman, & Loftus, 1991). However, this account cannot explain how arousal sometimes enhances and sometimes impairs memory for information that precedes or follows an arousing stimulus, as reviewed above.
To address the puzzling discrepancies that have been observed across studies, we outlined a new theory of arousal and memory (Mather & Sutherland, 2011). This arousal-biased competition (ABC) theory builds on the notion that during perception and thought, our active mental representations compete with each other (Beck & Kastner, 2009; Duncan, 2006). Whichever representation becomes dominant tends to suppress the less prominent representations. ABC theory proposes that arousal leads to both “winner-take-more” and “loser-take-less” effects, resulting in stronger biased competition in the brain. Thus, arousal modulates ongoing competitive processes of mental representation. However, the key to understanding arousal-biased competition lies in the concept of ‘priority,’ that determines which mental representations will be enhanced versus suppressed by the process of selective attention.
Two primary factors determine priority—top-down goals and bottom-up perceptual salience (Fecteau & Munoz, 2006). Top-down goals refer to the subjective importance assigned to, and the expectations one has for what is perceived. Bottom-up perceptual salience refers to the degree to which a stimulus attracts attention as a result of its perceptual properties, such as when a brightly lit object attracts more attention than a dimly lit one. Thus if a stimulus in an experiment is relevant to the participant’s task (top-down goal), or it is more perceptually salient (bottom-up perceptual salience) than other stimuli in view, it will have priority. According to ABC theory, perception and memory for high priority stimuli are enhanced by arousal, while low priority stimuli are suppressed.
Arousal-biased competition in perception
ABC theory makes specific predictions about what arousal will do to mental representations once the arousal is experienced, and the influence it will have on these representations in memory. When a person becomes emotionally aroused, any high priority information that is perceived will be represented in attention and working memory more strongly. Often the high priority information is also the stimulus that induced the arousal, and a wide range of experiments have shown that arousing stimuli are enhanced in attention and memory (Mather, 2007).
However other experiments have revealed that being exposed to an emotionally arousing stimulus can enhance visual processing of neutral stimuli that are presented next. For example, briefly viewing an image of a face with a fearful expression, rather than a neutral expression, can increase a person’s ability to identify features of line gratings shown next (Phelps, Ling, & Carrasco, 2006). Similarly, hearing or seeing taboo words that evoke strong emotional responses can enhance one’s ability to identify briefly displayed non-emotional words that immediately follow (Bocanegra & Zeelenberg, 2009; Zeelenberg & Bocanegra, 2010). It is important to note that in each of these studies the non-emotional stimulus that followed the arousing stimulus had priority because it was goal-relevant. Thus once the emotional stimulus was removed and no longer competing for attention, the lingering arousal enhanced visual processing of the neutral item because that item had priority and was the focus of attention.
To investigate these effects more closely we created a working memory task that allowed us to compare attention to high and low priority stimuli (Sutherland & Mather, under review). We wanted to see how emotional arousal would influence attention to more than one neutral object competing for attention. So we had people listen to short sound clips that varied in emotional intensity. After the sound played eight letters were briefly flashed onto a computer screen (Fig. 1A). Some of the letters were printed in a dark font, giving the letters a high contrast with the white background. Other letters were printed in a lighter font, giving them a relatively low contrast with the white background. The first finding we observed was that regardless of what type of sound was played, high contrast letters were more often correctly recalled compared to low contrast letters, which is evidence that the high contrast letters had priority. However, the key finding was that when participants heard an emotionally arousing sound, they became even more likely to report the high contrast letters and even less likely to report the low contrast letters, compared to when they heard neutral sounds (Fig. 1B). This increase in the influence of salience under arousal was small, but statistically significant. What this shows is that emotional arousal modulates the effects of priority by enhancing representations of high priority letters and weakening representations of low priority letters. Thus, to return to the opening scenario, a woman wearing a bright orange dress in the library might attract more attention than usual, and might be more memorable in the short term if she is seen immediately after a frightening gunshot.
Arousal-biased competition in memory
In addition to accounting for arousal effects on visual processing, the ABC perspective also explains many of the discrepancies across studies looking at how arousal affects memory. For instance, ABC theory predicts that if you experience a sudden brief increase in arousal (such as when hearing a gunshot), this should increase the degree to which you remember high priority neutral information presented shortly before or after the arousing event. Thus, studies that asked participants to try to learn a list of neutral words for a later test, but then had them watch arousing or nonarousing videos afterwards found better memory for words seen before the arousing video, compared to words seen before the neutral video (Nielson & Powless, 2007; Nielson & Bryant, 2005). Because participants were purposefully trying to learn the words, the words were given priority, meaning their representations were strong, and the arousal experienced afterwards enhanced memory for these words (compared with memory for words learned before watching the neutral video).
But the effects of a post arousal or post stress induction change when emotional items are included in the material that is learned beforehand. In studies that had participants view a mixed list of emotional and neutral stimuli, followed by a stress manipulation (Buchanan & Lovallo, 2001; Cahill et al., 2003; Smeets et al., 2008), only memory for the emotional items was enhanced, as they received priority due to their arousing nature. In this case neutral items lose the competition for mental representation when pitted against emotional items, and thus receive no benefit from arousal or stress experienced shortly after the items are learned.
In studies that showed that an emotionally arousing picture or word impairs memory for neutral items seen just before and after it (e.g., Detterman & Ellis, 1972; Strange et al., 2003), participants were shown lists of neutral items with one emotional or non-emotional oddball included in the list. Whereas a study showing the opposite effect of this, namely better memory a week later for neutral images shown before emotional pictures (Anderson et al., 2006) had participants learn only one neutral image before the arousal-inducing picture was shown.
The key difference between these studies is that the one in which arousal enhanced memory presented only a single neutral stimulus prior to the arousing stimulus on each trial (with a time gap in between each trial), meaning the neutral stimulus did not have to compete for attention with other preceding stimuli. Thus it received priority at the time it was processed and was enhanced in memory if arousal was experienced shortly after. Studies showing the opposite effect (retrograde impairment) had participants learn multiple neutral items that directly competed for mental representation with other neutral items before the emotional oddball items appeared (e.g., Detterman & Ellis, 1972; Strange et al., 2003). None of the neutral items in the oddball lists were strong winners in the competition for representation and thus they were inhibited (loser-take-less) as the emotional oddball stimuli were enhanced (winner-take-more). ABC theory accounts for these conflicting findings, as it predicts that emotionally arousing items will lead to retrograde amnesia when the preceding information was not something already dominating the competition for mental resources, but retrograde enhancement when it was the highest priority mental representation at that moment.
The last set of conflicting findings that ABC theory can explain has to do with arousal’s influence on memory for gist and memory for detail. When viewing individual pictures one by one accompanied by a narrative that makes a coherent story or theme out of the pictures, if that theme is emotionally arousing, people have better gist memory for what went on in the story (Adolphs et al., 2005). However, other studies report that when pictures are shown individually people have better memory for the details of the picture if it is emotionally arousing (Kensinger et al., 2006; Mather & Nesmith, 2008). While these findings appear to conflict, it is important to note that when narratives are combined with visual stimuli to simulate a thematic story or event, the theme becomes the most salient, and thus has priority. Therefore, when the theme of the story turns emotional, it enhances gist memory for the thematic information of the story because this information has priority. On the other hand, when an individual emotionally arousing picture is shown, it captures attention, leading any benefits of arousal to be concentrated on the details of that picture. Thus the concept of priority allows ABC theory to account for both of these seemingly contradictory effects.
Finally, some additional evidence for ABC theory comes from Knight and Mather (2009), whom used an oddball-list paradigm to examine a number of factors to see which ones determine whether emotionally arousing stimuli create retrograde amnesia or enhancement for the neutral non-oddball items in the list. They found that reducing the number of neutral items on the list reduced the retrograde impairment effect, consistent with the idea that arousal is most likely to impair memory for information that was already somewhat “lost in the crowd.” Also, they found that when participants were trying to learn the neutral items on the list for an upcoming memory test (“recall” condition), the emotional oddballs led to retrograde enhancement more than when they were just rating whether the neutral items were natural or artificial (“no-recall” condition; Fig. 2).
In other words, arousal enhanced memory for what happened just beforehand if (and only if) that preceding information was the dominant focus of attention. Thus returning to the opening scenario in the library, if the brain image you were studying before the gunshot was your dominant mental representation at that moment, then your memory for the picture of the hippocampus would be stronger than it would be had nobody fired a gun in the stacks. In contrast, your memory for things that happened before the gunshot that you were not paying attention to, such as someone nearby coughing, should be even worse than it would be if there had been no gunshot.
In summary, the findings we reviewed here indicate that emotional arousal makes things that are perceptually salient stand out even more and makes any high priority information even more memorable. At the same time, arousal reduces processing of low priority information. This increase in selectivity under arousal is likely to be adaptive in many situations, and can explain why sometimes arousing stimuli impair memory for nearby stimuli and sometimes they enhance it.
The work described here was supported by grants RO1AG025340, K02 AG032309 and T32AG000037 from the National Institute on Aging.
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