Binding neutral information to emotional contexts: Brain dynamics of long-term recognition memory

There is abundant evidence in memory research that emotional stimuli are better remembered than neutral stimuli. However, effects of an emotionally charged context on memory for associated neutral elements is also important, particularly in trauma and stress-related disorders, where strong memories are often activated by neutral cues due to their emotional associations. In the present study, we used event-related potentials (ERPs) to investigate long-term recognition memory (1-week delay) for neutral objects that had been paired with emotionally arousing or neutral scenes during encoding. Context effects were clearly evident in the ERPs: An early frontal ERP old/new difference (300–500 ms) was enhanced for objects encoded in unpleasant compared to pleasant and neutral contexts; and a late central-parietal old/new difference (400–700 ms) was observed for objects paired with both pleasant and unpleasant contexts but not for items paired with neutral backgrounds. Interestingly, objects encoded in emotional contexts (and novel objects) also prompted an enhanced frontal early (180–220 ms) positivity compared to objects paired with neutral scenes indicating early perceptual significance. The present data suggest that emotional—particularly unpleasant—backgrounds strengthen memory for items encountered within these contexts and engage automatic and explicit recognition processes. These results could help in understanding binding mechanisms involved in the activation of trauma-related memories by neutral cues.     

情绪唤醒影响记忆巩固过程的神经生理机制

白鼠和人类都对情绪唤醒的经历有更好的记忆。情绪唤醒影响记忆巩固的神经生理机制主要有以下几种方式:(a)情绪唤醒或急性应激,会引发个体内部应激激素的释放,从而增强其记忆巩固过程。(b1)杏仁核的激活对情绪唤醒影响记忆巩固过程十分重要,杏仁核内部去甲肾上腺素(NE)的释放影响记忆巩固过程。(b2)杏仁核投射到负责不同类型记忆加工的脑区,如海马和皮层,从而影响记忆。(c)应激激素影响记忆巩固的过程中,杏仁核内NE的激活在这一过程中扮演着重要角色。综上,情绪唤醒影响记忆巩固的过程,涉及到激素调节、神经调节及二者的共同作用。     

Emotionally arousing pictures increase blood glucose levels and enhance recall

Arousal enhances memory in human participants and this enhancing effect is likely due to the release of peripheral epinephrine. As epinephrine does not readily enter the brain, one way that peripheral epinephrine may enhance memory is by increasing circulating blood glucose levels. The present study investigated the possibility that emotionally arousing color pictures would improve memory and elevate blood glucose levels in human participants. Blood glucose levels were measured before, 15 min, and 30 min after male university students viewed 60 emotionally arousing or relatively neutral pictures. Participants viewed each picture for 6 s and then had 10 s to rate the arousal (emotional intensity) and valence (pleasantness) of each picture. A free-recall memory test was given 30 min after the last picture was viewed. Although the emotionally arousing and neutral picture sets were given comparable valence ratings, participants who viewed the emotionally arousing pictures rated the pictures as being more arousing, recalled more pictures, and had higher blood glucose levels after viewing the pictures than did participants who viewed the neutral pictures. These findings indicate that emotionally arousing pictures increase blood glucose levels and enhance memory, and that this effect is not due to differences in the degree of pleasantness of the stimuli. These findings support the possibility that increases in circulating blood glucose levels in response to emotional arousal may be part of the biological mechanism that allows emotional arousal to enhance memory.     

Memory enhancement by a semantically unrelated emotional arousal source induced after learning

It has been well established that moderate physiological or emotional arousal modulates memory. However, there is some controversy about whether the source of arousal must be semantically related to the information to be remembered. To test this idea, 35 healthy young adult participants learned a list of common nouns and afterward viewed a semantically unrelated, neutral or emotionally arousing videotape. The tape was shown after learning to prevent arousal effects on encoding or attention, instead influencing memory consolidation. Heart rate increase was significantly greater in the arousal group, and negative affect was significantly less reported in the non-arousal group after the video. The arousal group remembered significantly more words than the non-arousal group at both 30 min and 24 h delays, despite comparable group memory performance prior to the arousal manipulation. These results demonstrate that emotional arousal, even from an unrelated source, is capable of modulating memory consolidation. Potential reasons for contradictory findings in some previous studies, such as the timing of "delayed" memory tests, are discussed.     

Only “efficient” emotional stimuli affect the content of working memory during free-recollection from natural scenes

Emotional events are thought to have privileged access to attention and memory, consuming resources needed to encode competing emotionally neutral stimuli. However, it is not clear whether this detrimental effect is automatic or depends on the successful maintenance of the specific emotional object within working memory. Here, participants viewed everyday scenes including an emotional object among other neutral objects followed by a free-recollection task. Results showed that emotional objects—irrespective of their perceptual saliency—were recollected more often than neutral objects. The probability of being recollected increased as a function of the arousal of the emotional objects, specifically for negative objects. Successful recollection of emotional objects (positive or negative) from a scene reduced the overall number of recollected neutral objects from the same scene. This indicates that only emotional stimuli that are efficient in grabbing (and then consuming) available attentional resources play a crucial role during the encoding of competing information, with a subsequent bias in the recollection of neutral representations.     

Implicit effects of emotional contexts: An ERP study

Previous recognition memory experiments have demonstrated that the ERPs elicited by correctly recognized test items differ according to whether the items were encoded in an emotionally arousing or an emotionally neutral context. It is not clear, however, whether these ERP differences depend on the explicit recognition of the items. We addressed this question in the present study by contrasting the ERPs elicited by test items encoded in emotionally negative or emotionally neutral study contexts, according to whether the items were correctly recognized or misclassified as new. Recognized items associated with emotional rather than neutral contexts elicited an early positive-going and a later negative-going effect that resembled the effects reported in prior studies. Relative to unrecognized items encoded in neutral contexts, unrecognized items encoded in emotional contexts elicited a sustained, frontal-maximum, positive-going effect that onset at about 200?ms poststimulus. This effect may reflect an influence of emotional arousal on the neural correlates of implicit memory.     

Amygdala oscillations and the consolidation of emotional memories

The amygdala receives multi-modal sensory inputs and projects to virtually all levels of the central nervous system. Via these widespread projections, the amygdala facilitates consolidation of emotionally arousing memories. How the amygdala promotes synaptic plasticity elsewhere in the brain remains unknown, however. Recent work indicates that amygdala neurons show theta activity during emotional arousal, and various types of oscillations during sleep. These synchronized neuronal events could promote synaptic plasticity by facilitating interactions between neocortical storage sites and temporal lobe structures involved in declarative memory.     

Arousal-Mediated Memory Consolidation: Role of the Medial TemporalLobe in Humans

Although the influence of emotional arousal on declarative memory has been documented behaviorally, the mechanisms underlying arousal-memory interactions and their representation in the human brain remain uncertain. One route through which arousal achieves its effects on memory performance is by regulating consolidation processes. Animal research has revealed that the amygdala strengthens hippocampal-dependent memory consolidation in a limited time window following participation in an arousing task. To examine whether this integrative function of amygdalo-hippocampal structures extends to the human brain, we tested unilateral-temporal-lobectomy patients on an adaptation of a classic paradigm in which levels of physiological arousal at encoding modulate retention over time. Subjects rated emotionally arousing (taboo) and neutral words on an arousal scale while their skin conductance responses (SCRs) were monitored. Recall for the words was assessed immediately and after a 1-hr delay. Both temporal-lobectomy patients and control subjects generated enhanced SCRs and arousal ratings for the arousing words at the time of encoding. However, only control subjects exhibited an increase in memory for the arousing words over time. This group difference in the effect of arousal on the rate of forgetting suggests that the role of medial temporal lobe structures in memory consolidation for arousing events is conserved across species.     

Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories

Stressful events frequently comprise both neutral and emotionally arousing information, yet the impact of stress on emotional and neutral events is still not fully understood. The hippocampus and frontal cortex have dense concentrations of receptors for stress hormones, such as cortisol, which at high levels can impair performance on hippocampally dependent memory tasks. Yet, the same stress hormones can facilitate memory for emotional information, which involves interactions between the hippocampus and amygdala. Here, we induced psychosocial stress prior to encoding and examined its long-term effects on memory for emotional and neutral episodes. The stress manipulation disrupted long-term memory for a neutral episode, but facilitated long-term memory for an equivalent emotional episode compared with a control condition. The stress manipulation also increased salivary cortisol, catecholamines as indicated by the presence of alpha-amylase, heart rate, and subjectively reported stress. Stressed subjects reported more false memories than nonstressed control subjects, and these false memories correlated positively with cortisol levels, providing evidence for a relationship between stress and false memory formation. Our results demonstrate that stress, when administered prior to encoding, produces different patterns of long-term remembering for neutral and emotional episodes. These differences likely emerge from differential actions of stress hormones on memory-relevant regions of the brain.     

The role of attention in the associative binding of emotionally arousing words

In the present study, we examined the role of attention in modulating the memory benefit of emotional arousal for same-valence word pair associations. To assess the role of attention either at encoding or at retrieval, participants studied lists of positive, neutral, and negative words pairs under full attention, divided attention at encoding, or divided attention at retrieval, and then were tested on the single words and on the associations between words. Consistent with past studies, memory accuracy was higher for emotional items than for neutral items, and no memory difference was observed across emotional arousal conditions for associations when encoding occurred under full attention. In contrast, memory accuracy was higher for emotionally arousing items and associations relative to neutral items when encoding occurred under divided attention. Finally, dividing attention at retrieval revealed similar effects across emotion conditions, suggesting that retrieval of emotional stimuli relative to neutral stimuli, unlike encoding, does not benefit from automatic processing. The discussion emphasizes the role of automatic processing during encoding in producing the benefit of emotionally enhanced memory, as well as the extent to which controlled attention is responsible for eliminating or reversing (relative to neutral materials) emotionally enhanced memory for associations. Additionally, the implications of the divided-attention-at-retrieval manipulation include consideration of the way in which emotional items may be consciously processed during encoding.     

More than a feeling: Emotional cues impact the access and experience of autobiographical memories

Remembering is impacted by several factors of retrieval, including the emotional content of a memory cue. Here we tested how musical retrieval cues that differed on two dimensions of emotion—valence (positive and negative) and arousal (high and low)—impacted the following aspects of autobiographical memory recall: the response time to access a past personal event, the experience of remembering (ratings of memory vividness), the emotional content of a cued memory (ratings of event arousal and valence), and the type of event recalled (ratings of event energy, socialness, and uniqueness). We further explored how cue presentation affected autobiographical memory retrieval by administering cues of similar arousal and valence levels in a blocked fashion to one half of the tested participants, and randomly to the other half. We report three main findings. First, memories were accessed most quickly in response to musical cues that were highly arousing and positive in emotion. Second, we observed a relation between a cue and the elicited memory’s emotional valence but not arousal; however, both the cue valence and arousal related to the nature of the recalled event. Specifically, high cue arousal led to lower memory vividness and uniqueness ratings, but cues with both high arousal and positive valence were associated with memories rated as more social and energetic. Finally, cue presentation impacted both how quickly and specifically memories were accessed and how cue valence affected the memory vividness ratings. The implications of these findings for views of how emotion directs the access to memories and the experience of remembering are discussed.     

Developmental reversals in false memory: Effects of emotional valence and arousal

Do the emotional valence and arousal of events distort children’s memories? Do valence and arousal modulate counterintuitive age increases in false memory? We investigated those questions in children, adolescents, and adults using the Cornell/Cortland Emotion Lists, a word list pool that induces false memories and in which valence and arousal can be manipulated factorially. False memories increased with age for unpresented semantic associates of word lists, and net accuracy (the ratio of true memory to total memory) decreased with age. These surprising developmental trends were more pronounced for negatively valenced materials than for positively valenced materials, they were more pronounced for high-arousal materials than for low-arousal materials, and developmental increases in the effects of arousal were small in comparison with developmental increases in the effects of valence. These findings have ramifications for legal applications of false memory research; materials that share the emotional hallmark of crimes (events that are negatively valenced and arousing) produced the largest age increases in false memory and the largest age declines in net accuracy.     

诱发及个体自发认知重评对情绪唤醒反应及情绪记忆的影响

为了明确诱发（IRE）及个体习惯化的自发（SRE）认知重评策略对情绪唤醒反应及情绪记忆的影响,在测量被试SRE水平的基础上,先呈现一系列中性与负性情绪图片,要求被试对图片内容进行自然观看或认知重评,同时记录被试的主观与生理唤醒水平,之后对图片进行自由回忆及再认测试。发现IRE显著降低了情绪唤醒水平及再认正确率,但只对情绪唤醒反应较高的LR（SRE水平较低）被试有效。结果提示,IRE对情绪唤醒反应与情绪记忆的调控受到SRE的影响。     

不同延时条件下的情绪记忆鲜活性

大量研究表明,情绪在一定程度上提高了记忆的准确性,但是情绪对记忆鲜活性的影响更大,该文关注延时条件下情绪记忆鲜活性的研究。研究采用记得/知道范式,操控图片情绪性和测验延时变量,结果发现情绪记忆的记得成绩好于中性记忆,且在不同延时测验下,正性高唤醒图片的记得成绩下降由慢到快再到慢的变化,负性高唤醒图片的记得下降由快到慢变化,而中性则快速下降。说明情绪记忆更具鲜活性,且是效价在高唤醒下起的作用。     

情绪记忆增强效应的时间依赖性

探讨情绪记忆短时和长时增强效应相对特异性机制以及唤醒度和效价在情绪记忆中的作用。运用不同阶段提取和不同情绪类别相结合的多因素设计方法, 对20位正常年轻成人进行行为学检测。结果显示, 情绪对记忆加工不同阶段(短时和长时)的调节作用(增强效应)具有时间依赖性, 且主要取决于情绪唤醒度, 而无显著正负效价性差异。在短时阶段主要涉及高唤醒度的增强; 而长时阶段涉及不同水平唤醒度的增强, 不同唤醒度的增强效应存在相对分离。     

Distinct parietal sites mediate the influences of mood,arousal, and their interaction on human recognition memory

The two dimensions of emotion, mood valence and arousal, have independent effects on recognition memory. At present, however, it is not clear how those effects are reflected in the human brain. Previous research in this area has generally dealt with memory for emotionally valenced or arousing stimuli, but the manner in which interacting mood and arousal states modulate responses in memory substrates remains poorly understood. We investigated memory for emotionally neutral items while independently manipulating mood valence and arousal state by means of music exposure. Four emotional conditions were created: positive mood/high arousal, positive mood/low arousal, negative mood/high arousal, and negative mood/low arousal. We observed distinct effects of mood valence and arousal in parietal substrates of recognition memory. Positive mood increased activity in ventral posterior parietal cortex (PPC) and orbitofrontal cortex, whereas arousal condition modulated activity in dorsal PPC and the posterior cingulate. An interaction between valence and arousal was observed in left ventral PPC, notably in a parietal area distinct from the those identified for the main effects, with a stronger effect of mood on recognition memory responses here under conditions of relative high versus low arousal. We interpreted the PPC activations in terms of the attention-to-memory hypothesis: Increased arousal may lead to increased top-down control of memory, and hence dorsal PPC activation, whereas positive mood valence may result in increased activity in ventral PPC regions associated with bottom-up attention to memory. These findings indicate that distinct parietal sites mediate the influences of mood, arousal, and their interplay during recognition memory.     

Differential effects of emotional arousal in short- and long-term memory in healthy adults

Recent studies demonstrated important differences between short- and long-term memory mechanisms. Besides, the emotional component has a crucial role in memory formation. This study was carried out to answer whether there is a differential influence of emotional arousal in short- and long-term memory in healthy adults. Thirty-one healthy volunteers were divided into two major groups. In the first group long-term memory (LTM) was evaluated, with the testing session one week after training. The second group was tested 1h after training, where short-term memory (STM) was evaluated. Each group was divided in to two subgroups. One half of the volunteers was exposed to an emotionally neutral story, and the other half of each group was exposed to a closely matched but more emotionally arousing story. The testing session consisted of a questionary containing 80 questions of multiple choices. The results were evaluated through percentage of correct answers. Results showed that correct answers were increased, in LTM measures, in the subjects that were given the emotional version of the test. In STM measures, no differences were found between the emotional and neutral version. However, the presentation of emotional story caused an emotional reaction in both groups. The lack of effect of emotional arousal in STM suggests that amygdala is not related to STM mechanisms. Further studies using different approaches are needed to elucidate if STM processes are influenced by emotional arousal.     

Memory for emotionally arousing stimuli: a comparison of younger and older adults

The authors compared emotional memory in younger (aged 18-32 years) and older (aged 59-84 years) adults. Previous researchers who investigated the emotionmemory relationship in younger adults consistently showed that emotional arousal enhances memory for central detail. The present authors' goal was to determine whether a similar effect could be found with older adults. Younger and older adults viewed a series of 12 slides, accompanied by a taped narrative, that showed emotionally arousing or neutral scenes in the middle phase (Slides 5-8). Participants then completed recognition tests that were scored for central detail, peripheral detail, and gist. The results indicated that, although younger adults showed higher performance than older adults did, both groups showed increased memory for central detail. In contrast, the authors found no such enhancement for peripheral detail or gist in either group. These results indicated that the arousal manipulation produced a similar effect on memory in younger and older adults. Furthermore, these results were consistent with the notion of poststimulus elaboration, which is the continued processing of central detail after the termination of an arousing event.     

Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory

Noradrenergic activation of the basolateral complex of the amygdala (BLA) modulates the consolidation of memory for many kinds of highly emotionally arousing training tasks. The present experiments investigated whether posttraining noradrenergic activation of the BLA is sufficient to enable memory consolidation of a low-arousing training experience. Sprague-Dawley rats received intra-BLA infusions of norepinephrine, the beta-adrenoceptor antagonist propranolol or saline immediately after either 3 or 10 min of object recognition training. Saline-infused controls exhibited poor 24-h retention when given 3 min of object recognition training and good retention when given 10 min of training. Norepinephrine administered after 3 min of object recognition training produced dose-dependent enhancement of 24-h object recognition memory whereas propranolol administered after 10 min of training produced dose-dependent impairment of memory. These findings provide evidence that posttraining noradrenergic activation of the BLA enhances memory of a low-arousing training experience that would otherwise not induce long-term memory. Thus, regardless of the degree of emotional arousal induced by an experience, noradrenergic activation of the BLA after the experience ensures that it will be better remembered.