Stress and emotional memory retrieval: effects of sex and cortisol response

In some situations, memory is enhanced by stressful experience, while in others, it is impaired. The specific components of the stress-response that may result in these differing effects remain unclear, and the current study sought to address this knowledge gap. Forty healthy participants (20 women, 20 men) were exposed to emotionally arousing and neutral pictures. Twenty-four hours later, 20 participants underwent a social stressor (speech and math tests), and 20 underwent a control reading task, both followed by a delayed free recall task. Cortisol responders to the stress condition (5 men and 1 woman) showed reduced memory retrieval for both neutral and emotionally arousing pictures. Men and women in the stress condition who did not produce a cortisol response showed increased retrieval of unpleasant pictures compared to controls. The results provide further evidence that cortisol is a primary effector in the stress-induced memory retrieval deficit. At the same time, stress can enhance memory retrieval performance, especially for emotional stimuli, when the cortisol response is absent.     

Effects of pre-learning stress on memory for neutral, positive and negative words: Different roles of cortisol and autonomic arousal

Stress can have enhancing or impairing effects on memory. Here, we addressed the effect of pre-learning stress on subsequent memory and asked whether neutral and emotionally valent information are differentially affected by specific stress components, autonomic arousal and stress-induced cortisol. Ninety-six healthy men and women underwent either a stressor (modified cold pressor test) or a control warm water exposure. During stress, participants showed comparable autonomic arousal (heart rate, blood pressure), while 60 percent showed an increase of cortisol (responders vs. 40 percent non-responders). Ten minutes after the cold pressor test neutral, positive and negative words were presented. Free recall was tested 1 and 24 h later. Overall, positive and negative words were better recalled than neutral words. Stress enhanced the recall of neutral words independently of cortisol response. In contrast, the free recall of negative words was enhanced in cortisol responders in the 1-h but not 24-h test which might suggest different effects of cortisol on consolidation and reconsolidation processes. Recall for positive words was unaffected by stress-induced cortisol. To summarize, (i) pre-learning stress can enhance memory for neutral words independently of cortisol and (ii) stress effects on memory for negative words appear to rely on stress-induced cortisol elevations, the absence of this effect for positive words might be at least partly due to differences in arousal evoked by positive vs. negative words.     

The effects of cortisol increase on long-term memory retrieval during and after acute psychosocial stress

In this study the effects of stress-induced cortisol increases on long-term memory retrieval during and after acute psychosocial stress were examined. Seventy male students were exposed to either a psychosocial stress task or to a non-stressful control task. During and after this task, retrieval was tested for idiosyncratic emotionally negative and neutral word pair associations that were learned 1 day or 5 weeks earlier. Within the stress condition, retrieval of negative words, 5 weeks after learning, was impaired both during and after the stress task compared to the control group. Further, during the stress task, when sympathetic activity was enhanced, impaired retrieval of both neutral and emotional words was significantly related to enhanced cortisol response. In contrast, after the stress task, when cortisol levels were still increased but sympathetic activity was low again, no association was found between cortisol increase and retrieval of either neutral or emotional material. These results are in line with the previous animal research showing that when arousal is high, cortisol increase can impair memory retrieval.     

Brief,pre-retrieval stress differentially influences long-term memory depending on sex and corticosteroid response

Previous work has indicated that stress generally impairs memory retrieval. However, little research has addressed discrepancies that exist in this line of work and the factors that could explain why stress can exert differential effects on retrieval processes. Therefore, we examined the influence of brief, pre-retrieval stress that was administered immediately before testing on long-term memory in males and females. Participants learned a list of 42 words varying in emotional valence and arousal. Following the learning phase, participants were given an immediate free recall test. Twenty-four hours later, participants submerged their non-dominant hand in a bath of ice cold (Stress) or warm (No Stress) water for 3 min. Immediately following this manipulation, participants’ memory for the word list was assessed via free recall and recognition tests. We observed no group differences on short-term memory. However, male participants who showed a robust cortisol response to the stress exhibited enhanced long-term recognition memory, while male participants who demonstrated a blunted cortisol response to the stress exhibited impaired long-term recall and recognition memory. These findings suggest that the effects of brief, pre-retrieval stress on long-term memory are sex-specific and mediated by corticosteroid mechanisms.     

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.     

Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding

Abundant evidence indicates that endogenous stress hormones such as epinephrine and corticosterone modulate memory consolidation in animals. We recently provided the first demonstration that an endogenous stress hormone (epinephrine) can enhance human memory consolidation. However, these findings also suggested that post-learning stress hormone activation does not uniformly enhance memory for all recently acquired information; rather, that it interacts with the degree of arousal at initial encoding of material in modulating memory for the material. Here we tested this hypothesis by administering cold pressor stress (CPS) or a control procedure to subjects after they viewed slides of varying emotional content, and assessing memory for the slides 1 wk later. CPS, which significantly elevated salivary cortisol levels, enhanced memory for emotionally arousing slides compared with the controls, but did not affect memory for relatively neutral slides. These findings further support the view that post-learning stress hormone-related activity interacts with arousal at initial encoding to modulate memory consolidation.     

Women with diarrhoea-predominant irritable bowel syndrome show an increased pressure response to 35% carbon dioxide stress challenge

The responses to inhalation of 35% carbon dioxide (CO(2)) as a stressor were compared in female irritable bowel syndrome (IBS) patients and healthy controls to assess potential differences in cardiovascular, neuroendocrine and behavioural responses to stress. A total of 22 women (12 patients with ROME II defined diarrhoea-predominant IBS and 10 aged-matched controls) were challenged with a single vital capacity breath of 35% CO(2) (with 65% oxygen). Beat-to-beat blood pressure and heart rate were recorded prior to, during and after the inhalation. Serum cortisol concentration and behavioural ratings were measured pre- and post-inhalation. A typical pattern of responses to CO(2) was observed, characterised by a reduction in heart rate and increases in serum cortisol and anxiogenic symptoms; however, these responses did not differ between groups. Both groups also demonstrated an increase in systolic blood pressure; however, this response was significantly enhanced in IBS patients compared to healthy controls (P < 0.05). These findings demonstrate that females with diarrhoea-predominant IBS have an exaggerated pressor response to 35% CO(2) stress challenge, suggesting a more stress-responsive sympathetic nervous system.     

Taboo words: The effect of emotion on memory for peripheral information

In three experiments, we examined memory for peripheral information that occurred in the same context as emotion-inducing information. In the first two experiments, participants studied either a sentence (Experiment 1) or a pair of words (Experiments 2A—2C) containing a neutral peripheral word, as well as a neutral, negative-valence, or taboo word, to induce an emotional response. At retrieval, the participants were asked to recall the neutral peripheral word from a sentence fragment or emotion-inducing word cue. In Experiment 3, we presented word pairs at encoding and tested memory with associative recognition. In all three experiments, memory for peripheral words was enhanced when it was encoded in the presence of emotionally arousing taboo words but not when it was encoded in the presence of words that were only negative in valence. These data are consistent with priority-binding theory (MacKay et al., 2004) and inconsistent with the attention-narrowing hypothesis (Easterbrook, 1959), as well as with object-based binding theory (Mather, 2007).     

Immediate and prolonged effects of cortisol, but not propranolol, on memory retrieval in healthy young men

BackgroundWhile acute cortisol administration has been found to impair retrieval of emotional memories in healthy subjects, the duration of this memory impairment is still unknown. Propranolol, on the other hand, may impair the reconsolidation of emotional memories during reactivation, although human studies examining such effects are scarce. The present investigation was therefore undertaken to examine the immediate and prolonged effects of a single administered dose of cortisol or propranolol on memory retrieval in a double-blind placebo controlled design.MethodsEighty-five healthy male participants were asked to retrieve previously learned emotional and neutral information after ingestion of 35 mg cortisol, 80 mg propranolol or placebo. After a washout period of 1 week, recall was again tested.ResultsMemory retrieval of neutral and emotional information was impaired by a single dose of cortisol compared to placebo. The memory impairment due to cortisol remained, even after a washout period of 1 week. No immediate or prolonged effects of propranolol on memory retrieval were found, despite significant reductions in sympathetic arousal.ConclusionsThese results lend support to the hypothesis that cortisol is able to attenuate (emotional) memory recall in men over longer time spans and may therefore augment the treatment of disorders like post-traumatic stress disorder and phobias, but do not clarify the mechanism(s) through which propranolol exerts its therapeutic effects.     

Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words

Studies in rodents have demonstrated that glucocorticoids enhance memory consolidation but impair delayed memory retrieval. Similar findings have been reported in humans. Emotional items are better remembered than neutral items. However, it is unknown if emotional valence influences the effects of cortisol on retrieval. In this double-blind crossover study, 16 healthy women learned a wordlist containing 15 neutral and 15 negative words. Delayed recall was tested 5h later. Cortisol administered before recall testing significantly reduced retrieval (p<.01). Exploratory follow-up analysis revealed that cortisol significantly impaired retrieval of negative words (p<.01), while having no significant effect on neutral words (p=.47). The current findings could suggest that emotional material is especially sensitive to the memory modulating effects of stress hormones.     

Does source memory impairment associated with emotionally arousing stimuli occur at encoding or retrieval?

The present experiment investigated whether negatively arousing stimuli produce source memory impairment and whether the impairment occurs at encoding or retrieval. Participants were presented with negatively arousing, positively arousing, and neutral pictures. Each picture was followed by an instructional slide that indicated whether the picture was an Apple-kind or an Orange-kind. Item memory was assessed by free recall and source memory was assessed by asking participants to classify the recalled pictures into the two kinds of pictures. The results indicated that item memory was greater for the negatively arousing pictures than for the positively arousing and the neutral pictures. However, the negatively arousing pictures produced more misattribution errors than the neutral pictures, replicating source memory impairment. It was concluded that source memory impairment associated with negatively arousing stimuli occurs at encoding.     

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.     

Emotion, directed forgetting, and source memory

We investigated the role of emotion on item and source memory using the item method of directed forgetting (DF) paradigm. We predicted that emotion would produce source memory impairment because emotion would make it more difficult to distinguish between to-be-remembered (R items) and to-be-forgotten items (F items) by making memory strength of R and F items similar to each other. Participants were presented with negatively arousing, positively arousing, and neutral pictures. After each picture, they received an instruction to remember or forget the picture. At retrieval, participants were asked to recall both R and F items and indicate whether each item was an R or F item. Recall was higher for the negatively arousing than for the positively arousing or neutral pictures. Further, DF occurred for the positively arousing and neutral pictures, whereas DF was not significant for the negatively arousing pictures. More importantly, the negatively arousing pictures, particularly the ones with violent content, showed a higher tendency of producing misattribution errors than the other picture types, supporting the notion that negative emotion may produce source memory impairment, even though it is still not clear whether the impairment occurs at encoding or retrieval.     

Emotionally enhanced memory for negatively arousing words: storage or retrieval advantage?

People typically remember emotionally negative words better than neutral words. Two experiments are reported that investigate whether emotionally enhanced memory (EEM) for negatively arousing words is based on a storage or retrieval advantage. Participants studied non-word–word pairs that either involved negatively arousing or neutral target words. Memory for these target words was tested by means of a recognition test and a cued-recall test. Data were analysed with a multinomial model that allows the disentanglement of storage and retrieval processes in the present recognition-then-cued-recall paradigm. In both experiments the multinomial analyses revealed no storage differences between negatively arousing and neutral words but a clear retrieval advantage for negatively arousing words in the cued-recall test. These findings suggest that EEM for negatively arousing words is driven by associative processes.     

Cortisol and stimulus-induced arousal level differentially impact memory for items and backgrounds

Most studies examine the effects of stress on memory for visual information test memory for entire scenes. However, arousal levels may differentially influence memory for backgrounds as opposed to items. Participants encoded scenes that included a negative-high-arousal, negative-moderate-arousal, or neutral item on a neutral background. After a 30-minute (Experiment 1) or 48-hour delay (Experiment 2), participants underwent a stressor or control task while heart rate was recorded. A recognition memory task was then given with items and backgrounds presented separately. High-arousal images had a greater detriment in background memory than moderate-arousal images. Further, though there was evidence that change in cortisol level at retrieval was associated with impaired memory for items, it was not associated with detriments in background memory. Increased heart rate was associated with impaired memory for both items and backgrounds. This suggests that the level of sympathetic and cortisol reactivity differentially affects memory for items and backgrounds.     

Acute consolidation stress enhances reality monitoring in healthy young adults

Source monitoring refers to cognitive processes involved in making attributions about the origins of memories, knowledge, and beliefs. One particular type of source monitoring with ample practical significance is reality monitoring, i.e., the ability to discriminate between internally vs. externally generated memories. Abundant evidence indicates that exposure to acute stress enhances declarative memory consolidation. To date, no study has looked at whether exposure to acute stress during the consolidation phase may promote reality monitoring performance. The authors examined this by administering cold pressor stress (CPS) or a control procedure to participants (N = 80) after they had either performed or only imagined performing simple motor acts, and assessing reality monitoring 24 h later. When compared with the control condition, CPS significantly elevated salivary free cortisol concentrations and enhanced reality monitoring. Stress-induced cortisol responses, however, were found not to be related to improved reality monitoring performance. Our findings are consistent with the view that post-learning stress hormone-related activity may modulate source memory consolidation.     

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.     

情绪效价的记忆增强效应:存储或提取优势?

情绪效价和情绪唤醒是描述情绪的两个维度。情绪增强记忆效应表明情绪唤醒事件的记忆往往优于非情绪唤醒事件的记忆,但关于积极情绪记忆和消极情绪记忆哪个在记忆中处于优势仍存在争论。实验以情绪词对和中性词对为实验材料。实验一探讨积极情绪词语或消极情绪词语的记忆优势; 实验二探讨积极情绪环境或消极情绪环境中中性词语的记忆优势。在两种实验条件下,积极情绪下的自由回忆都优于消极情绪下的自由回忆; 多项加工树的存储—提取模型使用实验自由回忆和线索回忆的结果将记忆的存储和提取优势分离开来,结果表明:积极情绪事件记忆优势发生在存储阶段,而积极情绪环境记忆优势发生在存储和提取阶段; 积极情绪事件记忆偏向支持“刺激后编码增强假设”,积极情绪环境记忆偏向支持“唤醒—偏向竞争假设”。     

Enhancing effects of acute psychosocial stress on priming of non-declarative memory in healthy young adults

Social stress affects cognitive processes in general, and memory performance in particular. However, the direction of these effects has not been clearly established, as it depends on several factors. Our aim was to determine the impact of the hypothalamus-pituitary-adrenal (HPA) axis and sympathetic nervous system (SNS) reactivity to psychosocial stress on short-term non-declarative memory and declarative memory performance. Fifty-two young participants (18 men, 34 women) were subjected to the Trier Social Stress Task (TSST) and a control condition in a crossover design. Implicit memory was assessed by a priming test, and explicit memory was assessed by the Rey Auditory Verbal Learning Test (RAVLT). The TSST provoked greater salivary cortisol and salivary alpha-amylase (sAA) responses than the control task. Men had a higher cortisol response to stress than women, but no sex differences were found for sAA release. Stress was associated with an enhancement of priming but did not affect declarative memory. Additionally, the enhancement on the priming test was higher in those whose sAA levels increased more in response to stress (r(48)?=?0.339, p?=?0.018). Our results confirm an effect of acute stress on priming, and that this effect is related to SNS activity. In addition, they suggest a different relationship between stress biomarkers and the different memory systems.     

The moderating effects of stimulus valence and arousal on memory suppression

This study examined the separate and combined effects of stimulus valence and arousal on retrieval inhibition. Participants performed Anderson and Green's (2001) memory suppression task with stimuli varying across dimensions of valence and arousal. Memory was tested through free and cued recall as well as speeded recognition. Results showed that both stimulus valence and arousal influenced the extent to which participants successfully inhibited retrieval, but not in the ways anticipated. Specifically, the strongest inhibition effects were for highly arousing, pleasant words. In addition, unpleasant stimuli that were suppressed were better recalled during both cued and free-recall tasks than pleasant stimuli that were suppressed. Across all tests of memory performance, there were no significant differences between the experimental conditions for highly arousing, unpleasant words. The implications of these findings are discussed.