Sex differences in emotional memory consolidation: the effect of stress-induced salivary alpha-amylase and cortisol

This study examined sex differences in the emotional memory consolidation, and the impact of stress-induced cortisol and salivary alpha amylase responses on emotional memory recall. Following baseline salivary measures, 39 healthy women and 41 men viewed 20 neutral and 20 negative arousing images, and then underwent either a cold pressor stress test or control condition, followed by further salivary measures. Participants returned two days later for a free recall test. The stress condition induced greater cortisol response, and negative images were better recalled than neutral. Whereas women displayed greater recall of negative images under stress than men, they recalled fewer negative images in the control condition. Stress-induced cortisol predicted recall of negative images in women, and neutral images in men. This suggests there is an enhanced consolidation of negative images under stress in women that may be a potential mechanism for the greater female prevalence for developing anxiety disorders.     

Pre-learning stress differentially affects long-term memory for emotional words, depending on temporal proximity to the learning experience

Stress exerts a profound, yet complex, influence on learning and memory and can enhance, impair or have no effect on these processes. Here, we have examined how the administration of stress at different times before learning affects long-term (24-hr) memory for neutral and emotional information. Participants submerged their dominant hand into a bath of ice cold water (Stress) or into a bath of warm water (No stress) for 3 min. Either immediately (Exp. 1) or 30 min (Exp. 2) after the water bath manipulation, participants were presented with a list of 30 words varying in emotional valence. The next day, participants' memory for the word list was assessed via free recall and recognition tests. In both experiments, stressed participants exhibited greater blood pressure, salivary cortisol levels, and subjective pain and stress ratings than non-stressed participants in response to the water bath manipulation. Stress applied immediately prior to learning (Exp. 1) enhanced the recognition of positive words, while stress applied 30 min prior to learning (Exp. 2) impaired free recall of negative words. Participants' recognition of positive words in Experiment 1 was positively associated with their heart rate responses to the water bath manipulation, while participants' free recall of negative words in Experiment 2 was negatively associated with their blood pressure and cortisol responses to the water bath manipulation. These findings indicate that the differential effects of pre-learning stress on long-term memory may depend on the temporal proximity of the stressor to the learning experience and the emotional nature of the to-be-learned information.     

Psychosocial stress enhances non-drug-related positive memory retrieval in male abstinent heroin addicts

Stress exposure in addicted individuals is known to provoke drug craving, presumably through a memory-like process, but less is known about the effects of stress on non-drug-related affective memory retrieval per se in such individuals, which is likely to provide important insights into therapy for relapse. In present study, we explored the effect of stress on retrieval of neutral and emotionally valenced (positive and negative) words in abstinent heroin addicts. In present study, 28 male inpatient abstinent heroin addicts and 20 sex-, age-, education- and economic status-matched healthy control participants were assessed for 24 h delayed recall of valenced and neutral word lists on two occasions 4 weeks apart—once in a nonstress control condition, once after exposure to the Trier Social Stress Test in a counterbalanced design. In addition, attention, working memory, blood pressure, heart rate and salivary cortisol were assessed. We found acute stress at the time of word list recall enhanced retrieval of positively valenced words, but no effect on negative and neutral word retrieval in abstinent heroin addicts was observed. No changes were detected for attention and working memory. The stressor induced a significant increase in salivary free cortisol, blood pressure and heart rate. Stress can enhance non-drug-related positive memory in abstinent heroin addicts. Our findings will provide richer information in understanding dysregulation of their emotional memory processing under stress and hopefully provide insight into designing improved treatments for drug addiction.     

Cortisol variation in humans affects memory for emotionally laden and neutral information

In a test of the effects of cortisol on emotional memory, 90 men were orally administered placebo or 20 or 40 mg cortisol and presented with emotionally arousing and neutral stimuli. On memory tests administered within 1 hr of stimulus presentation, cortisol elevations caused a reduction in the number of errors committed on free-recall tasks. Two evenings later, when cortisol levels were no longer manipulated, inverted-U quadratic trends were found for recognition memory tasks, reflecting memory facilitation in the 20-mg group for both negative and neutral information. Results suggest that the effects of cortisol on memory do not differ substantially for emotional and neutral information. The study provides evidence of beneficial effects of acute cortisol elevations on explicit memory in humans.     

The neural fate of neutral information in emotion‐enhanced memory

In this study, we report evidence that neural activity reflecting the encoding of emotionally neutral information in memory is reduced when neutral and emotional stimuli are intermixed during encoding. Specifically, participants studied emotional and neutral pictures organized in mixed lists (in which emotional and neutral pictures were intermixed) or in pure lists (only‐neutral or only‐emotional pictures) and performed a recall test. To estimate encoding efficiency, we used the Dm effect, measured with event‐related potentials. Recall for neutral items was lower in mixed compared to pure lists and posterior Dm activity for neutral items was reduced in mixed lists, whereas it remained robust in pure lists. These findings might be caused by an asymmetrical competition for attentional and working memory resources between emotional and neutral information, which could be a major determinant of emotional memory effects.     

Hormonal contraception use alters stress responses and emotional memory

Emotionally arousing material is typically better remembered than neutral material. Since norepinephrine and cortisol interact to modulate emotional memory, sex-related influences on stress responses may be related to sex differences in emotional memory. Two groups of healthy women – one naturally cycling (NC women, n = 42) and one using hormonal contraceptives (HC women, n = 36) – viewed emotionally arousing and neutral images. Immediately after, they were assigned to Cold Pressor Stress (CPS) or a control procedure. One week later, participants received a surprise free recall test. Saliva samples were collected and later assayed for salivary alpha-amylase (biomarker for norepinephrine) and cortisol. Compared to NC women, HC women exhibited significantly blunted stress hormone responses to the images and CPS. Recall of emotional images differed between HC and NC women depending on noradrenergic and cortisol responses. These findings may have important implications for understanding the neurobiology of emotional memory disorders, especially those that disproportionately affect women.     

Sleep benefits emotional and neutral associative memories equally

Background

Emotions modulate memory. It has been suggested that sleep contributes to improved memory of emotional events by preferentially consolidating emotional memories, presumably because of a selective off-line reactivation of information relevant to future behavior.

Objectives

We aimed to validate sleep-dependent memory consolidation in a new associative emotional memory paradigm suitable for inducing memory reactivations during sleep. We hypothesized that sleep preferentially might benefit the consolidation of emotional associations independently of their negative vs positive emotional valence.

Methods

Seventy-two healthy young participants performed an associative emotional memory task in either the evening or the morning. During the task, they were asked to associate neutrally spoken words to neutral, negative or positive pictures. Cued recall was tested after a 12-h retention interval filled with either night-time sleep or daytime wakefulness.

Results

Generally, emotional associations were better remembered than neutral ones. However, we were not able to replicate a selective benefit of sleep on emotional memory. Sleep robustly improved the cued recall performance of all picture types compared with wakefulness, without any modulating influence of emotional arousal or valence.

Conclusions

We conclude that the consolidation of explicitly learned associations benefits from sleep, independent of emotional arousal or valence. Selective emotional memory consolidation during sleep may be restricted to non-associative item memory or incidentally learned emotional associations.

     

A non-arousing test situation abolishes the impairing effects of cortisol on delayed memory retrieval in healthy women

Animal and human studies have repeatedly shown that stress hormones influence memory. Glucocorticoids (GCs) enhance memory consolidation but impair memory retrieval. Studies in rodents indicate that adrenergic activation is necessary for GC induced effects on memory. We have shown, in two previous placebo-controlled double-blind experiments, that memory retrieval is significantly impaired after oral cortisol (30 mg) treatment in healthy young women. Here, we changed the experimental setting before and during the retrieval testing, so that the participants (n=31) experienced a more relaxed test situation. The learning material, the timing and the tester used were identical to the two previous studies. In the relaxed condition no effect of cortisol on memory retrieval occurred (p=0.84). The results indicate that the experimental setting can influence the effect of cortisol on memory. Our findings suggest that glucocorticoid effects on memory retrieval require testing-associated arousal in humans.     

Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions

Extensive evidence from rat and human studies indicates that glucocorticoid hormones influence cognitive performance. Posttraining activation of glucocorticoid-sensitive pathways dose-dependently enhances the consolidation of long-term memory. Glucocorticoid effects on memory consolidation rely on noradrenergic activation of the basolateral amygdala and interactions of the basolateral amygdala with other brain regions. Glucocorticoids interact with the noradrenergic system both at a postsynaptic level, increasing the efficacy of the beta-adrenoceptor-cyclic AMP/protein kinase A system, as well as presynaptically in brainstem noradrenergic cell groups that project to the basolateral amygdala. In contrast, memory retrieval and working memory performance are impaired with high circulating levels of glucocorticoids. Glucocorticoid-induced impairment of these two memory functions also requires the integrity of the basolateral amygdala and the noradrenergic system. Such critical interactions between glucocorticoids and noradrenergic activation of the basolateral amygdala have important consequences for the role of emotional arousal in enabling glucocorticoid effects on these different memory functions.     

The effects of glucocorticoids on the inhibition of emotional information: A dose-response study

There is evidence that cortisol influences cognitive and affective processes such as selective attention and memory for emotional events, yet the effects of glucocorticoids on attentional inhibition in humans remain unknown. Consequently, this double-blind study examined dose-dependent effects of exogenous glucocorticoids on the inhibition of emotional information. Sixty-three university students (14 male, 49 female) ingested either a placebo pill or hydrocortisone (10 mg or 40 mg), and completed a negative priming task assessing the inhibition of pictures depicting angry, sad, and happy faces. The 10 mg, but not the 40 mg hydrocortisone dose elicited increased inhibition for angry faces relative to placebo. Thus, moderate glucocorticoid elevations may have adaptive effects on emotional information processing, whereas high glucocorticoid elevations appear to attenuate this effect, consistent with the view that there are dose-dependent effects of glucocorticoids on cognition.     

Temporal effects of dehydroepiandrosterone sulfate on memory formation in day-old chicks

Dehydroepiandrosterone sulfate (DHEAS) has been shown to enhance memory retention in different animal models and in various learning paradigms. In the present study, we investigated the effect of peripherally administered DHEAS on the acquisition, consolidation and retention of memory using a weak version of the one-trial passive avoidance task in day-old chicks. Intraperitoneally administered DHEAS (20 mg/kg) either 30 min before or 30 min and 4.5 h after training on the weakly aversive stimulus, enhanced recall at 24 h following training, suggesting a potentiation of not only the acquisition but also the early and late phases of memory consolidation. In contrast, when DHEAS was administered at 30 min prior to the 24 h retention test there was no memory enhancement, indicating a lack of effect on memory retrieval. Memory recall was unaltered when DHEAS was administered at 30 min before training in a control group trained on a strongly aversive stimulus, confirming memory-specific effects. Interestingly, the memory enhancement appeared to be sex-specific as male chicks showed higher recall than females. These findings provide further evidence that DHEAS enhances memory and may be involved in the temporal cascade of long-term memory formation.     

Local context influences memory for emotional stimuli but not electrophysiological markers of emotion‐dependent attention

Emotional enhancement of free recall can be context dependent. It is readily observed when emotional and neutral scenes are encoded and recalled together in a “mixed” list, but diminishes when these scenes are encoded separately in “pure” lists. We examined the hypothesis that this effect is due to differences in allocation of attention to neutral stimuli according to whether they are presented in mixed or pure lists, especially when encoding is intentional. Using picture stimuli that were controlled for semantic relatedness, our results contradicted this hypothesis. The amplitude of well‐known electrophysiological markers of emotion‐related attention—the early posterior negativity (EPN), the late positive potential (LPP), and the slow wave (SW)—was higher for emotional stimuli. Crucially, the emotional modulation of these ERPs was insensitive to list context, observed equally in pure and mixed lists. Although list context did not modulate neural markers of emotion‐related attention, list context did modulate the effect of emotion on free recall. The apparent decoupling of the emotional effects on attention and memory, challenges existing hypotheses accounting for the emotional enhancement of memory. We close by discussing whether findings are more compatible with an alternative hypothesis, where the magnitude of emotional memory enhancement is, at least in part, a consequence of retrieval dynamics.     

Acute cortisol effects on immediate free recall and recognition of nouns depend on stimulus valence

The present study investigated the acute effects of cortisol administration in normal healthy male volunteers on immediate free recall and recognition of pleasant, unpleasant, and neutral nouns using a between-subjects double-blind design. Two hours after cortisol (10 mg) or placebo administration, impaired recall and recognition of neutral and pleasant words was found in the treatment group, whereas recall and recognition of unpleasant words was similar in both groups. The interaction between treatment and stimulus valence was not mediated by "semantic cohesion," nor does it seem to have been mediated by stimulus arousal. Cortisol did not change mood. The changes with cortisol in recall and recognition of pleasant and unpleasant words parallel those found in depression, a condition that is often accompanied by elevated basal cortisol levels.     

Relationship between the effects of word emotionality and the consciousness of retrieval process in memory

Two experiments were carried out to examine the effects of word emotionality on explicit and implicit memory. In Experiment 1, 46 undergraduates studied a word list followed by free recall or word-stem completion test. The list was consisted of 36 nouns with pleasant, neutral, and unpleasant words. In free recall test, both the pleasant and unpleasant words were more recalled than the neutral words. In word-stem completion test, there were no significant effects of emotional value. Experiment 2 reexamined the result of word-stem completion test in Experiment 1. A process-dissociation procedure was used to estimate two components of conscious and automatic retrieval process in implicit memory. The results suggest that the emotionality of words had a facilitative effect on conscious component but no effect on unconscious component.     

Laugh yourself to sleep: memory consolidation for humorous information

There is extensive evidence that emotional information is better remembered than neutral information across long delays, especially if the delay interval contains an opportunity for sleep. However, as prior studies have focused on memory for negative stimuli, it is unclear whether positive memories benefit from time and sleep as well. To investigate the consolidation of positive memories, the current study examined differences in memory for humorous and non-humorous cartoons. While prior evidence demonstrates that humorous information is preferentially remembered relative to non-humorous information over brief delays, it is unknown whether this benefit lasts across longer delay intervals or whether sleep is important for lasting humor memories to form. Thus, we tested memory for 27 cartoons across 12-h delay periods containing either sleep or wakefulness. Results indicate that humor’s enhancing effect on recall memory is robust across a 12-h delay and that a period of sleep facilitates this effect over wakefulness when cartoons are novel to participants and ranked based on subjective emotional ratings. Further, in accordance with previous studies that reveal diminished emotional reactivity to stimuli following sleep, in a supplemental experiment, we found that sleep reduced subjective ratings of humor, arousal, and positivity of humorous cartoons. These findings provide preliminary evidence that sleep’s impact on negative emotional memory consolidation and emotional reactivity can be extended to positive stimuli as well.     

Event‐related potentials of emotional and neutral memories: The role of encoding position and delayed testing

Previous research found that memory is not only better for emotional information but also for neutral information that has been encoded in the context of an emotional event. In the present ERP study, we investigated two factors that may influence memory for neutral and emotional items: temporal proximity between emotional and neutral items during encoding, and retention interval (immediate vs. delayed). Forty‐nine female participants incidentally encoded 36 unpleasant and 108 neutral pictures (36 neutral pictures preceded an unpleasant picture, 36 followed an unpleasant picture, and 36 neutral pictures were preceded and followed by neutral pictures) and participated in a recognition memory task either immediately (N = 24) or 1 week (N = 25) after encoding. Results showed better memory for emotional pictures relative to neutral pictures. In accordance, enhanced centroparietal old/new differences (500–900 ms) during recognition were observed for unpleasant compared to neutral pictures, most pronounced for the 1‐week interval. Picture position effects, however, were only subtle. During encoding, late positive potentials for neutral pictures were slightly lower for neutral pictures following unpleasant ones, but only at trend level. To summarize, we could replicate and extend previous ERP findings showing that emotionally arousing events are better recollected than neutral events, particularly when memory is tested after longer retention intervals. Picture position during encoding, however, had only small effects on elaborative processing and no effects on memory retrieval.     

No effect of targeted memory reactivation during slow‐wave sleep on emotional recognition memory

Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (versus non‐salient) memories. Using a technique known as targeted memory reactivation, it is possible to selectively strengthen newly learned memories by re‐exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to targeted memory reactivation in slow‐wave sleep than neutral memories. In an initial training phase, participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90‐min nap opportunity, during which half the sounds were re‐presented during slow‐wave sleep (as assessed via online polysomnographic sleep monitoring). We observed no effect of targeted memory reactivation on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess targeted memory reactivation, and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural targeted memory reactivation benefits. To fully assess the impacts of targeted memory reactivation on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.     

Inverted-U function between salivary cortisol and retrieval of verbal memory after hydrocortisone treatment

The present study investigated the effect of a single oral dose of hydrocortisone (cortisol) on retrieval of verbal and nonverbal declarative memory. Fifty-nine healthy participants were randomly assigned to either receive 25 mg cortisol or a placebo 45 min before retrieval in a standardized memory test procedure. There was no global effect of cortisol on either verbal or nonverbal memory. However, a specific negative effect on free recall of associative verbal material appeared. In addition, high responders (salivary cortisol concentration>68.25 nmol/L) exhibited impaired verbal memory compared with low responders (<68.25 nmol/L). The results suggest specific nonlinear effects of cortisol on declarative memory retrieval, which appear to be more pronounced for verbal material.     

Memory enhancement for emotional stimuli is impaired in early Alzheimer's disease

Emotional arousal is associated with enhanced memory in neurologically intact individuals, but it is unknown whether this effect is obtained in Alzheimer's disease (AD). The current study compared emotional memory and emotional reactions in patients with early AD and in older controls. Participants viewed emotionally arousing (both pleasant and unpleasant) and neutral photographs while cognitive and electrophysiological reactions were assessed. Memory was tested by free recall and recognition. Emotional reactions were normal in the AD group, but the emotional memory effect (enhanced memory for emotional vs. neutral stimuli) was impaired. Recall results indicated that this effect was normal for pleasant stimuli but abnormal for unpleasant stimuli. These results suggest that the neural basis for the emotional memory effect may be disrupted in AD. Findings are discussed in terms of the role of the amygdala in mediating emotional memory.     

Filling in memory gaps through emotional communication; promising pathways in caring for persons with dementia

ObjectiveTo explore in what way emotional communication can enhance the memory of people with (different types of) dementia.MethodsRelevant studies published after 2000 were searched using the terms: dementia, positive, words, communication, recall, and memory. Papers were included that reported results of studies with people with dementia that investigated memory effects of communication with either an emotionally valent content or context.ResultsTwelve papers grouped under four prevailing themes (pictures, facial emotions, stories and words) are described. The studies provide mixed results: in some studies negative emotional information enhances memory in older people with dementia, in other studies positive emotional information is helpful or hardly any effect is found.ConclusionEmotional communication seems to enhance memory in people with dementia. None of the studies described focused on the association between personally relevant, emotionally valent information and memory, so further research is needed.Practice implicationsCaregivers in dementia care should realize that 1) the information they provide might carry an emotional valence, and 2) this valence might influence the extent to which people with dementia remember information.