Sleep preferentially consolidates negative aspects of human memory: Well-powered evidence from two large online experiments.

Research suggests that sleep benefits memory. Moreover, it is often claimed that sleep selectively benefits memory for emotionally salient information over neutral information. However, not all scientists are convinced by this relationship [e.g., J. M. Siegel. Curr. Sleep Med. Rep., 7, 15-18 (2021)]. One criticism of the overall sleep and memory literature-like other literature-is that many studies are underpowered and lacking in generalizability [M. J. Cordi, B. Rasch. Curr. Opin. Neurobiol., 67, 1-7 (2021)], thus leaving the evidence mixed and confusing to interpret. Because large replication studies are sorely needed, we recruited over 250 participants spanning various age ranges and backgrounds in an effort to confirm sleep's preferential emotional memory consolidation benefit using a well-established task. We found that sleep selectively benefits memory for negative emotional objects at the expense of their paired neutral backgrounds, confirming our prior work and clearly demonstrating a role for sleep in emotional memory formation. In a second experiment also using a large sample, we examined whether this effect generalized to positive emotional memory. We found that while participants demonstrated better memory for positive objects compared to their neutral backgrounds, sleep did not modulate this effect. This research provides strong support for a sleep-specific benefit on memory consolidation for specifically negative information and more broadly affirms the benefit of sleep for cognition.

The effects of shared, depression-specific, and anxiety-specific internalizing symptoms on negative and neutral episodic memories following post-learning sleep.

Emotional memory bias is a common characteristic of internalizing symptomatology and is enhanced during sleep. The current study employs bifactor S-1 modeling to disentangle depression-specific anhedonia, anxiety-specific anxious arousal, and the common internalizing factor, general distress, and test whether these internalizing symptoms interact with sleep to influence memory for emotional and neutral information. Healthy adults (N = 281) encoded scenes featuring either negative objects (e.g., a vicious looking snake) or neutral objects (e.g., a chipmunk) placed on neutral backgrounds (e.g., an outdoor scene). After a 12-hour period of daytime wakefulness (n = 140) or nocturnal sleep (n = 141), participants judged whether objects and backgrounds were the same, similar, or new compared with what they viewed during encoding. Participants also completed the mini version of the Mood and Anxiety Symptom Questionnaire. Higher anxious arousal predicted worse memory across all stimuli features, but only after a day spent being awake-not following a night of sleep. No significant effects were found for general distress and anhedonia in either the sleep or wake condition. In this study, internalizing symptoms were not associated with enhanced emotional memory. Instead, memory performance specifically in individuals with higher anxious arousal was impaired overall, regardless of emotional valence, but this was only the case when the retention interval spanned wakefulness (i.e., not when it spanned sleep). This suggests that sleep may confer a protective effect on general memory impairments associated with anxiety.

Perceived event resolution-rather than time-allows older adults to reduce the negativity of their memories.

In addition to showing greater memory positivity soon after negative events, older adults can be more likely than younger adults to show decreases in memory negativity as events grow more distant. We recently showed that this latter effect was not present when adults were asked to rate memories of the initial phase of the COVID-19 pandemic (March-May 2020): after a short (June/July 2020) and long delay (October/November 2020), older age was associated with greater reflections on positive aspects, but with no difference in negative aspects. We suggested that older adults did not show decreased negativity because the pandemic was still prevalent in their daily lives. The present study examines whether perceived event resolution-rather than time on its own-may be necessary to show age-related decreases in negativity by surveying participants during a time when many may have felt like the pandemic had resolved (Summer 2021). Once again, age was associated with increased ratings of the positive aspects, but at this timepoint, age was also associated with decreased ratings of the negative aspects. These results suggest that older adults may more successfully decrease the negativity of their memories compared to younger adults only when they feel that events have resolved.

How list composition affects the emotional enhancement of memory in younger and older adults.

Young adults show an immediate emotional enhancement of memory (EEM) when emotional and non-emotional information are presented in mixed lists but not pure lists, but it is unclear whether older adults' memories also benefit from the cognitive factors producing the list-composition effect. The present study examined whether the list-composition effect extended to older adults (55+), testing the following alternatives: (1) younger and older adults could show the list-composition effect, (2) due to age-related decreases in cognitive resources, older adults may show weaker effects of list-composition, or (3) due to age-related positivity effects, older adults' list-composition effect may vary by valence. Results supported the first alternative: the list-composition effect occurred for older as well as younger adults, when testing memory for pictures (Experiment 1) or words (Experiment 2). In a third experiment, we explored whether mixing information at only encoding or retrieval (and blocking in the other phase) would suffice for the list composition effect to occur. Results revealed that mixed encoding/blocked retrieval did not elicit the EEM in either age group. Overall, the results suggest age-related stability in the cognitive processes that give rise to the immediate EEM.

The effects of cognitive reappraisal and sleep on emotional memory formation.

Emotion regulation (i.e. either up- or down-regulating affective responses to emotional stimuli) has been shown to modulate long-term emotional memory formation. Further, research has demonstrated that the emotional aspects of scenes are preferentially remembered relative to neutral aspects (known as the emotional memory trade-off effect). This trade-off is often enhanced when sleep follows learning, compared to an equivalent period of time spent awake. However, the interactive effects of sleep and emotion regulation on emotional memory are poorly understood. We presented 87 participants with pictures of neutral or negative objects on neutral backgrounds paired with instructions to either increase or decrease their emotional response by altering personal relevance, or to passively view the stimuli. Following a 12 h period of sleep or wakefulness, participants were tested for their memory of objects and backgrounds separately. Although we replicated the emotional memory trade-off effect, no differences in the magnitude of the trade-off effect were observed between regulation conditions. Sleep improved all aspects of memory, but it did not preferentially benefit memory for emotional components of scenes. Irrespective of a period of sleep or wake following encoding, findings suggest emotion regulation during encoding did not influence memory for emotional items at a 12-hour delay.

Medial prefrontal cortex has a causal role in selectively enhanced consolidation of emotional memories after a 24-hour delay: A TBS study.

Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared to co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short (30-minute) and a long delay (24-hour, including a night of sleep) to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information.SIGNIFICANCE STATEMENT:Understanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation (repetitive transcranial magnetic stimulation, rTMS) to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24-hr delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this "tag-and-capture" mechanism during the initial formation of such memories.

Slow oscillation-spindle coupling is negatively associated with emotional memory formation following stress.

Both stress and sleep enhance emotional memory. They also interact, with the largest effect of sleep on emotional memory being seen when stress occurs shortly before or after encoding. Slow wave sleep (SWS) is critical for long-term episodic memory, facilitated by the temporal coupling of slow oscillations and sleep spindles. Prior work in humans has shown these associations for neutral information in non-stressed participants. Whether coupling interacts with stress to facilitate emotional memory formation is unknown. Here, we addressed this question by reanalyzing an existing dataset of 64 individuals. Participants underwent a psychosocial stressor (32) or comparable control (32) prior to the encoding of 150-line drawings of neutral, positive, and negative images. All participants slept overnight with polysomnography, before being given a surprise memory test the following day. In the stress group, time spent in SWS was positively correlated with memory for images of all valences. Results were driven by those who showed a high cortisol response to the stressor, compared to low responders. The amount of slow oscillation-spindle coupling during SWS was negatively associated with neutral and emotional memory in the stress group only. The association with emotional memory was significantly stronger than for neutral memory within the stress group. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory.

Distinct stress-related changes in intrinsic amygdala connectivity predict subsequent positive and negative memory performance.

Experiencing stress before an event can influence how that event is later remembered. In the current study, we examine how individual differences in one's physiological response to a stressor are related to changes to underlying brain states and memory performance. Specifically, we examined how changes in intrinsic amygdala connectivity relate to positive and negative memory performance as a function of stress response, defined as a change in cortisol. Twenty-five participants underwent a social stressor before an incidental emotional memory encoding task. Cortisol samples were obtained before and after the stressor to measure individual differences in stress response. Three resting state scans (pre-stressor, post-stressor/pre-encoding and post-encoding) were conducted to evaluate pre- to post-stressor and pre- to post-encoding changes to intrinsic amygdala connectivity. Analyses examined relations between greater cortisol changes and connectivity changes. Greater cortisol increases were associated with a greater decrease in prefrontal-amygdala connectivity following the stressor and a reversal in the relation between prefrontal-amygdala connectivity and negative vs. positive memory performance. Greater cortisol increases were also associated with a greater increase in amygdala connectivity with a number of posterior sensory regions following encoding. Consistent with prior findings in non-stressed individuals, pre- to post-encoding increases in amygdala-posterior connectivity were associated with greater negative relative to positive memory performance, although this was specific to lateral rather than medial posterior regions and to participants with the greatest cortisol changes. These findings suggest that stress response is associated with changes in intrinsic connectivity that have downstream effects on the valence of remembered emotional content.

The power of negative and positive episodic memories.

The power of episodic memories is that they bring a past moment into the present, providing opportunities for us to recall details of the experiences, reframe or update the memory, and use the retrieved information to guide our decisions. In these regards, negative and positive memories can be especially powerful: Life's highs and lows are disproportionately represented in memory, and when they are retrieved, they often impact our current mood and thoughts and influence various forms of behavior. Research rooted in neuroscience and cognitive psychology has historically focused on memory for negative emotional content. Yet the study of autobiographical memories has highlighted the importance of positive emotional memories, and more recently, cognitive neuroscience methods have begun to clarify why positive memories may show powerful relations to mental wellbeing. Here, we review the models that have been proposed to explain why emotional memories are long-lasting (durable) and likely to be retrieved (accessible), describing how in overlapping-but distinctly separable-ways, positive and negative memories can be easier to retrieve, and more likely to influence behavior. We end by identifying potential implications of this literature for broader topics related to mental wellbeing, education, and workplace environments.

Age and chronotype influenced sleep timing changes during the first wave of the COVID-19 pandemic.

Social restrictions necessary to reduce the spread of coronavirus disease 2019 (COVID-19) profoundly changed how we socialised, worked and, for students, attended classes. Interestingly, significant sleep pattern shifts occurred in the context of pandemic-related social restrictions. Whether age and chronotype influenced these sleep pattern changes remains poorly understood. In this pre-registered (https://osf.io/4a3fx), web-based study, United States residents reported, in one-time assessments, demographic information, self-reported chronotype using the reduced Morningness-Eveningness Questionnaire, and pre-pandemic and pandemic first wave sleep timing using the Ultrashort Munich Chronotype Questionnaire. Participants reported sleep phase delays, reduced social jetlag (SJL) and reduced social sleep restriction (SSR) during the first wave of the pandemic compared to pre-pandemic. Pandemic-related changes in SJL and SSR varied with participants' age and self-reported chronotype. Young adults reported the greatest reductions in SJL and young adults and individuals with evening chronotypes reported the greatest reductions in SSR. We conclude that these groups may have been the most vulnerable to social-biological sleep timing desynchrony under pre-pandemic social, occupational, and educational schedules.

Consciousness as a Memory System.

We suggest that there is confusion between why consciousness developed and what additional functions, through continued evolution, it has co-opted. Consider episodic memory. If we believe that episodic memory evolved solely to accurately represent past events, it seems like a terrible system-prone to forgetting and false memories. However, if we believe that episodic memory developed to flexibly and creatively combine and rearrange memories of prior events in order to plan for the future, then it is quite a good system. We argue that consciousness originally developed as part of the episodic memory system-quite likely the part needed to accomplish that flexible recombining of information. We posit further that consciousness was subsequently co-opted to produce other functions that are not directly relevant to memory per se, such as problem-solving, abstract thinking, and language. We suggest that this theory is compatible with many phenomena, such as the slow speed and the after-the-fact order of consciousness, that cannot be explained well by other theories. We believe that our theory may have profound implications for understanding intentional action and consciousness in general. Moreover, we suggest that episodic memory and its associated memory systems of sensory, working, and semantic memory as a whole ought to be considered together as the conscious memory system in that they, together, give rise to the phenomenon of consciousness. Lastly, we suggest that the cerebral cortex is the part of the brain that makes consciousness possible, and that every cortical region contributes to this conscious memory system.

With age comes well-being: older age associated with lower stress, negative affect, and depression throughout the COVID-19 pandemic.

Objectives: Despite initial concerns about older adult's emotional well-being during the COVID-19 pandemic, reports from the first months of the pandemic suggested that older adults were faring better than younger adults, reporting lower stress, negative affect, depression, and anxiety. In this study, we examined whether this pattern would persist as the pandemic progressed.Method: A convenience sample of 1,171 community-dwelling adults in the United States, ages 18-90, filled out surveys on various metrics of emotional well-being starting in March 2020 and at various time points through April 2021. We created time bins to account for the occurrence of significant national events, allowing us to determine how age would relate to affective outcomes when additional national-level emotional events were overlaid upon the stress of the pandemic.Results: Older age was associated with lower stress, negative affect, and depressive symptomatology, and with higher positive affect, and this effect was consistent across time points measured from March, 2020 through April, 2021. Age was less associated with measures of worry and social isolation, but older adults were more worried about their personal health throughout the pandemic.Conclusion: These results are consistent with literature suggesting that older age is associated with increased resilience in the face of stressful life experiences and show that this pattern may extend to resilience in the face of a prolonged real-world stressor.Supplemental data for this article can be accessed online at https://doi.org/10.1080/13607863.2021.2010183 .

Higher post-encoding cortisol benefits the selective consolidation of emotional aspects of memory.

Emotional experiences create durable memory traces in the brain, especially when these memories are consolidated in the presence of stress hormones such as cortisol. Although some research suggests cortisol elevation can increase long-term memory for emotional relative to neutral content, the impact of stress and cortisol on the consolidation of emotional and neutral aspects of memories when they are part of the same experience remains unknown. Here, after encoding complex scenes consisting of negative or neutral objects placed on neutral backgrounds, participants were exposed to a psychosocial stressor (or matched control condition) in order to examine the impact of stress and cortisol on early consolidation processes. The next day, once cortisol levels had returned to baseline, specific and gist recognition memory were tested separately for objects and backgrounds. Results indicate that while there was a numerical increase in memory for negative objects in the stress group, higher endogenous cortisol concentrations were specifically associated with decreased memory for the neutral backgrounds originally paired with negative objects. Moreover, across all participants, cortisol levels were positively correlated with the magnitude of the emotional memory trade-off effect. Specifically, while memory for negative objects was preserved, elevated cortisol during early consolidation was associated with decreased memory for neutral backgrounds that were initially paired with negative objects. These memory effects were observed in both the stricter specific measure of memory and the less conservative measure of gist memory. Together, these findings suggest that rather than influencing all aspects of an experience similarly, elevated cortisol during early consolidation selectively preserves what is most emotionally salient and adaptive to remember while allowing the loss of memory for less important neutral information over time.

Retrieval of Emotional Events from Memory.

The enhancing effects of emotion on memory have been well documented; emotional events are often more frequently and more vividly remembered than their neutral counterparts. Much of the prior research has emphasized the effects of emotion on encoding processes and the downstream effects of these changes at the time of retrieval. In the current review, we focus specifically on how emotional valence influences retrieval processes, examining how emotion influences the experience of remembering an event at the time of retrieval (retrieval as an end point) as well as how emotion alters the way in which remembering the event affects the underlying memory representation and subsequent retrievals (retrieval as a starting point). We suggest ways in which emotion may augment or interfere with the selective enhancement of particular memory details, using both online and offline processes, and discuss how these effects of emotion may contribute to memory distortions in affective disorders.

Post-Encoding Amygdala-Visuosensory Coupling Is Associated with Negative Memory Bias in Healthy Young Adults.

The amygdala is well documented as the critical nexus of emotionally enhanced memory, yet its role in the creation of negative memory biases, better memory for negative compared with positive stimuli, has not been clarified. Although prior work suggests valence-specific effects at the moment of "online" encoding and retrieval, with enhanced visuosensory processes supporting negative memories in particular, here we tested the novel hypothesis that the amygdala engages with distant cortical regions after encoding in a manner that predicts inter-individual differences in negative memory biases in humans. Twenty-nine young adults (males and females) were scanned while they incidentally encoded negative, neutral, and positive scenes, each preceded by a line-drawing sketch of the scene. Twenty-four hours later, participants were scanned during an Old/New recognition memory task with only the line-drawings presented as retrieval cues. We replicated and extended our prior work, showing that enhanced online visuosensory recapitulation supports negative memory. Critically, resting-state scans flanked the encoding task, allowing us to show for the first time that individual differences in "off-line" increases in amygdala resting-state functional connectivity (RSFC) immediately following encoding relate to negative and positive memory bias at test. Specifically, post-encoding increases in amygdala RSFC with visuosensory and frontal regions were associated with the degree of negative and positive memory bias, respectively. These findings provide new evidence that valence-specific negative memory biases can be linked to the way that sensory processes are integrated into amygdala-centered emotional memory networks.SIGNIFICANCE STATEMENT Decades of research has placed the amygdala at the center of the emotional memory network. Despite the clinical importance of disproportionate memory for negative compared with positive events, it is not known whether post-encoding increases in amygdala-cortical coupling, possibly reflective of early consolidation processes, bear any influence on the degree or direction of such emotional memory biases. We demonstrate that, across participants, increases in post-encoding amygdala coupling with visuosensory and frontal regions are associated with more pronounced negative and positive memory biases, respectively. These findings provide the first evidence linking post-encoding amygdala modulation to the degree of negative or positive memory bias, emphasizing the need for valence-based accounts of the amygdala's role in emotional memory.

Interactive effects of stress reactivity and rapid eye movement sleep theta activity on emotional memory formation.

Sleep and stress independently enhance emotional memory consolidation. In particular, theta oscillations (4-7 Hz) during rapid eye movement (REM) sleep increase coherence in an emotional memory network (i.e., hippocampus, amygdala, and prefrontal cortex) and enhance emotional memory. However, little is known about how stress during learning might interact with subsequent REM theta activity to affect emotional memory. In the current study, we examined whether the relationship between REM theta activity and emotional memory differs as a function of pre-encoding stress exposure and reactivity. Participants underwent a psychosocial stressor (the Trier Social Stress Task; n = 32) or a comparable control task (n = 32) prior to encoding. Task-evoked cortisol reactivity was assessed by salivary cortisol rise from pre- to post-stressor, and participants in the stress condition were additionally categorized as high or low cortisol responders via a median split. During incidental encoding, participants studied 150 line drawings of negative, neutral, and positive images, followed by the complete color photo. All participants then slept overnight in the lab with polysomnographic recording. The next day, they were given a surprise recognition memory task. Results showed that memory was better for emotional relative to neutral information. Critically, these findings were observed only in the stress condition. No emotional memory benefit was observed in the control condition. In stressed participants, REM theta power significantly predicted memory for emotional information, specifically for positive items. This relationship was observed only in high cortisol responders. For low responders and controls, there was no relationship between REM theta and memory of any valence. These findings provide evidence that elevated stress at encoding, and accompanying changes in neuromodulators such as cortisol, may interact with theta activity during REM sleep to promote selective consolidation of emotional information.

Affect enhances object-background associations: evidence from behaviour and mathematical modelling.

In recognition memory paradigms, emotional details are often recognised better than neutral ones, but at the cost of memory for peripheral details. We previously provided evidence that, when peripheral details must be recalled using central details as cues, peripheral details from emotional scenes are at least as likely to be recalled as those from neutral scenes. Here we replicated and explicated this result by implementing a mathematical modelling approach to disambiguate the influence of target type, scene emotionality, scene valence, and their interactions. After incidentally encoding scenes that included neutral backgrounds with a positive, negative, or neutral foreground objects, participants showed equal or better cued recall of components from emotional scenes compared to neutral scenes. There was no evidence of emotion-based impairment in cued recall in either of two experiments, including one in which we replicated the emotion-induced memory trade-off in recognition. Mathematical model fits indicated that the emotionality of the encoded scene was the primary driver of improved cued-recall performance. Thus, even when emotion impairs recognition of peripheral components of scenes, it can preserve the ability to recall which scene components were studied together.

Prior Emotional Context Modulates Early Event-Related Potentials to Neutral Retrieval Cues.

Memory retrieval is thought to involve the reactivation of encoding processes. Previous fMRI work has indicated that reactivation processes are modulated by the residual effects of the prior emotional encoding context; different spatial patterns emerge during retrieval of memories previously associated with negative compared with positive or neutral context. Other research suggests that event-related potential (ERP) indicators of memory retrieval processes, like the left parietal old/new effect, can also be modulated by emotional context, but the spatial distribution and temporal dynamics of these effects are unclear. In the current study, we examined "when" emotion affects recognition memory and whether that timing reflects processes that come before and may guide successful retrieval or postrecollection recovery of emotional episodic detail. While recording EEG, participants (n = 25) viewed neutral words paired with negative, positive, or neutral pictures during encoding, followed by a recognition test for the words. Analyses focused on ERPs during the recognition test. In line with prior ERP studies, we found an early positive-going parietally distributed effect starting around 200 msec after retrieval-cue onset. This effect emerged for words that had been encoded in an emotional compared with neutral context (no valence differences), before the general old/new effect. This emotion-dependent effect occurred in an early time window, suggesting that emotion-related reactivation is a precursor to successful recognition.

Memories Fade: The Relationship Between Memory Vividness and Remembered Visual Salience.

Past events, particularly emotional experiences, are often vividly recollected. However, it remains unclear how qualitative information, such as low-level visual salience, is reconstructed and how the precision and bias of this information relate to subjective memory vividness. Here, we tested whether remembered visual salience contributes to vivid recollection. In three experiments, participants studied emotionally negative and neutral images that varied in luminance and color saturation, and they reconstructed the visual salience of each image in a subsequent test. Results revealed, unexpectedly, that memories were recollected as less visually salient than they were encoded, demonstrating a novel memory-fading effect, whereas negative emotion increased subjective memory vividness and the precision with which visual features were encoded. Finally, memory vividness tracked both the precision and remembered salience (bias) of visual information. These findings provide evidence that low-level visual information fades in memory and contributes to the experience of vivid recollection.

The role of the amygdala in emotional experience during retrieval of personal memories.

Although the role of the amygdala in emotional memory retrieval has long been established, how such engagement varies depending on valence and retrieval context is less clearly understood. Participants retrieved personal memories associated with primarily positive, primarily negative, and mixed-valence images, pressing a button when successful. The button press divided trials into search and elaboration phases. Participants provided positivity and negativity ratings immediately following each trial, and then again in a post-retrieval survey. The relation between amygdala recruitment and emotionality exhibited a four-way interaction, with no other significant main effects or interactions. The interaction was driven by a temporal shift in the role of amygdala recruitment during retrieval of memories associated with mixed-valence images: Negativity ratings were supported more by search-related activity whereas positivity was more strongly associated with elaboration. Amygdala activity during retrieval relates to emotional experience in more complicated ways than previously understood. When participants were able to consider positive and negative aspects of the same event, amygdala recruitment during search and elaboration were associated with opposite behavioural effects. Such findings suggest that the amygdala may support distinct aspects of emotional experience for the same memory depending on when during retrieval it is recruited.