The influence of encoding strategy on associative memory consolidation across wake and sleep.

Sleep benefits memory consolidation. However, factors present at initial encoding may moderate this effect. Here, we examined the role that encoding strategy plays in subsequent memory consolidation during sleep. Eighty-nine participants encoded pairs of words using two different strategies. Each participant encoded half of the word pairs using an integrative visualization technique, where the two items were imagined in an integrated scene. The other half were encoded nonintegratively, with each word pair item visualized separately. Memory was tested before and after a period of nocturnal sleep (N = 47) or daytime wake (N = 42) via cued recall tests. Immediate memory performance was significantly better for word pairs encoded using the integrative strategy compared with the nonintegrative strategy (P < 0.001). When looking at the change in recall across the delay, there was significantly less forgetting of integrated word pairs across a night of sleep compared with a day spent awake (P < 0.001), with no significant difference in the nonintegrated pairs (P = 0.19). This finding was driven by more forgetting of integrated compared with not-integrated pairs across the wake delay (P < 0.001), whereas forgetting was equivalent across the sleep delay (P = 0.26). Together, these results show that the strategy engaged in during encoding impacts both the immediate retention of memories and their subsequent consolidation across sleep and wake intervals.

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.

Sleep spectral power correlates of prospective memory maintenance.

Prospective memory involves setting an intention to act that is maintained over time and executed when appropriate. Slow wave sleep (SWS) has been implicated in maintaining prospective memories, although which SWS oscillations most benefit this memory type remains unclear. Here, we investigated SWS spectral power correlates of prospective memory. Healthy young adult participants completed three ongoing tasks in the morning or evening. They were then given the prospective memory instruction to remember to press "Q" when viewing the words "horse" or "table" when repeating the ongoing task after a 12-h delay including overnight, polysomnographically recorded sleep or continued daytime wakefulness. Spectral power analysis was performed on recorded sleep EEG. Two additional groups were tested in the morning or evening only, serving as time-of-day controls. Participants who slept demonstrated superior prospective memory compared with those who remained awake, an effect not attributable to time-of-day of testing. Contrary to prior work, prospective memory was negatively associated with SWS. Furthermore, significant increases in spectral power in the delta-theta frequency range (1.56 Hz-6.84 Hz) during SWS was observed in participants who failed to execute the prospective memory instructions. Although sleep benefits prospective memory maintenance, this benefit may be compromised if SWS is enriched with delta-theta activity.

Insufficient chunk concatenation may underlie changes in sleep-dependent consolidation of motor sequence learning in older adults.

Sleep enhances motor sequence learning (MSL) in young adults by concatenating subsequences ("chunks") formed during skill acquisition. To examine whether this process is reduced in aging, we assessed performance changes on the MSL task following overnight sleep or daytime wake in healthy young and older adults. Young adult performance enhancement was correlated with nREM2 sleep, and facilitated by preferential improvement of slowest within-sequence transitions. This effect was markedly reduced in older adults, and accompanied by diminished sigma power density (12-15 Hz) during nREM2 sleep, suggesting that diminished chunk concatenation following sleep may underlie reduced consolidation of MSL in older adults.

The influence of sleep on fear extinction in trauma-related disorders.

In Posttraumatic Stress Disorder (PTSD), fear and anxiety become dysregulated following psychologically traumatic events. Regulation of fear and anxiety involves both high-level cognitive processes such as cognitive reattribution and low-level, partially automatic memory processes such as fear extinction, safety learning and habituation. These latter processes are believed to be deficient in PTSD. While insomnia and nightmares are characteristic symptoms of existing PTSD, abundant recent evidence suggests that sleep disruption prior to and acute sleep disturbance following traumatic events both can predispose an individual to develop PTSD. Sleep promotes consolidation in multiple memory systems and is believed to also do so for low-level emotion-regulatory memory processes. Consequently sleep disruption may contribute to the etiology of PTSD by interfering with consolidation in low-level emotion-regulatory memory systems. During the first weeks following a traumatic event, when in the course of everyday life resilient individuals begin to acquire and consolidate these low-level emotion-regulatory memories, those who will develop PTSD symptoms may fail to do so. This deficit may, in part, result from alterations of sleep that interfere with their consolidation, such as REM fragmentation, that have also been found to presage later PTSD symptoms. Here, sleep disruption in PTSD as well as fear extinction, safety learning and habituation and their known alterations in PTSD are first briefly reviewed. Then neural processes that occur during the early post-trauma period that might impede low-level emotion regulatory processes through alterations of sleep quality and physiology will be considered. Lastly, recent neuroimaging evidence from a fear conditioning and extinction paradigm in patient groups and their controls will be considered along with one possible neural process that may contribute to a vulnerability to PTSD following trauma.

The Impact of Sleep on Fear Extinction.

Sleep plays a crucial role in the consolidation of memories, including those for fear acquisition and extinction training. This chapter reviews findings from studies testing this relationship in laboratory, naturalistic, and clinical settings. While evidence is mixed, several studies in humans have linked fear and extinction recall/retention to both rapid eye-movement and slow wave sleep. Sleep appears to further aid in the processing of both simulated and actual trauma and improves psychotherapeutic treatment outcomes in those with anxiety and trauma- and stressor-related disorders. This chapter concludes with a discussion of the current challenges facing sleep and emotional memory research in addition to suggestions for improving future research.

Beta spectral power during sleep is associated with impaired recall of extinguished fear.

The failure to retain memory for extinguished fear plays a major role in the maintenance of posttraumatic stress disorder (PTSD), with successful extinction recall necessary for symptom reduction. Disturbed sleep, a hallmark symptom of PTSD, impairs fear extinction recall. However, our understanding of the electrophysiological mechanisms underpinning sleep's role in extinction retention remains underdetermined. We examined the relationship between the microarchitecture of sleep and extinction recall in healthy humans (n = 71, both male and females included) and a pilot study in individuals with PTSD (n = 12). Participants underwent a fear conditioning and extinction protocol over 2 days, with sleep recording occurring between conditioning and extinction. Twenty-four hours after extinction learning, participants underwent extinction recall. Power spectral density (PSD) was computed for pre- and post-extinction learning sleep. Increased beta-band PSD (~17-26 Hz) during pre-extinction learning sleep was associated with worse extinction recall in healthy participants (r = 0.41, p = .004). Beta PSD was highly stable across three nights of sleep (intraclass correlation coefficients > 0.92). Results suggest beta-band PSD is specifically implicated in difficulties recalling extinguished fear.

Representing the Good and Bad: fMRI signatures during the encoding of multisensory positive, negative, and neutral events.

Few studies have examined how multisensory emotional experiences are processed and encoded into memory. Here, we aimed to determine whether, at encoding, activity within functionally-defined visual- and auditory-processing brain regions discriminated the emotional category (i.e., positive, negative, or neutral) of the multisensory (audio-visual) events. Participants incidentally encoded positive, negative, and neutral multisensory stimuli during event-related functional magnetic resonance imaging (fMRI). Following a 3-h post-encoding delay, their memory for studied stimuli was tested, allowing us to identify emotion-category-specific subsequent-memory effects focusing on medial temporal lobe regions (i.e., amygdala, hippocampus) and visual- and auditory-processing regions. We used a combination of univariate and multivoxel pattern fMRI analyses (MVPA) to examine emotion-category-specificity in mean activity levels and neural patterning, respectively. Univariate analyses revealed many more visual regions that showed negative-category-specificity relative to positive-category-specificity, and auditory regions only showed negative-category-specificity. These results suggest that negative emotion is more closely tied to information contained within sensory regions, a conclusion that was supported by the MVPA analyses. Functional connectivity analyses further revealed that the visual amplification of category-selective processing is driven, in part, by mean signal from the amygdala. Interestingly, while stronger representations in visuo-auditory regions were related to subsequent-memory for neutral multisensory stimuli, they were related to subsequent-forgetting of positive and negative stimuli. Neural patterning in the hippocampus and amygdala were related to memory for negative multisensory stimuli. These results provide new evidence that negative emotional stimuli are processed with increased engagement of visuosensory regions, but that this sensory engagement-that generalizes across the entire emotion category-is not the type of sensory encoding that is most beneficial for later retrieval.

Changes in Sleep Regularity and Perceived Life Stress across the COVID-19 Pandemic: A Longitudinal Analysis of a Predominately Female United States Convenience Sample.

The Coronavirus Disease 2019 (COVID-19) pandemic had a profound impact on sleep and psychological well-being for individuals worldwide. This pre-registered investigation extends our prior study by tracking self-reported social jetlag (SJL), social sleep restriction (SSR), and perceived life stress from May 2020 through October 2021. Using web-based surveys, we collected self-reported sleep information with the Ultrashort Munich Chronotype Questionnaire at three additional timepoints (September 2020, February 2021 and October 2021). Further, we measured perceived life stress with the Perceived Stress Scale at two additional timepoints (February 2021 and October 2021). In a subsample of 181, predominantly female (87%), United States adults aged 19-89 years, we expanded our prior findings by showing that the precipitous drop in SJL during the pandemic first wave (May 2020), compared to pre-pandemic (February, 2020), rapidly rose with loosening social restrictions (September 2020), though never returned to pre-pandemic levels. This effect was greatest in young adults, but not associated with self-reported chronotype. Further, perceived life stress decreased across the pandemic, but was unrelated to SJL or SSR. These findings suggest that sleep schedules were sensitive to pandemic-related changes in social restrictions, especially in younger participants. We posit several possible mechanisms supporting these findings.

How the 2020 US Presidential election impacted sleep and its relationship to public mood and alcohol consumption.

OBJECTIVES: Major sociopolitical events can influence the general public's affective state and other affect-related processes, such as sleep. Here, we investigated the extent that the 2020 US presidential election impacted sleep, public mood, and alcohol consumption. We also explored the relationship between affect and sleep changes during the peak period of election stress. PARTICIPANTS: US-residing (n = 437) and non-US-residing (n = 106) participants were recruited online for participation in the study. METHODS: A non-representative, convenience sample responded to daily assessments of their affect, sleep, and alcohol consumption during a baseline period (October 1-13, 2020) and in the days surrounding the 2020 US Election (October 30-November 12, 2020). RESULTS: Analyses determined changes within and between US and non-US participants. Election Day evoked significantly reduced sleep amount and efficiency, coupled with heightened stress, negative affect, and increased alcohol use. While US participants were significantly more impacted in a number of domains, non-US participants also reported reduced sleep and greater stress compared to baseline. Across participants, disrupted sleep on Election Night correlated with changes in emotional well-being and alcohol consumption on Election Day. CONCLUSION: These results suggest that major sociopolitical events can have global impacts on sleep that may interact with significant fluctuations in public mood and well-being. Further, while the largest impact is on the local population, these results suggest that the effects can extend beyond borders. These findings highlight the potential impact of future sociopolitical events on public well-being.

Sleep Power Spectral Density and Spindles in PTSD and Their Relationship to Symptom Severity.

Sleep disturbances are common in post-traumatic stress disorder (PTSD), although which sleep microarchitectural characteristics reliably classify those with and without PTSD remains equivocal. Here, we investigated sleep microarchitectural differences (i.e., spectral power, spindle activity) in trauma-exposed individuals that met (n = 45) or did not meet (n = 52) criteria for PTSD and how these differences relate to post-traumatic and related psychopathological symptoms. Using ecologically-relevant home sleep polysomnography recordings, we show that individuals with PTSD exhibit decreased beta spectral power during NREM sleep and increased fast sleep spindle peak frequencies. Contrary to prior reports, spectral power in the beta frequency range (20.31-29.88 Hz) was associated with reduced PTSD symptoms, reduced depression, anxiety and stress and greater subjective ability to regulate emotions. Increased fast frequency spindle activity was not associated with individual differences in psychopathology. Our findings may suggest an adaptive role for beta power during sleep in individuals exposed to a trauma, potentially conferring resilience. Further, we add to a growing body of evidence that spindle activity may be an important biomarker for studying PTSD pathophysiology.

1H MRS Measurement of Cortical GABA and Glutamate in Primary Insomnia and Major Depressive Disorder: Relationship to Sleep Quality and Depression Severity.

BACKGROUND: Both Major Depressive Disorder (MDD) and Primary Insomnia (PI) have been linked to deficiencies in cortical γ-aminobutyric acid (GABA) and glutamate (Glu) thus suggesting a shared neurobiological link between these two conditions. The extent to which comorbid insomnia contributes to GABAergic or glutamatergic deficiencies in MDD remains unclear. METHODS: We used single-voxel proton magnetic resonance spectroscopy (1H MRS) at 4 Tesla to examine GABA+ and Glu relative to creatine (Cr) in the dorsal anterior cingulate cortex (dACC) and in the parieto-occipital cortex (POC) of 51 non-medicated adults with MDD, 24 adults with Primary Insomnia (PI), and 25 age- and sex-matched good sleeper controls (HC). Measures of depression severity and subjective and objective sleep quality were compared with 1H MRS metabolite measures. RESULTS: MDD subjects exhibited a 15% decrease in Glu/Cr in the dACC compared to HC. Within the MDD group, there was a trend inverse correlation between dACC Glu/Cr and anhedonia ratings. We observed no significant association between measures of sleep quality with dACC Glu/Cr in those with MDD. LIMITATIONS: The protocol and data interpretation would have been enhanced by the recruitment of MDD subjects with a broader range of affect severity and a more comprehensive assessment of clinical features. CONCLUSIONS: These findings support the role of cortical glutamatergic mechanisms in the pathophysiology of MDD. Insomnia severity did not further contribute to the relative deficiency of glutamatergic measures in MDD.

Comparing the Impact of COVID-19-Related Social Distancing on Mood and Psychiatric Indicators in Sexual and Gender Minority (SGM) and Non-SGM Individuals.

Empirical evidence demonstrates mental health disparities between sexual and gender minority individuals (SGM) compared with cisgender heterosexual individuals. SGM individuals report elevated rates of emotional distress, symptoms related to mood and anxiety disorders, self-harm, and suicidal ideation and behavior. Social support is inversely related to psychiatric symptoms, regardless of SGM status. The COVID-19 pandemic-with its associated limited social interactions-represents an unprecedented period of acute distress with potential reductions in accessibility of social support, which might be of particular concern for SGM individuals' mental well-being. In the present study, we explored the extent to which potential changes in mental health outcomes (depressive symptoms, worry, perceived stress, positive and negative affect) throughout the duration of the pandemic were related to differences in perceptions of social support and engagement in virtual social activity, as a function of SGM status. Utilizing a large sample of US adults (N = 1,014; 18% reported SGM status), we assessed psychiatric symptoms, perceptions of social isolation, and amount of time spent socializing virtually at 3 time windows during the pandemic (between March 21 and May 21). Although SGM individuals reported greater levels of depression compared with non-SGM individuals at all 3 time points, there was no interaction between time and SGM status. Across all participants, mental health outcomes improved across time. Perceived social isolation was associated with poorer mental health outcomes. Further, time spent engaging in virtual socialization was associated with reduced depression, but only for those in self-reported quarantine. We discuss these results in terms of the nature of our sample and its impact on the generalizability of these findings to other SGM samples as well as directions for future research aimed at understanding potential health disparities in the face of the COVID-19 pandemic.

Fear extinction memory is negatively associated with REM sleep in insomnia disorder.

STUDY OBJECTIVES: Formation and maintenance of fear-extinction memories are disrupted in post-traumatic stress disorder (PTSD) and anxiety disorders. Sleep contributes to emotional memory consolidation and emotion regulation. Insomnia disorder (ID) is characterized by persistent sleep disturbance as well as rapid eye movement (REM) sleep abnormalities and often precedes or develops in parallel with PTSD and anxiety disorders. Here, we explore the impact of chronic poor sleep and sleep immediately following fear conditioning and extinction learning on preservation of extinction memories. METHODS: Twenty-four ID age- and sex-matched to 24 healthy, good sleeper controls (GS) completed up to 2 weeks of habitual sleep monitoring with daily sleep-wake diaries and actigraphy, and then participated in a two-session fear conditioning, extinction learning and extinction recall procedure. Fear Conditioning and Extinction Learning occurred during session 1, followed by Extinction Recall approximately 24 hours later. Skin-conductance responses (SCR) and shock expectancies were recorded throughout all experimental phases to evaluate associative learning and memory. Overnight sleep between sessions 1 and 2 was recorded using ambulatory polysomnography. RESULTS: ID showed greater physiological reactivity during Fear Conditioning. REM sleep physiology was associated with poorer extinction memory in ID but better extinction memory in GS. CONCLUSION: REM sleep physiology may differentially support emotional memory retention and expression in ID and GS. In the former, REM may enhance retention of fear memories, while in the later, REM may enhance the expression of extinction memories.

Delayed fear extinction in individuals with insomnia disorder.

Study Objectives: Insomnia increases the risk for anxiety disorders that are also associated with fear-extinction deficits. We compared activation of fear and extinction networks between insomnia disorder (ID) without comorbidity and good sleepers (GS). Methods: Twenty-three ID participants age- and sex-matched to 23 GS participants completed 14 days of actigraphy and diaries, three nights of ambulatory polysomnography and a 2-day fear conditioning and extinction paradigm. Fear conditioning and extinction learning occurred on the first day, followed 24 hours later by extinction recall. Blood-oxygen-level-dependent functional magnetic resonance imaging (fMRI) signal and skin conductance responses (SCR) were recorded. Nineteen participants per group produced usable fMRI data. Beta weights from areas where activation differed between groups were regressed against sleep and psychophysiological measures. SCR was compared between groups at various stages of the paradigm. Results: During fear conditioning, both ID (N = 19) and GS (N = 19) activated fear-related structures. Across extinction learning, ID (N = 19) demonstrated little change, whereas GS (N = 16) activated both fear and extinction-related areas, including the hippocampus, insula, dorsal anterior cingulate (dACC), and ventromedial prefrontal (vmPFC) cortices. During extinction recall, while GS (N = 17) demonstrated limited activation, ID (N = 16) activated regions similar to those previously activated in GS (vmPFC, dACC, insula). Sleep quality was predictive of activations seen at various stages of the paradigm. SCR data suggested ID were more physiologically reactive than GS. Conclusions: Across extinction learning, GS but not ID activated both fear and extinction-related networks. At extinction recall, ID engaged similar regions whereas GS no longer did so. Individuals with ID may show a delayed acquisition of fear extinction memories.

Effects of post-exposure naps on exposure therapy for social anxiety.

Exposure therapy for social anxiety disorder (SAD) utilizes fear extinction, a memory process enhanced by sleep. We investigated whether naps following exposure sessions might improve symptoms and biomarkers in response to social stress in adults undergoing 5-week exposure-based group SAD therapy. Thirty-two participants aged 18-39 (18 females) with SAD were randomized. Before and after treatment, participants completed the Liebowitz Social Anxiety Scale (LSAS) and underwent a Trier Social Stress Test with psychophysiological monitoring (mpTSST) that included skin conductance (SCL), electromyographic (EMG) and electrocardiographic recording, and an auditory startle procedure while anticipating the social stressor. At sessions 3 and 4, exposure was followed by either a 120-min polysomnographically monitored sleep opportunity (Nap, N = 17) or wakefulness (Wake, N = 15). Primary hypotheses about SAD symptom change (LSAS) and EMG blink-startle response failed to differ with naps, despite significant symptom improvement (LSAS) with therapy. Some secondary biomarkers, however, provided preliminary support for enhanced extinction learning with naps, with trend-level Time (pre-, post-treatment) × Arm interactions and significant reduction from pre- to post treatment in the Nap arm alone for mpTSST SCL and salivary cortisol rise. Because of the small sample size and limited sleep duration, additional well-powered studies with more robust sleep interventions are indicated.

Resting state functional connectivity in primary insomnia, generalized anxiety disorder and controls.

Sleep abnormalities are extremely common in anxiety disorders and may contribute to their development and persistence. Their shared pathophysiological mechanisms could thus serve as biomarkers or targets for novel therapeutics. Individuals with Primary Insomnia were age- and sex-matched to controls and to persons with Generalized Anxiety Disorder. All underwent fMRI resting-state scans at 3-T. In Primary Insomnia and controls, sleep was recorded for 2 weeks using diaries and actigraphy. All participants completed state-anxiety and neuroticism inventories. Whole-brain connectivity of 6 fear- and extinction-related seeds were compared between the 3 groups using ANOVA. The only significant between-group main effect was seen for connectivity between the left amygdala seed and a bilateral cluster in the rostral anterior cingulate cortex. The latter is believed to exert top-down control over amygdala activity and their interaction may thus constitute an emotion regulatory circuit. This connectivity was significantly greatest in controls while Primary Insomnia was intermediate between that of controls and Generalized Anxiety Disorder. Across Primary Insomnia and control subjects, mean connectivity decreased with poorer sleep. Across all 3 groups, connectivity decreased with greater neuroticism and pre-scan anxiety. Decreased top-down control of the amygdala may increase risk of developing an anxiety disorder with preexisting Primary Insomnia.