Prioritized memory consolidation over sleep: Do psychological and physiological markers at encoding set the stage?

Thesis advisor: Elizabeth A. KensingerEmotion enhances memory longevity and vividness. Perceiving an experience as emotional, as well as the autonomic and functional brain responses involved in initially encoding an emotional experience, have been theorized to “tag” these memories. Tagged memories may then be prioritized for consolidation during sleep. However, direct evidence supporting this theory is sparse. The aim of the present study was to determine which encoding-related indicators of memory tagging interact with post-encoding sleep oscillations to promote emotional memory retention and vividness. To test this, participants incidentally encoded positive, neutral and negative multisensory stimuli during 3T fMRI scanning with concurrent heart rate monitoring. Participants provided emotional intensity ratings after each stimulus presentation. Following a 120-min post-encoding nap opportunity recorded with polysomnography, participants completed a surprise memory test. Memory for emotional and neutral stimuli was equivalent, though emotional stimuli tended to be remembered more vividly. Perceived emotional intensity, but not heart rate deceleration (HRD) magnitude or functional brain activity, was diagnostic of later successful retrieval of emotional, but not neutral stimuli. Higher REM sleep theta power during the nap was associated with a greater emotional intensity (EI) subsequent memory effect (i.e., higher EI for later remembered compared to forgotten stimuli) for positive stimuli, which were also remembered more vividly. Higher NREM spindle density was associated with a greater EI subsequent memory effect for neutral stimuli and lesser EI subsequent memory effect for negative stimuli. Lastly, higher numbers of NREM spindle-slow oscillation coupling events predicted a negative relationship between perceived emotional intensity at encoding and memory vividness for negative stimuli. Taken together, the present findings suggest that subjective, rather than objective, encoding-related arousal responses acted as emotion “tags”. How subjective arousal impacted later memory varied as a function of the memory’s emotion category and REM and NREM-specific oscillations. Future work is needed to clarify the underlying mechanisms for these observed effects.Thesis (PhD) — Boston College, 2022.Submitted to: Boston College. Graduate School of Arts and Sciences.Discipline: Psychology

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

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

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 post-traumatic 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 remain 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 two 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 (~17-26Hz) during pre-extinction learning sleep was associated with worse extinction recall in healthy participants (r=.41, p=.004). Beta PSD was highly stable across three nights of sleep (intraclass correlations (ICC)>0.92). Results suggest beta band PSD is elevated in PTSD, and is specifically implicated in difficulties recalling extinguished fear

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

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