Does sleep promote adaptation to acute stress: An experimental study.

Objectives: Evidence of the impact of chronic stress on sleep is abundant, yet experimental sleep studies with a focus on acute stress are scarce and the results are mixed. Our study aimed to fill this gap by experimentally investigating the effects of pre-sleep social stress on sleep dynamics during the subsequent night, as measured with polysomnography (PSG). Methods: Thirty-four healthy individuals (65% females, Mage = 25.76 years SD = 3.35) underwent a stress-inducing (SC) or neutral control condition (CC) in virtual reality (VR). We used overnight EEG measurements to analyze the basic sleep parameters and power spectral density (PSD) across the sleep cycles, and measured heart rate and its variability (HRV), skin electrodermal activity (EDA), and salivary cortisol to capture physiological arousal during the VR task and the pre-sleep period. Results: Following acute stress (SC), the amount of slow-wave sleep (SWS) was higher and N2 sleep lower relative to CC, specifically in the first sleep cycle. In SC, PSD was elevated in the beta-low (16-24 Hz) and beta-high (25-35 Hz) frequency ranges during both stages N2 and SWS over the entire night. Conclusions: Sleep promoted adaptation to acute social stress by a longer duration of SWS in the subsequent sleep period, especially in early sleep. A similar homeostatic effect towards restorative sleep is well-evidenced in animal model stress studies but has not been previously reported in experimental human studies. Whether the high-frequency PSD activity during stages N2 and SWS also serves in the resolution of transient stress, remains open.

Inter-brain synchronization occurs without physical co-presence during cooperative online gaming.

Inter-brain synchronization during social interaction has been linked with several positive phenomena, including closeness, cooperation, prosociality, and team performance. However, the temporal dynamics of inter-brain synchronization during collaboration are not yet fully understood. Furthermore, with collaboration increasingly happening online, the dependence of inter-brain phase synchronization of oscillatory activity on physical presence is an important but understudied question. In this study, physically isolated participants performed a collaborative coordination task in the form of a cooperative multiplayer game. We measured EEG from 42 subjects working together as pairs in the task. During the measurement, the only interaction between the participants happened through on-screen movement of a racing car, controlled by button presses of both participants working with distinct roles, either controlling the speed or the direction of the car. Pairs working together in the task were found to have elevated neural coupling in the alpha, beta, and gamma frequency bands, compared to performance matched false pairs. Higher gamma synchrony was associated with better momentary performance within dyads and higher alpha synchrony was associated with better mean performance across dyads. These results are in line with previous findings of increased inter-brain synchrony during interaction, and show that phase synchronization of oscillatory activity occurs during online real-time joint coordination without any physical co-presence or video and audio connection. Synchrony decreased during a playing session, but was found to be higher during the second session compared to the first. The novel paradigm, developed for the measurement of real-time collaborative performance, demonstrates that changes in inter-brain EEG phase synchrony can be observed continuously during interaction.

Benefits of choir singing on complex auditory encoding in the aging brain: An ERP study.

Aging is accompanied by difficulties in auditory information processing, especially in more complex sound environments. Choir singing requires efficient processing of multiple sound features and could, therefore, mitigate the detrimental effects of aging on complex auditory encoding. We recorded auditory event-related potentials during passive listening of sounds in healthy older adult (≥ 60 years) choir singers and nonsinger controls. We conducted a complex oddball condition involving encoding of abstract regularities in combinations of pitch and location features, as well as in two simple oddball conditions, in which only either the pitch or spatial location of the sounds was varied. We analyzed change-related mismatch negativity (MMN) and obligatory P1 and N1 responses in each condition. In the complex condition, the choir singers showed a larger MMN than the controls, which also correlated with better performance in a verbal fluency test. In the simple pitch and location conditions, the choir singers had smaller N1 responses compared to the control subjects, whereas the MMN responses did not differ between groups. These results suggest that regular choir singing is associated both with more enhanced encoding of complex auditory regularities and more effective adaptation to simple sound features.

Brain oscillation recordings of the audience in a live concert-like setting.

There are only a few previous EEG studies that were conducted while the audience is listening to live music. However, in laboratory settings using music recordings, EEG frequency bands theta and alpha are connected to music improvisation and creativity. Here, we measured EEG of the audience in a concert-like setting outside the laboratory and compared the theta and alpha power evoked by partly improvised versus regularly performed familiar versus unfamiliar live classical music. To this end, partly improvised and regular versions of pieces by Bach (familiar) and Melartin (unfamiliar) were performed live by a chamber trio. EEG data from left and right frontal and central regions of interest were analysed to define theta and alpha power during each performance. After the performances, the participants rated how improvised and attractive each of the performances were. They also gave their affective ratings before and after each performance. We found that theta power was enhanced during the familiar improvised Bach piece and the unfamiliar improvised Melartin piece when compared with the performance of the same piece performed in a regular manner. Alpha power was not modulated by manner of performance or by familiarity of the piece. Listeners rated partly improvised performances of a familiar Bach and unfamiliar Melartin piece as more improvisatory and innovative than the regular performances. They also indicated more joy and less sadness after listening to the unfamiliar improvised piece of Melartin and less fearful and more enthusiastic after listening to the regular version of Melartin than before listening. Thus, according to our results, it is possible to study listeners' brain functions with EEG during live music performances outside the laboratory, with theta activity reflecting the presence of improvisation in the performances.

Self-Conscious Affect Is Modulated by Rapid Eye Movement Sleep but Not by Targeted Memory Reactivation-A Pilot Study.

The neurophysiological properties of rapid eye movement sleep (REMS) are believed to tune down stressor-related emotional responses. While prior experimental findings are controversial, evidence suggests that affective habituation is hindered if REMS is fragmented. To elucidate the topic, we evoked self-conscious negative affect in the participants (N = 32) by exposing them to their own out-of-tune singing in the evening. Affective response to the stressor was measured with skin conductance response and subjectively reported embarrassment. To address possible inter-individual variance toward the stressor, we measured the shame-proneness of participants with an established questionnaire. The stressor was paired with a sound cue to pilot a targeted memory reactivation (TMR) protocol during the subsequent night's sleep. The sample was divided into three conditions: control (no TMR), TMR during slow-wave sleep, and TMR during REMS. We found that pre- to post-sleep change in affective response was not influenced by TMR. However, REMS percentage was associated negatively with overnight skin conductance response habituation, especially in those individuals whose REMS was fragmented. Moreover, shame-proneness interacted with REM fragmentation such that the higher the shame-proneness, the more the affective habituation was dependent on non-fragmented REMS. In summary, the potential of REMS in affective processing may depend on the quality of REMS as well as on individual vulnerability toward the stressor type.

The Paradox of Fiction Revisited-Improvised Fictional and Real-Life Social Rejections Evoke Associated and Relatively Similar Psychophysiological Responses.

Theatre-based practices, such as improvisation, are frequently applied to simulate everyday social interactions. Although the improvisational context is acknowledged as fictional, realistic emotions may emerge, a phenomenon labelled the 'paradox of fiction'. This study investigated how manipulating the context (real-life versus fictional) modulates psychophysiological reactivity to social rejection during dyadic interactions. We measured psychophysiological responses elicited during real-life (interview) and fictional (improvisation exercises) social rejections. We analysed the heart rate (HR), skin conductance, facial muscle activity, and electrocortical activity (electroencephalographic (EEG) alpha asymmetry) of student teachers (N = 39) during various social rejections (devaluing, interrupting, nonverbal rejection). All social rejections evoked negative EEG alpha asymmetry, a measure reflecting behavioural withdrawal motivation. Psychophysiological responses during real-life and fictional rejections correlated, and rejection type modified the responses. When comparing responses across all rejection types, facial muscle activity and EEG alpha asymmetry did not differ between real-life and fictional rejections, whereas HR decelerated and skin conductance increased during fictional rejections. These findings demonstrate that regardless of cognitive awareness of fictionality, relatively subtle social rejections elicited psychophysiological reactivity indicating emotional arousal and negative valence. These findings provide novel, biological evidence for the application of theatre-based improvisation to studying experientially everyday social encounters.

Psychological and Physiological Signatures of Music Listening in Different Listening Environments-An Exploratory Study.

We compared music emotion ratings and their physiological correlates when the participants listened to music at home and in the laboratory. We hypothesized that music emotions are stronger in a familiar environment, that is, at home. Participants listened to their self-selected favorite and neutral music excerpts at home and in the laboratory for 10 min in each environment. They completed the questionnaires about their emotional states and gave saliva samples for the analyses of the stress hormone cortisol. We found that in the context of music listening, the participants' emotion ratings differed between home and the laboratory. Furthermore, the cortisol levels were generally lower at home than in the laboratory and decreased after music listening at home and in the laboratory. However, the modulatory effects of music listening on cortisol levels did not differ between the home and the laboratory. Our exploratory multimethodological data offer novel insight about the psychological and physiological consequences of music listening. These data reveal the sensitivity of the current research methods to investigate human emotions in various contexts without excluding the use of laboratory environment in investigating them.

No evidence for theta power as a marker of hypnotic state in highly hypnotizable subjects.

EEG spectral-power density was analyzed in a group of nine highly hypnotizable subjects via ten frontal, central, parietal, and occipital electrodes under four conditions: 1) wake state, 2) neutral hypnosis, 3) hypnotic suggestion for altering perception of tones, and 4) post-hypnosis. Results indicate no theta-power changes between conditions, challenging previous findings that increased theta power is a marker of hypnosis. A decrease in gamma power under hypnotic suggestion and an almost significant decrease under neutral hypnosis were observed, compared to post-hypnosis. Anteroposterior power distribution remained stable over all conditions. The results are discussed and compared to earlier studies, which report heterogenous findings.

Presleep physiological stress is associated with a higher cortical arousal in sleep and more consolidated REM sleep.

How sleep regulates physiological stress in healthy individuals is not well understood. We explored the associations between naturally occurring pre-sleep physiological arousal and EEG power spectral density together with rapid eye movement sleep (REMS) continuity. One hundred and fifty-four individuals (mean age 16.9, SD 0.1 years) collected five samples of saliva between the evening (mean time 18:20) and bedtime (mean 23:00) by using swabs, and underwent an overnight in-home polysomnography. We calculated spectral density for REMS and non-rapid eye movement sleep (non-REMS), and the number and duration of REMS arousals (<15 s) during sleep. An observational design allowed for measurement of natural variation in physiological and sleep arousal. Increasing cortisol levels toward bedtime were associated with higher EEG power spectral density at all frequency ranges in frontal locations, the highest association being for the beta1 frequency band. In central locations, the associations were pronounced for beta1 and beta2 bands. Higher overall cortisol levels in the evening were associated with less fragmented REMS. Presleep arousal was not associated with sleep staging. Physiological arousal toward bedtime was associated with EEG power spectral density values during sleep specifically at high EEG frequencies. This may represent a compensatory mechanism that serves as an adaptation to stress, since the REMS was more continuous along a higher physiological arousal level in the evening. Although causality cannot be inferred, a design with nonmanipulated physiological stress followed by naturally timed sleep at home provides new insights into stress regulation homeostasis.

The Effects of Presleep Slow Breathing and Music Listening on Polysomnographic Sleep Measures - a pilot trial.

Knowledge on efficient ways to reduce presleep arousal and, therefore, improve sleep, is scanty. We explored the effects of presleep slow breathing and music listening conditions on sleep quality and EEG power spectral density in young adults in a randomized, controlled trial with a crossover design. Participants' (N = 20, 50% females) sleep was measured on two consecutive nights with polysomnography (40 nights), the other night serving as the control condition. The intervention condition was either a 30-minute slow breathing exercise or music listening (music by Max Richter: Sleep). The intervention and control conditions were placed in a random order. We measured heart rate variability prior to, during and after the intervention condition, and found that both interventions increased immediate heart rate variability. Music listening resulted in decreased N2 sleep, increased frontal beta1 power spectral density, and a trend towards increased N3 sleep was detected. In the slow breathing condition higher central delta power during N3 was observed. While some indices pointed to improved sleep quality in both intervention groups, neither condition had robust effects on sleep quality. These explorative findings warrant further replication in different populations.

Polygenic impact of morningness on the overnight dynamics of sleep spindle amplitude.

Sleep spindles are thalamocortical oscillations that contribute to sleep maintenance and sleep-related brain plasticity. The current study is an explorative study of the circadian dynamics of sleep spindles in relation to a polygenic score (PGS) for circadian preference towards morningness. The participants represent the 17-year follow-up of a birth cohort having both genome-wide data and an ambulatory sleep electroencephalography measurement available ( N = 154, Mean age = 16.9, SD = 0.1 years, 57% girls). Based on a recent genome-wide association study, we calculated a PGS for circadian preference towards morningness across the whole genome, including 354 single-nucleotide polymorphisms. Stage 2 slow (9-12.5 Hz, N = 186 739) and fast (12.5-16 Hz, N = 135 504) sleep spindles were detected using an automated algorithm with individual time tags and amplitudes for each spindle. There was a significant interaction of PGS for morningness and timing of sleep spindles across the night. These growth curve models showed a curvilinear trajectory of spindle amplitudes: those with a higher PGS for morningness showed higher slow spindle amplitudes in frontal derivations, and a faster dissipation of spindle amplitude in central derivations. Overall, the findings provide new evidence on how individual sleep spindle trajectories are influenced by genetic factors associated with circadian type. The finding may lead to new hypotheses on the associations previously observed between circadian types, psychiatric problems and spindle activity.

BDNF Val66Met polymorphism moderates the association between sleep spindles and overnight visual recognition.

A common single nucleotide polymorphism (SNP) of the brain-derived neurotrophic factor (BDNF) gene, Val66Met, has been reported to impair BDNF secretion and memory function. However, few studies have investigated the interaction of BDNF genotype and sleep characteristics, such as sleep spindles, that promote long-term potentiation during sleep. In this study we compared overnight visual memory between the carriers of BDNF Met and non-carriers (Val homozygotes), and examined how sleep spindle density associated with memory performance. The sample constituted of 151 adolescents (mean age 16.9 years; 69% Val homozygotes, 31% Met carriers). The learning task contained high and low arousal pictures from Interactive Affective Picture System. The learning task and all-night polysomnography were conducted at the homes of the adolescents. Slow (10-13 Hz) and fast (13-16 Hz) spindles were detected with automated algorithm. Neither post-sleep recognition accuracy nor spindle density differed between Val homozygotes and Met carriers. While frontal slow and fast spindle densities associated with better recognition accuracy in the entire sample, examining the allelic groups separately indicated paralleling associations in Val homozygotes only. Interaction analyses revealed a significant genotype-moderated difference in the associations between frontal fast sleep spindles and high arousal pictures. In sum, sleep spindles promote or indicate visual learning in Val homozygote adolescents but not in Met carriers. The result suggests that the role of sleep spindles in visual recognition memory is not equal across individuals but moderated by a common gene variant.

Autistic Traits Are Associated With Decreased Activity of Fast Sleep Spindles During Adolescence.

STUDY OBJECTIVES: Autistic traits present a continuum from mild symptoms to severe disorder and have been associated with a high prevalence of sleep problems. Sleep spindles have a key function in sleep maintenance and in brain plasticity. Previous studies have found decreased spindle activity in clinical autism. Here we examine the associations between the entire range of autistic traits and sleep spindle activity in a nonclinical community cohort of adolescents. METHODS: Our cohort is based on 172 adolescents born in 1998 (58.7% girls, mean age = 16.9 years, standard deviation = 0.1), who filled in the adult autism-spectrum quotient (AQ), consisting of total score, and social interaction and attention to details subscales. Participants underwent an ambulatory overnight sleep electroencephalography. Sleep spindles (amplitude, duration, density, and intensity) were automatically detected from stage N2 sleep, and divided to slow and fast spindles. RESULTS: Higher AQ total sum and social interaction sum associated with lower fast spindle amplitude and intensity (P < .04). No associations were observed for attention to details. CONCLUSIONS: Our findings indicate that a higher level of autistic traits in the nonclinical range among generally healthy adolescents associate with similar alterations in sleep spindle activity as observed in many neuropsychiatric conditions, indicating lower sleep-related brain plasticity. This indicates that sleep microstructures form a continuum that follows self-reported symptoms of autism.

Schizotypal traits are associated with sleep spindles and rapid eye movement in adolescence.

Research suggests an association between schizophrenia and a decrease in sleep spindle activity, as well as a change in sleep architecture. It is unknown how the continuum of psychotic symptoms relates to different features in the sleep electroencephalogram. We set out to examine how sleep architecture and stage 2 spindle activity are associated with schizotypy in a healthy adolescent population. The participants in our study (n = 176, 61% girls) came from a community-based cohort. Schizotypal traits were evaluated using the Schizotypal Personality Scale (STA) in early adolescence (mean age 12.3 years, SD = 0.5) and the participants underwent ambulatory overnight polysomnography at mean age 16.9 years (SD = 0.1). Sleep was scored in 30-s epochs into stages 1, 2, 3 and rapid eye movement (REM) sleep. Stage 2 spindles were detected using an automated algorithm. Spindle analyses from central and frontal derivations included spindle duration and density for slow (10-13 Hz) and fast (13-16 Hz) ranges. Covariates included sex and age. Those with the highest STA scores had a higher percentage of REM (B = 2.07 [95% CI, 0.17, 4.0]; p = .03) than those with the lowest scores. Those with the highest scores had shorter spindle duration, as derived from the frontal regions, and a slower oscillation range (B = -0.04 [95% CI, -0.07, -0.01]; p = .023) than those with the lowest scores. We conclude that high levels of schizotypy characteristics measured in early adolescence may be associated with distinguished features of sleep architecture, namely with spindle morphology and a higher proportion of REM sleep.

Genetic risk factors for schizophrenia associate with sleep spindle activity in healthy adolescents.

Schizophrenia has been associated with disturbed sleep, even before the onset of the disorder, and also in non-schizophrenic first-order relatives. This may point to an underlying genetic influence. Here we examine whether weighted polygenic risk scores (PRS) for schizophrenia are associated with sleep spindle activity in healthy adolescents. Our sample comes from a community-based cohort of 157 non-schizophrenic adolescents (57% girls) having both genetic data and an overnight sleep EEG measurement available. Based on a recent genome-wide association study, we calculated PRS for schizophrenia across the whole genome. We also calculated PRS for the CACNA1l gene region, which has been associated with both schizophrenia and sleep spindle formation. We performed an overnight sleep EEG at the homes of the participants. Stage two sleep spindles were detected using an automated algorithm. Sleep spindle amplitude, duration, intensity and density were measured separately for central and frontal derivations and for fast (13-16 Hz) and slow (10-13 Hz) spindles. PRS for schizophrenia was associated with higher fast spindle amplitude (p = 0.04), density (p = 0.006) and intensity (p = 0.04) at the central derivation, and PRS in the CACNA1l region associated with higher slow spindle amplitude (p = 0.01), duration (p = 0.03) and intensity (p = 0.002) at the central derivation. A positive association between genetic variants for schizophrenia and sleep spindle activity among healthy adolescents supports a view that sleep spindles and schizophrenia share similar genetic pathways. This study suggests that altered sleep spindle activity might serve as an endophenotype of schizophrenia.

Higher sleep spindle activity is associated with fewer false memories in adolescent girls.

BACKGROUND: Sleep facilitates the extraction of semantic regularities amongst newly encoded memories, which may also lead to increased false memories. We investigated sleep stage proportions and sleep spindles in the recollection of adolescents' false memories, and their potential sex-specific differences. METHODS: 196 adolescents (mean age 16.9 y; SD = 0.1, 61% girls) underwent the Deese, Roediger & McDermott (DRM) false memory procedure and overnight polysomnography, with free recall the following morning. Sleep was scored manually into stages 1, 2, 3 and REM. Stage 2 sleep spindle frequency, density, and peak amplitude were used as measures of spindle activity for slow (10-13 Hz) and fast (13-16 Hz) ranges. RESULTS: In girls, a lower number of critical lures was associated with higher spindle frequency (p ≤ 0.01), density (p ≤ 0.01), and amplitude (p = 0.03). Additionally, girls' longer sleep duration was associated with more intrusion words (p = 0.03), but not with critical lures. These associations survived adjustment for age, pubertal status, and intelligence. No significant results emerged in boys. CONCLUSIONS: In adolescent girls, higher spindle activity was associated with fewer critical lures being falsely recalled in the DRM paradigm. Unlike studies using adult participants, we did not observe any association between slow-wave sleep and false memory recollection.

ADHD symptoms are associated with decreased activity of fast sleep spindles and poorer procedural overnight learning during adolescence.

ADHD and its subclinical symptoms have been associated with both disturbed sleep and weakened overnight memory consolidation. As sleep spindle activity during NREM sleep plays a key role in both sleep maintenance and memory consolidation, we examined the association between subclinical ADHD symptoms and sleep spindle activity. Furthermore, we hypothesized that sleep spindle activity mediates the effect of ADHD symptoms on overnight learning outcome in a procedural memory task. We studied these questions in a community-based cohort of 170 adolescents (58% girls, mean age = 16.9, SD = 0.1 years), who filled in the Adult ADHD Self-Report Scale (ASRS-v1.1), and underwent an overnight sleep EEG coupled with a mirror tracing task before and after sleep. Elevated ADHD symptoms were associated with weaker fast sleep spindle activity, and poorer overnight learning in the procedural memory test. However, sleep spindles, contrary to the hypothesis, did not mediate the association between ADHD symptoms and overnight learning. Our results showed that a higher level of ADHD symptoms in adolescence is associated with similar alterations in sleep spindle activity as observed in many neuropsychiatric conditions and might contribute to altered synaptic connectivity and sleep fragmentation observed in ADHD.

Publisher Correction: Circadian preference towards morningness is associated with lower slow sleep spindle amplitude and intensity in adolescents.

A correction to this article has been published and is linked from the HTML version of this paper. The error has been fixed in the paper.

Circadian preference towards morningness is associated with lower slow sleep spindle amplitude and intensity in adolescents.

Individual circadian preference types and sleep EEG patterns related to spindle characteristics, have both been associated with similar cognitive and mental health phenotypes. However, no previous study has examined whether sleep spindles would differ by circadian preference. Here, we explore if spindle amplitude, density, duration or intensity differ by circadian preference and whether these associations are moderated by spindle location, frequency, and time distribution across the night. The participants (N = 170, 59% girls; mean age = 16.9, SD = 0.1 years) filled in the shortened 6-item Horne-Östberg Morningness-Eveningness Questionnaire. We performed an overnight sleep EEG at the homes of the participants. In linear mixed model analyses, we found statistically significant lower spindle amplitude and intensity in the morning as compared to intermediate (P < 0.001) and evening preference groups (P < 0.01; P > 0.06 for spindle duration and density). Spindle frequency moderated the associations (P < 0.003 for slow (<13 Hz); P > 0.2 for fast (>13 Hz)). Growth curve analyses revealed a distinct time distribution of spindles across the night by the circadian preference: both spindle amplitude and intensity decreased more towards morning in the morning preference group than in other groups. Our results indicate that circadian preference is not only affecting the sleep timing, but also associates with sleep microstructure regarding sleep spindle phenotypes.