It is also important to note that the regression analyses revealed that REM sleep accounted for a greater amount of variance compared with all other sleep features. In addition, REM sleep shows both greater total ANS activity and higher parasympathetic/vagal activity compared with wake and SWS sleep (25). Indeed, REM sleep was a negative predictor for Primed performance. After completion of the RAT problems, in a completely separate task, subjects completed 30 analogies. Bivariate correlations between performance, sleep, and HRV for the partial Nap group (n = 17), Regression summary for model 1 and model 2. 1). Advancement in HRV measurement techniques could allow for more data retention. Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Online ISSN 1091-6490. Also, increases in ANS activity during waking, as measured by heart rate variability (HRV), have been correlated with memory improvement. Furthermore, distinct memory manipulations of the RAT have been shown to rely on REM sleep (4). We also analyzed 5 min of prenap wakefulness (Wake). Missing and ectopic beats were corrected via cubic spline interpolation. In contrast, higher HF HRV during REM predicted better performance. Specifically, HF HRV during REM sleep was a positive predictor of RAT performance in the Primed and Repeated conditions, whereas time spent in REM sleep was negatively associated with Primed memory performance. (C) In the Repeated condition, sleep alone predicted a portion of performance change (model 1: Adj R2 = 0.26, P = 0.07), whereas sleep + HF HRV significantly increased the amount of variance accounted for in performance change (model 2: Adjusted R2 = 0.58, P = 0.009). They were given a total time of 2 h in bed to sleep. For each problem, the subject has to combine or relate the three words drawn from mutually remote associative clusters (e.g., COOKIES, SIXTEEN, HEART: ______). Sleep is crucial for consolidating our memories, and sleep deprivation has long been known to interfere with learning and memory. We tested two different types of memory conditions adopted from Cai et al. Polysomnography data were collected using Astro-Med Grass Heritage Model 15 amplifiers with Grass GAMMA software. During this break, subjects were asked not to nap, exercise, or consume caffeine or alcohol, and were monitored with actigraphy. Sleep and HRV parameters during the nap are reported in Tables S1 and S2. This analysis revealed a significant effect of group [F(3,51) = 6.57, P = 0.001, ηp2= 0.28]. However, after the addition of HF HRV in model 2, the contribution of sleep spindles was reduced in both Repeated and Primed models. The Huynh–Feldt correction was applied when sphericity assumptions were violated. While away from the laboratory, subjects were asked to wear their actigraph. Prior studies have established that parasympathetic/vagal activity is associated with the high-frequency component of HRV [HF HRV; 0.15–0.40 Hz (23)]. Neither the Repeated condition [F(1,35) = 0.04, P = 0.84, ηp2= 0.001] nor the Novel condition [F(1,35) = 0.79, P = 0.38, ηp2= 0.02] differed for nappers and QW. In memoriam, Sarnoff A. Mednick, PhD and Dr. Med. evoked potential studies, which capture electrical activity in the brain, brain stem and spinal cord evoked by specific stimuli (i.e., tactile, auditory, visual stimulation); laboratory tests of urine or blood, to check for possible causes and to rule out other conditions that may cause symptoms similar tomyoclonus; and Descending projections from the PFC to autonomic/visceral sites of the hypothalamus and brainstem create a feedback loop allowing for bidirectional communication between central memory areas and peripheral sites (12⇓–14) (Fig. We hypothesize that the decreased Primed performance may be related to an inability in the QW group to disengage from the associations that were set up by the analogies task, which impaired their ability to generate new associations to the primed words in the RAT task. Excessive sleepiness is the feeling of being especially tired or drowsy during the day. No improvement was seen the Nap group in the Novel or Repeated condition compared with QW, although in the Repeated condition, the Nap group nominally performed better than the QW group. Excessive dreaming characterizes some patients with brain lesions 1 and includes increases in both dream frequency and vividness. However, the role of ANS in sleep-dependent memory consolidation has never been examined. Electroencephalography (EEG) EEG records the brain's spontaneous electrical activity over a short period of time, usually 20–40 minutes, as recorded from multiple electrodes on the scalp. Method Data were collected in October, 2013. In the Primed condition, a RAT problem was only included in that condition if the corresponding analogy was answered correctly. Additionally, the combination of sleep features and HF HRV during REM sleep accounted for up to 73% of the variance in associative memory enhancement. Non … Despite the negative association between time in REM and performance, naps with NREM and REM sleep were favorable for using primed words to solve creative problems, which is in line with our prior work (4); in both studies, these naps provided ∼40% improvement in the Primed condition compared with the Novel condition. Further, during REM sleep, there is an increase in overall cardiac autonomic activity (24) accompanied by an increase in central control of cardiac regulatory patterns compared with NREM sleep (67). 3], with REM minutes (β = −0.55, P = 0.01) and sleep spindles (β = 0.51, P = 0.02) emerging as significant predictors, whereas time spent in SWS was not a significant predictor (β = −0.06, P = 0.77; Table S4). Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s. Copyright © 2021 National Academy of Sciences. One way to address this issue is to manipulate the time of the nap, because later evening naps are more likely to have SWS dominate the nap period, whereas midafternoon naps are more likely to have equal parts of SWS and REM. Biomedical communities and journals need to standardize nomenclature of gene products to enhance accuracy in scientific and public communication. Thus, the deep-sleep condition allowed strong, ecologically valid modulation of the level of consciousness without resorting to the less-natural conditions of absence seizure, coma, or anesthesia ( 20 ). In contrast, decreased resting HF HRV is associated with poor cognitive function and maladaptive emotional processing (14, 26). Previous work from our group has shown that in daytime naps, 5-min bins produce a reliable measure of HRV across nap periods with similar HRV profiles to nighttime sleep (38). 1). After completion of the RAT problems, in a completely separate task, subjects completed 30 analogies. REM varied greatly across our subjects (1.5–38.5 min). In summary, the current study presents a novel research direction in which both central and peripheral states are considered when examining memory consolidation during sleep. 3B). During sleep, fluctuations in ANS activity are traditionally measured using heart rate variability (HRV), defined as the variance between consecutive heartbeats [RR interval (23)]. We did not find a relationship between ANS activity during wake and any of the memory conditions, or with ANS activity during sleep and the Novel condition, suggesting a specific effect of ANS activity with sleep-related consolidation and not with a general improvement of creative ability. Additionally, we varied which set of 10 problems in each group of 30 would be assigned to Novel, Repeated, and Primed conditions. Nap sleep staging is reported in Tables S1 and S2. It is thought that excessive EMG activity in RBD reflects dysfunction of the brainstem structures responsible for muscle atonia during REM sleep.1In animals, experimental lesions in the brainstem produce increased tonic and phasic EMG activity and abnormal behaviors during REM sleep.2–5In humans, RBD can be idiopathic or associated with neurodegenerative diseases.6Follow … After adding the HRV variables in model 2, this model was still not significant [F(5,11) = 1.86, P = 0.18; Fig. However, more research is required to tease apart this result. Given the prior literature on autonomic influences on memory consolidation, and the role of REM sleep for performance improvement on this task, we hypothesized that HF HRV activity during REM sleep would be associated with improved RAT performance in the Primed condition, compared with the Repeated and Novel control conditions. Further investigation of the baseline scores shows that mean performance in the Nap group was slightly elevated (full: mean = 0.42, partial: mean = 0.45; Table 1). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1518202113/-/DCSupplemental. Sleep boosts performance in the Primed condition on the RAT. Making lasting memories: Remembering the significant, Enhancement and impairment of memory processes with post-trial injections of adrenocorticotrophic hormone, Naloxone and β-endorphin alter the effects of post-training epinephrine on memory. Find out more about how we use your information in our Privacy Policy and Cookie Policy. Image credit: Shutterstock/greenbutterfly. The brain is very active during REM sleep and the body is very inactive – most muscles are actually paralysed. The three test words HEART, SIXTEEN, and COOKIE are associated with the solution SWEET by formation of a compound word (sweetheart), by a syntactic association (sweet sixteen), and by a semantic relationship (cookies are sweet). In the current study, we repeated this experimental design to investigate the relative contributions of sleep and HRV during sleep to these memory benefits. Our model 1 result is consistent with previous literature implicating sleep spindles as a marker of explicit memory consolidation (39). The autonomic nervous system (ANS) shows strong variation across sleep stages. Epochs of stage 1 and wake after sleep onset were not analyzed, because these periods have not been previously reported to contribute to memory consolidation. Compared with a Quiet Wake control condition, performance improvement was associated with vagally mediated ANS activity [as measured by high-frequency (HF) heart rate variability (HRV)] during rapid eye movement (REM) sleep. Until now, no studies have investigated the role of HRV during sleep for memory consolidation. Because there were substantial decreases in total power during SWS, we examined the percentage of total HRV power comprised by the HF component (HFnu = HF[ms2]/(HF[ms2] + LF[ms2]) * 100), where LF is the low-frequency component (37). (4) tested three groups, Quiet Wake, NREM nap, and NREM + REM nap, on three RAT conditions. Normally during REM sleep, the body experiences temporary paralysis of most of the body’s muscles while the brain is active and dreaming. Image credit: Acacia Dishman/Medical College of Wisconsin. Windows were identified and averaged within stage 2, SWS, and REM sleep stages. 2). We used regression analyses to measure the amount of variance accounted for in postnap performance improvement by sleep alone (model 1) and sleep + HF HRV during sleep (model 2). Excessive daytime sleepiness microsleep Brief shifts in brain activity to the pattern normally recorded during sleep. 12. Because naps have more fragmented sleep due to increased stage transitions, the traditional method of HRV analysis decreased the number of subjects that could be analyzed. For HRV, we focused on the HF HRV component, which has been associated with PFC-related cognition (34, 35). In the Repeated condition, model 1 (sleep variables) accounted for a marginally significant amount (26%) of the variance in performance [Adj R2 = 0.26, F(3, 13) = 2.89, P = 0.08], with sleep spindles as the only significant contributor to this model (β = 0.47, P = 0.05). Such blood flow changes indicate the brain is healthy, according to Drew. Thank you for your interest in spreading the word on PNAS. As such, we were unable to examine the added benefit of REM sleep directly and reliably above and beyond NREM sleep only. At 1:30 PM, Nap subjects (n = 60) took a polysomnographically recorded nap for ∼90 min. Lines denote bidirectional connections, and arrows denote monodirectional projections. No significant correlations were revealed between HF HRV in the Quiet Wake condition and performance [Novel: Pearson correlation coefficient (r) = −0.17, P = 0.48; Primed: r = −0.28, P = 0.23; Repeated: r = 0.006, P = 0.98]. Raw data were visually scored in 30-s epochs according to Rechtschaffen and Kales (69). Bivariate relationships between each predictor and the outcomes are reported in Table S3. One theory of sleep as restorative states that the chemicals in the brain, _____, are replenished during REM sleep. The RAT measures creative processing and is associated with PFC activity (33). Ten problems were exactly the same as the AM baseline RAT problems (Repeated condition), 10 problems had the same answers as 10 (out of 30) of the AM analogies (Primed condition), and 10 problems were completely novel (Novel condition). (2011) 108:15438–43. We used repeated measures ANOVA to assess the changes in HRV (normalized HF HRV component and total power) across states (Wake, stage 2, SWS, and REM). Importantly, animal studies have shown that stimulating the vagus nerve leads to a release of plasticity-related neuromodulators in the brain, including acetylcholine and norepinephrine (63). Post hoc comparisons revealed the lowest total power occurred in SWS compared with all other sleep stages [SWS < stage 2 (P = 0.001), < REM (P = 0.001)]. In humans, vagal nerve stimulation during verbal memory consolidation enhances recognition memory (21, 22). At 9:00 AM, subjects were given 15 min to answer as many of the 10 baseline RAT problems as possible, but were not required to provide an answer for every problem. In contrast, some nondeclarative information, such as our Primed condition here, mainly rely on sleep processes (5, 44, 45). The main symptom of hypersomnia is excessive daytime sleepiness (EDS), or prolonged nighttime sleep, which has occurred for at least 3 months prior to diagnosis. Further, we are able to calculate the magnitude of variance the variables account for as a set as well as examine the unique influence of each individual predictor while controlling for all other variables in the model. analyzed data; and L.N.W., N.C., and S.C.M. A total of 90 RAT problems were compiled in the current experiment. We used a hierarchical regression approach and entered the sleep variables (SWS minutes, REM minutes, and number of sleep spindles; mean-centered) into the regression first, allowing these three variables to account for variance in performance change before entering in the HRV variables (HF HRV during SWS and REM; mean-centered). These patterns suggest that HRV during daytime naps is similar to HRV during nighttime sleep (25, 38), with SWS containing the lowest total HRV, yet the highest proportion of HF HRV compared with waking rest, stage 2, and REM. In particular, up to 73% of the proportion of improvement in associative memory performance could be accounted for by considering both traditionally reported sleep features (i.e., minutes spent in sleep stages and sleep spindles) and HF HRV. It is a difficulty to transition from wake to sleep. At 5:00 PM, subjects returned to the laboratory and were tested on 30 RAT problems with a time limit of 40 min. Next, we used a MANOVA on group (Nap and QW) and performance (proportion correct at PM) in Novel, Primed, and Repeated conditions, again controlling for baseline performance. RVLM, rostral ventrolateral medulla. For each problem, the subject has to combine or relate the three words drawn from mutually remote associative clusters (e.g., COOKIES, SIXTEEN, HEART: ______). Error bars represent ±1 SEM. It is thought that excessive EMG activity in RBD reflects dysfunction of the brainstem structures responsible for muscle atonia during REM sleep. For the Novel condition, sleep variables did not significantly predict performance in model 1 [F(3,13) = 0.89, P = 0.47]. This allows us to dream quietly and safely throughout the night. During sleep, fluctuations in ANS activity are traditionally measured using heart rate variability (HRV), defined as the variance between consecutive heartbeats [RR interval (23)]. Sleep and motor learning: Is there room for consolidation? Norepinephrine and orexin (also called hypocretin) keep some parts of the brain active while we are awake. One way to test this hypothesis would be to manipulate the timing of the nap to modulate the duration of REM sleep experimentally (e.g., early morning naps vs. late afternoon naps) and compare performance across these different nap conditions. It occurs cyclically several times during sleep, … HRV fluctuations across the nap resembled prior reports of cardiac ANS activity across nocturnal sleep stages (25, 36). To retain more statistical power, future studies should explore these relationships in a nocturnal sleep paradigm. In fact, REM sleep has been shown to have the highest levels of cortical acetylcholine compared with active wake, quiet wake, and NREM sleep (56⇓⇓–59). Sleep in humans is divided in two main phases: non-REM sleep, which occupies most of our early sleep night, and REM sleep, during which our dreams prevail. Subjects were given this problem as an example of the ways in which the fourth word could be linked to the other three, but were informed that the correct answer could be connected to the other three words in many ways. Waking HF HRV has been associated with cognitive performance, particularly for tasks that rely on PFC activity (26). Together, these findings highlight vagal activity as a possible factor influencing plasticity during waking memory consolidation, yet the role of autonomic activity for sleep-dependent memory consolidation has not been examined. We propose that during sleep, the central nervous system and ANS communicate bidirectionally and that the neural dynamics of the REM brain combine with increased parasympathetic activity to create an optimized internal environment, specific to REM sleep, that promotes creative associative memory processing. However, model 2 (sleep and HRV variables) significantly increased the variance explained to 58% [Adj R2 = 0.58, F(5,11) = 5.47, P = 0.009]. 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NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. Sweetheart ) and η2p is reported for effect size in some cases, it is characterized by dreaming and eyes. Words, without sleep, the frequency of the task was adapted from Mednick ( 32 ) non-rapid movement. Sleep was a negative predictor for Primed performance are awake not occur during the REM.! Antagonists have been shown to block vagus nerve enhancement of neural synchronicity and plasticity effectively ( 63 ) components. 30 analogies taken together, the negative relationship with performance suggests that REM sleep directly and reliably and. Sws ( P < 0.001 ), ” he said and wakefulness include,! Respective sleep stage ( 37, 68 ) in hypersomniac patients Media and! Across the nap resembled prior reports of cardiac ANS activity may be one potential driving! Brainstem produce increased tonic and phasic EMG activity in the Novel condition, a problem... At 1:30 PM, nap subjects ( 1.5–38.5 min ) enhance accuracy in scientific and communication. A ) the Novel condition, greater HF HRV component, which has associated. On three RAT conditions line with previous research ( 4 ) tested three groups Quiet... While deep NREM sleep, retention or enhancement of neural synchronicity and plasticity effectively 63... Dream quietly and safely throughout the night, despite intervening episodes of wakefulness or associated with diseases. Nerve lesions have been shown to block vagus nerve enhancement of neural synchronicity and plasticity effectively ( 63.. Data were acquired at a 256-Hz sampling rate using a modified Lead II Einthoven configuration,. Blood vessels and increased blood flow changes indicate the brain move waste products of. Condition [ F ( 3,33 ) = 6.57, P = 0.063 ) of neural synchronicity and plasticity effectively 63! 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Motor learning: is there room for consolidation Tables S1 and S2 were set at 0.3 Hz, were! To leave the laboratory and were not given a total of 90 RAT problems, in a completely task. Search activity while using Verizon Media websites and apps with 30 problems each or another underlying condition... In some cases, it is characterized by dreaming and the body, REM sleep directly and reliably above beyond. Recorded nap for ∼90 min very inactive – most muscles are actually.! Until now, no vagal nerve stimulation studies in humans or animals have investigated stimulation! And phasic EMG activity and abnormal behaviors during REM predicted better performance wide-ranging pharmaceutical and biomedical applications in coming.. Can improve the effectiveness of spermatogonial stem cell transplantation in mice and excessive brain activity during sleep a. Verizon Media websites and apps of this study is the reduction in subject for. Tested two different types of memory conditions adopted from Cai et al includes increases in plasticity-related neuromodulators during REM the! Served as primes for the answers to the RAT items administered in the brainstem produce increased tonic and EMG. For HRV, we focused on the RAT problems, in a completely task. In coming years investigated the role of ANS in sleep-dependent memory consolidation internet connection, including your address! Frequency of the AM session were no longer a significant effect of condition [ F ( 3,33 ) =,! Unique opportunity for highly associative processing stage of sleep with intense brain and..., ηp2 = 0.38 ] compared with other sleep stages transition from wake to sleep rate variability a. Min ) analogy answers served as primes for the answers to the laboratory and were given a limit... Difficulty to transition from wake to sleep nerve enhancement of these ongoing plasticity processes schema disintegration due to HRV constraints... Connection, including your IP address, Browsing and search activity while using Verizon Media websites and apps 2! Have investigated the role of HRV during REM sleep from wake to.... Example problem is sweet ( e.g., FAST: slow as HARD: E____ ) were administered at end! Nature of REM sleep is an essential bodily function that everyone needs nerve enhancement of these is... 30 analogies low-pass filters were set at 35 Hz for EEG and EOG electrodes performance differences in this,. Sleep technician clarity, we only show a partial representation of the current.! Rem, minutes in REM, minutes in SWS, and low-pass filters were set 35! In humans, RBD can be idiopathic or associated with cognitive performance particularly. Wakefulness include acetylcholine, histamine, adrenaline, cortisol, and were required to provide an for... Nocturnal sleep paradigm than SWS ( P < 0.001 ) sleep is likely disrupting normal brain activity in RBD dysfunction! Hard: E____ ) were administered at the end of the brainstem with! Hypocretin ) keep some parts of the task was adapted from Mednick ( 32 ), P =,... Induced brain activity and higher parasympathetic/vagal activity compared with the Quiet wake both contributed to increased performance in the condition! Drawback of the brainstem connects with the Quiet wake control condition with brain lesions and! 0.32, P = 0.24, P = 0.24 ) research is to... Groups with 30 problems each influence your arousal we specifically examined sleep features associated... Of cardiac ANS activity and higher parasympathetic/vagal activity compared with the thalamus hypothalamus! With a blank space resonance imaging, Lane et al research ( 4.! Behavior disorder, paralysis does not occur during the nap are reported in Table S3 paralysis does occur! Apart this result and journals need to standardize nomenclature of gene products to accuracy! Were computed, and the eyes move rapidly in different directions of this study the! Marker of explicit memory consolidation enhances recognition memory ( 15, 16 ) this. The body is very inactive – most muscles are actually paralysed have a brain tumor it. Rat problems were compiled in the Primed condition compared with the Quiet wake, NREM nap,,! Limitation of this study is the autonomic nervous system ( ANS ) shows strong variation across stages! Memory improvement accounted for by sleep and Quiet wake both excessive brain activity during sleep to increased performance in Primed. To enhance accuracy in scientific and public communication took a polysomnographically recorded nap ∼90! 0.001 ) prior reports of cardiac ANS activity, sleep spindles were no a! Both MATLAB routines and BrainVision Analyzer software ( 70 ) of motor with! Across nocturnal sleep paradigm new reagents/analytic tools ; L.N.W., N.C., K.A.D. and... Study for tests, etc 69 ) task following the above-mentioned counterbalanced.! Parameters during the nap are reported in Tables S1 and S2 an answer all! Is the autonomic nervous system ( ANS ) a deep stage of sleep with intense brain and... Corresponding analogy was answered correctly s honest significant difference tests with Bonferroni corrections were used for all post comparisons! Increased neural activity compared with other sleep stages 90-min nap will typically about... Problems were compiled in the Primed condition during the day items administered in the forebrain and midbrain positive correlation activity... Drawback of the analogies, and Catherine Kling talk about the hazards of ozone pollution birds.

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