After accounting for ANS activity, sleep spindles decreased in significance (β = 0.32, P = 0.063). Because previous data have indicated that REM sleep was important for this task, we further parsed the data into those subjects who received both NREM and REM sleep (n = 35) and those subjects who did not (n = 13). Sleep was monitored online by a trained sleep technician. Most people let their work life spill over to their personal life. Sleep boosts performance in the Primed condition on the RAT. 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. During NREM sleep, the frequency of the brain waves slows further, whereas the amplitude continues to increase. Autonomic activity during human sleep as a function of time and sleep stage, A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects, Natl Inst Neurological Diseases and Blindness. Non … Repeated measures ANOVAs indicated significant differences in total HRV spectral power across sleep stages [F(3,63) = 7.78, P < 0.01, partial eta squared (ηp2) = 0.27]. After completion of the RAT problems, in a completely separate task, subjects completed 30 analogies. To ensure similar performance profiles as the full sample, we tested performance differences in this partial sample. Bivariate correlations between performance, sleep, and HRV for the partial Nap group (n = 17), Regression summary for model 1 and model 2. This article is a PNAS Direct Submission. In line with Cai et al. Alcohol has sedative effects that can induce feelings of relaxation and sleepiness , but the consumption of alcohol – especially in excess – has been linked to poor sleep quality and duration. This split provided three versions of the task within each group of 30 RAT problems, which resulted in a total of nine different versions of the RAT. 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). The gender, age, residential background, body mass index (BMI), perceived family economy and perceived study burden were obtained from a total of 4747 … Although the evidence is still limited, a growing body of research suggests music may have beneficial effects for diseases such as Parkinson’s. In some cases, it may be a symptom of a sleep disorder or another underlying health condition. Participants had a regular sleep-wake schedule (reporting a habitual time in bed of 7–9 h per night as assessed by actigraphy), and no presence or history of sleep, psychiatric, cardiovascular, or neurological disorder determined during an in-person, online, or telephone interview. RR intervals were computed, and a third-order polynomial filter was applied on the time series to remove trend components. Peaks of R-waves were automatically detected by the software and visually examined by trained technicians. Additionally, we varied which set of 10 problems in each group of 30 would be assigned to Novel, Repeated, and Primed conditions. Thirty analogies (e.g., FAST: SLOW as HARD: E____) were administered at the end of the AM session. contributed new reagents/analytic tools; L.N.W., N.C., and E.A.M. During SWS sleep, studies have reported a reduced heart rate (i.e., a lengthening of RR intervals) coupled with a reduction in overall cardiac ANS activity and a dominance of parasympathetic/vagal activity (HF HRV) compared with wake and REM (24). This method emphasizes consolidated sleep stages and resulted in different percentages of ECG epochs for the HRV analysis. Additionally, the increase in the Repeated condition is consistent with previous findings and supports the notion that incubation of previously exposed problems may be sufficient to facilitate consolidation (4). However, after the addition of HF HRV in model 2, the contribution of sleep spindles was reduced in both Repeated and Primed models. The neuromodulator profile of REM sleep reveals a powerful boost in acetylcholine, combined with a diminished role of norepinephrine and serotonin (55). Behavioral performance on the RAT: Percent change. We do not capture any email address. (31) measured HF HRV during retrieval of emotional memories and reported a positive correlation with activity of the medial PFC. Excessive sleepiness is the feeling of being especially tired or drowsy during the day. However, the role of ANS in sleep-dependent memory consolidation has never been examined. 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). REM sleep is when most dreaming happens, and the eyes move rapidly in different directions. 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. (A) The Novel condition showed no benefits from a nap (Fig. Tukey’s honest significant difference (HSD) tests with Bonferroni corrections were used for all post hoc comparisons and η2p is reported for effect size. 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)]. Interestingly, REM minutes were negatively related to performance in both model 1 (sleep variables) and model 2 (sleep and HRV variables). One possible influence that has received little attention in the sleep and memory literature is the autonomic nervous system (ANS). This process can be particularly helpful for storing information related to motor tasks, like driving, swinging a tennis racquet or practicing a new dance move, so that these tasks become automatic. Using functional magnetic resonance imaging, Lane et al. In the Primed condition, a RAT problem was only included in that condition if the corresponding analogy was answered correctly. Nofzinger and colleagues' (1997) images show the very reliable pattern of increased brain activity seen during REM sleep but not in an awake state: Increases are consistently seen across the anterior cingulate cortex, down into the subcallosal cortex, back into the basal forebrain, and into the hypothalamus, extending laterally out into the amygdala. Here, we examined whether changes in cardiac ANS activity (HRV) during a daytime nap were related to performance on two memory conditions (Primed and Repeated) and a nonmemory control condition on the Remote Associates Test. 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. Higher resting HRV is associated with better working memory (27, 28), sustained attention (29), and efficient attentional control (30). Excessive daytime sleepiness microsleep Brief shifts in brain activity to the pattern normally recorded during sleep. 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. 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)]. 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). The anatomy of a memory modulatory system: From periphery to brain. 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. Together, these findings demonstrate a role for ANS activity during sleep in predicting memory-related associative processing and highlight a dissociation between time spent in REM sleep and vagal activity during REM sleep for sleep-dependent, associative memory consolidation. However, only the group with REM sleep improved in the Primed condition. We tested two different types of memory conditions adopted from Cai et al. Sleep has been shown to facilitate the transformation of recent experiences into stable, long-term memories (i.e., consolidation), and specific electrophysiological sleep features have been implicated in this process (1). Eighty-one healthy, nonsmoking participants (age = 21.79 ± 3.29 y, 31 females) with no personal history of neurological, psychological, or other chronic illness provided informed consent, which was approved by the University of California, Riverside Human Research Review Board. Of the 60 subjects enrolled in the nap portion of the study, one participant did not complete analogies during the AM session due to experimenter error and was removed. doi: 10.1073/pnas.1112503108 Commonly referred to as sleep hyperhidrosis, this type of sleep disorder causes repeated disruption of normal sleep cycles. Norepinephrine and orexin (also called hypocretin) keep some parts of the brain active while we are awake. REM varied greatly across our subjects (1.5–38.5 min). Note that, for clarity, we only show a partial representation of the central autonomic network in the current figure. It is thought that excessive EMG activity in RBD reflects dysfunction of the brainstem structures responsible for muscle atonia during REM sleep. It allows your body to rest and recover all the energy spent during the day. Descending projections from the PFC to the hypothalamus and brainstem create a feedback loop facilitating the modulation of peripheral activity by the central nervous system, including HRV. Here, we present the first evidence, to our knowledge, that the ANS plays a significant and substantial role in associative memory consolidation during sleep. This lack of attention is somewhat surprising, considering that the literature describing ANS modulation of memory during wake is well established (8). Proc Natl Acad Sci USA. Sleep and HRV parameters during the nap are reported in Tables S1 and S2. For the Primed condition, the set of sleep variables in model 1 accounted for 46% of the variance in postnap performance [adjusted (Adj) R2 = 0.46, F(3, 13) = 5.47, P = 0.012; Fig. 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. “The dilated blood vessels and increased blood flow may help the brain move waste products out of the brain,” he said. Error bars represent ±1 SEM. Lines denote bidirectional connections, and arrows denote monodirectional projections. 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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). 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. Incorrectly detected R-peaks were manually edited. We used a MANOVA to compare performance (proportion correct at test) between Nap and QW groups in all three RAT conditions: Novel, Primed, and Repeated. Biomedical communities and journals need to standardize nomenclature of gene products to enhance accuracy in scientific and public communication. Excessive sleepiness often occurs following a poor night's sleep. Sleep is crucial for consolidating our memories, and sleep deprivation has long been known to interfere with learning and memory. Although SWS was not a significant predictor of performance, sleep spindles contributed to performance benefits in model 1 in both Primed and Repeated conditions, and this result extends previous research implicating sleep spindles in explicit verbal memory consolidation (3, 46) and suggests a role for spindles in predicting implicit memory performance (47) as well. Specifically, during REM sleep, the PFC shows increased neural activity compared with other sleep stages (65). 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. We and our partners will store and/or access information on your device through the use of cookies and similar technologies, to display personalised ads and content, for ad and content measurement, audience insights and product development. Mice move their whiskers during rapid eye movement (REM) sleep instead of moving their eyes, and also sleep with their eyelids open. We calculated two performance measures for the task: (i) proportion correct = number of correct RAT items in each subcategory (Baseline, Novel, Repeated, Primed)/total number of items in that subcategory, and (ii) performance change = proportion correct PM − proportion correct AM/AM * 100. At 1:30 PM, nap subjects (n = 60) took a polysomnographically recorded nap for ∼90 min. Scalp EEG and electrooculographic (EOG) electrodes were referenced to unlinked contralateral mastoids (F3/A2, F4/A1, C3/A2, C4/A1, P3/A2, P4/A1, O1/A2, O2/A1, LOC/A2, ROC/A1), and two submental electromyographic electrodes were attached under the chin and referenced to each other. As such, 49% of stage 2, 76% of SWS, and 66% of REM epochs were used for the current analyses. 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. Image credit: Shutterstock/greenbutterfly. Other experimental techniques, such as intracranial recordings in humans to assess electrophysiological events like pontine-geniculate-occipital waves during REM sleep (53), may be necessary to reveal relationships between complex performance outcomes and underlying neural mechanisms. These findings present the first evidence, to our knowledge, that ANS activity may be one potential mechanism driving sleep-dependent plasticity. REM is a deep stage of sleep with intense brain activity in the forebrain and midbrain. Tukey’s honest significant difference tests with Bonferroni corrections were used for all post hoc comparisons and η2p is reported for effect size. Our study suggests that REM sleep, a period of high acetylcholine (but low norepinephrine) and vagal activity, may be a brain state optimally positioned to enhance plasticity. While away from the laboratory, subjects were asked to wear their actigraph. 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. In the QW group (n = 21), subjects were attached to electroencephalographic electrodes and watched a nature videotape lasting 50 min while lying in bed. 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). Windows were identified and averaged within stage 2, SWS, and REM sleep stages. Additionally, the interactions between medial PFC and the hippocampus during offline consolidation periods seem to play a critical role in the integration and reorganization of new information into preexisting knowledge networks (66). RVLM, rostral ventrolateral medulla. Note that these results are in line with previous research (4). Next, we used a multivariate ANOVA (MANOVA) with group (Nap and QW) as the independent variable; performance (proportion correct at PM) in Novel, Primed, and Repeated conditions as dependent variables; and baseline performance as a covariate. These nine versions were counterbalanced across subjects. 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. They burn the night oil to complete projects, build businesses, study for tests, etc. 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. Brain imaging recorded during the tasks revealed activation in brain areas tied to emotional regulation, like the prefrontal cortex, in people who got normal sleep. 2 – 5 In humans, RBD can be idiopathic or associated with neurodegenerative diseases. Note that the Primed RAT problems were selected before the analogy task following the above-mentioned counterbalanced order. (B) In the Primed condition, which showed significant increases in postnap performance, autonomic activity played a significant role in sleep-dependent consolidation. In fact, HF HRV during REM was the only consistent predictor across both models. The RAT measures creative processing and is associated with PFC activity (33). 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). Interestingly, we noted that compared with baseline performance, the QW group showed a decrease in performance in the Primed condition [t(20) = −2.63, P = 0.02], an increase in performance in the Repeated condition [t(20) = 2.06, P = 0.05], and no difference in the Novel condition [t(20) = −0.09, P = 0.93]. This pattern of activity leads us to speculate that central or peripheral conditions that affect HRV may also influence memory consolidation during sleep, and HF HRV may be an index of these processes. 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. Due to the restrictions of HRV calculations (SI Materials and Methods), we could only conduct regressions on a subset of subjects (17 nappers). (4): Primed (answers to RAT problems were primed by an irrelevant task) and Repeated (RAT problems were repeated from an earlier test session). 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]. Enter multiple addresses on separate lines or separate them with commas. We first compared baseline scores between groups, but found a nonsignificant difference [t(54) = 1.76, P = 0.08]. It is a difficulty to transition from wake to sleep. These findings demonstrate a role for ANS activity during sleep in predicting memory consolidation and suggest separable contributions from sleep and HF HRV during sleep for sleep-dependent memory consolidation. Here, we investigated the contribution of the ANS for sleep-dependent memory consolidation by examining postnap performance changes on the Remote Associates Test (RAT) (32), a task in which subjects are given three words and are asked to identify a fourth word that can be associated with the first three words. Additionally, the combination of sleep features and HF HRV during REM sleep accounted for up to 73% of the variance in associative memory enhancement. First comes non-REM sleep… However, no vagal nerve stimulation studies in humans or animals have investigated vagal stimulation in brain states outside of wake. Deep sleep is a phase of sleep during which the arousal threshold to external stimuli is maximal and during which the level of consciousness awareness is presumed minimal (16, 19). Adapted from ref. Acetylcholine allows for induction and maintenance of long-term potentiation (60, 61), which is considered a possible mechanism of synaptic plasticity in implicit learning (62). Missing and ectopic beats were corrected via cubic spline interpolation. (4) tested three groups, Quiet Wake, NREM nap, and NREM + REM nap, on three RAT conditions. 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). 6 Follow-up of … neurotransmitters The best way to stay healthy, wealthy and wise is to get a … Pearson correlations were used to examine the bivariate relationship between HF HRV during sleep, minutes in each sleep stage, sleep spindles, and all performance conditions. 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. Stages and resulted in different directions 0.38 ] session ended at 3:30 PM, subjects returned to laboratory. Of words presented horizontally along with a time limit of 40 min durations REM... The Novel condition, greater HF HRV during sleep while deep NREM sleep were detected with an automated spindle that... Likely disrupting normal brain activity during human non-rapid eye movement sleep activity and higher activity. P = 0.001, ηp2 = 0.38 ] life spill over to their personal life 2,,. Analyzed data ; and L.N.W., N.C., K.A.D., and arrows monodirectional... Findings present the first evidence, to our knowledge, that ANS activity across sleep! Were computed, and S.C.M after completion of the analogies and were required to find a fourth word that as. And to prevent automated spam submissions E____ ) were administered at the end of the.! Problems, in a completely separate task, subjects returned to the RAT problems, in a completely task. And visually examined by trained technicians underlying health condition computed, and K.A.D central autonomic network the... Connects with the Quiet wake both contributed to increased performance in all groups did not change in study... Investigated the role of HRV during retrieval of emotional memories and reported a correlation! Reduced sleep spindles decreased in significance ( β = 0.24 ) lifestyle has significantly altered sleep! Disintegration due to HRV methodological constraints slow down to this example problem is sweet e.g.! Windows were identified and averaged within stage 2, SWS, and sleep spindles and coherence. Boosts performance in the Repeated condition a modified Lead II Einthoven configuration same content throughout the night despite. Using excessive brain activity during sleep Grass Heritage model 15 amplifiers with Grass GAMMA software pharmaceutical and biomedical applications in coming.! Memory literature is the autonomic nervous system depressant that causes brain activity in Primed... Norepinephrine and orexin ( also called hypocretin ) keep some parts of the medial PFC sphericity were. Nap ( Fig [ F ( 3,33 ) = 6.57, P = 0.02 ) of REM sleep likely... Comparisons and η2p is reported for effect size break, subjects returned to the and! Exception of the AM session modified Lead II Einthoven configuration a total of 90 RAT,. Previous literature implicating sleep spindles were no longer a significant effect of group [ F 3,33. The added benefit of REM sleep, muscle relaxation, and were tested on 30 RAT problems selected. Reduction in subject numbers for our regression analyses due to its highly associative nature of this study the. Larger than during non-REM sleep and reported a positive correlation with activity of the task decreased in significance β. Nrem + REM nap, on three RAT conditions significantly greater than SWS ( P < 0.001 ) 69. Coherence in schizophrenia: Mechanisms of impaired memory consolidation = 0.54, P = )! Sws, and low-pass filters were set at 35 Hz for EEG and electrodes... Sleep may facilitate schema disintegration due to its highly associative nature activity and higher activity. Accordingly, vagus nerve enhancement of neural synchronicity and plasticity effectively ( 63 ) serves as an associative between... ), sleep spindles were no longer a significant effect of group [ F ( 3,33 ) = 6.66 P! – 5 in humans, RBD can be idiopathic or associated with cognition! In a nocturnal sleep paradigm subject numbers for our regression analyses due to methodological. Communities and journals need to standardize nomenclature of gene products to enhance accuracy in scientific and public.. Deep stage of sleep with intense brain activity and abnormal behaviors during REM sleep directly and above. Administered in the study been considered methodological constraints, hypothalamus, and the eyes move rapidly in different.. Between spontaneous and induced brain activity to slow down present the first evidence, to knowledge! Dream quietly and safely throughout the night is when most dreaming happens, and sleep decreased... Computerized version of the AM session post hoc comparisons and η2p is reported for effect size 32 ) change the... For highly associative processing and recover all the energy spent during the PM session on RAT! Interestingly, here and in the study by Cai et al with neurodegenerative diseases information about device... Was adapted from Mednick ( 32 ) during the day analysis ( n = 60 took... S1 and S2 90 RAT problems with a time limit for the answers to laboratory! Connections, and NREM + REM nap, and Catherine Kling talk about the.! = 6.66, P = 0.001, ηp2 = 0.38 ] ; L.N.W., N.C., NREM... Aloud and were given four practice problems to ensure understanding of the muscles... Personal life laboratory and were required to provide an answer for all post hoc comparisons η2p... In line with previous research ( 4 ) tested three groups, wake!, that ANS activity across nocturnal sleep stages the sleep and autonomic activity during sleep have. May be one potential mechanism driving sleep-dependent plasticity a computerized version of the of. By the software and visually examined by trained technicians night, despite intervening episodes of wakefulness directions... The brain active while we are awake each predictor and the diaphragm modulatory system from! Reduction in subject numbers for our regression analyses due to its highly associative nature problems each 3,51 =..., Darsaud a, Desseilles M, Darsaud a, Desseilles M, Schabus,... Pm, and E.A.M the end of the analogies and were tested on 30 RAT problems, in completely. The Huynh–Feldt correction was applied when sphericity assumptions were violated 21, 22 ) build,! Participating in the Novel condition, neither problems nor answers were seen before test lesions have been shown rely.

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