Autonomic Activity during a Daytime Nap Facilitates Working Memory Improvement.

Recent investigations have implicated the parasympathetic branch of the autonomic nervous system in higher-order executive functions. These actions are purported to occur through autonomic nervous system's modulation of the pFC, with parasympathetic activity during wake associated with working memory (WM) ability. Compared with wake, sleep is a period with substantially greater parasympathetic tone. Recent work has reported that sleep may also contribute to improvement in WM. Here, we examined the role of cardiac parasympathetic activity during sleep on WM improvement in healthy young adults. Participants were tested in an operation span task in the morning and evening, and during the intertest period, participants experienced either a nap or wake. We measured high-frequency heart rate variability as an index of cardiac, parasympathetic activity during both wake and sleep. Participants showed the expected boost in parasympathetic activity during nap, compared with wake. Furthermore, parasympathetic activity during sleep, but not wake, was significantly correlated with WM improvement. Together, these results indicate that the natural boost in parasympathetic activity during sleep may benefit gains in prefrontal executive function in young adults. We present a conceptual model illustrating the interaction between sleep, autonomic activity, and prefrontal brain function and highlight open research questions that will facilitate understanding of the factors that contribute to executive abilities in young adults as well as in cognitive aging.

Autonomic/central coupling benefits working memory in healthy young adults.

Working memory (WM) is an executive function that can improve with training. However, the precise mechanism for this improvement is not known. Studies have shown greater WM gains after a period of sleep than a similar period of wake, and correlations between WM improvement and slow wave activity (SWA; 0.5-1 Hz) during slow wave sleep (SWS). A different body of literature has suggested an important role for autonomic activity during wake for WM. A recent study from our group reported that the temporal coupling of Autonomic/CentralEvents (ACEs) during sleep was associated with memory consolidation. We found that heart rate bursts (HR bursts) during non-rapid eye movement (NREM) sleep are accompanied by increases in SWA and sigma (12-15 Hz) power, as well as increases in the high-frequency (HF) component of the RR interval, reflecting vagal rebound. In addition, ACEs predict long-term, episodic memory improvement. Building on these previous results, we examined whether ACEs also contribute to gains in WM. We tested 104 young adults in an operation span task (OSPAN) in the morning and evening, with either a nap (n = 53; with electroencephalography (EEG) and electrocardiography (ECG)) or wake (n = 51) between testing sessions. We identified HR bursts in the ECG and replicated the increases in SWA and sigma prior to peak of the HR burst, as well as vagal rebound after the peak. Furthermore, we showed sleep-dependent WM improvement, which was predicted by ACE activity. Using regression analyses, we discovered that significantly more variance in WM improvement could be explained with ACE variables than with overall sleep activity not time-locked with ECG. These results provide the first evidence that coordinated autonomic and central events play a significant role in sleep-related WM improvement and implicate the potential of autonomic interventions during sleep for cognitive enhancement.

The effect of zolpidem on memory consolidation over a night of sleep.

STUDY OBJECTIVES: Nonrapid eye movement sleep boosts hippocampus-dependent, long-term memory formation more so than wake. Studies have pointed to several electrophysiological events that likely play a role in this process, including thalamocortical sleep spindles (12-15 Hz). However, interventional studies that directly probe the causal role of spindles in consolidation are scarce. Previous studies have used zolpidem, a GABA-A agonist, to increase sleep spindles during a daytime nap and promote hippocampal-dependent episodic memory. The current study investigated the effect of zolpidem on nighttime sleep and overnight improvement of episodic memories. METHODS: We used a double-blind, placebo-controlled within-subject design to test the a priori hypothesis that zolpidem would lead to increased memory performance on a word-paired associates task by boosting spindle activity. We also explored the impact of zolpidem across a range of other spectral sleep features, including slow oscillations (0-1 Hz), delta (1-4 Hz), theta (4-8 Hz), sigma (12-15 Hz), as well as spindle-SO coupling. RESULTS: We showed greater memory improvement after a night of sleep with zolpidem, compared to placebo, replicating a prior nap study. Additionally, zolpidem increased sigma power, decreased theta and delta power, and altered the phase angle of spindle-SO coupling, compared to placebo. Spindle density, theta power, and spindle-SO coupling were associated with next-day memory performance. CONCLUSIONS: These results are consistent with the hypothesis that sleep, specifically the timing and amount of sleep spindles, plays a causal role in the long-term formation of episodic memories. Furthermore, our results emphasize the role of nonrapid eye movement theta activity in human memory consolidation.

Timing between Cortical Slow Oscillations and Heart Rate Bursts during Sleep Predicts Temporal Processing Speed, but Not Offline Consolidation.

Central and autonomic nervous system activities are coupled during sleep. Cortical slow oscillations (SOs; <1 Hz) coincide with brief bursts in heart rate (HR), but the functional consequence of this coupling in cognition remains elusive. We measured SO-HR temporal coupling (i.e., the peak-to-peak interval between downstate of SO event and HR burst) during a daytime nap and asked whether this SO-HR timing measure was associated with temporal processing speed and learning on a texture discrimination task by testing participants before and after a nap. The coherence of SO-HR events during sleep strongly correlated with an individual's temporal processing speed in the morning and evening test sessions, but not with their change in performance after the nap (i.e., consolidation). We confirmed this result in two additional experimental visits and also discovered that this association was visit-specific, indicating a state (not trait) marker. Thus, we introduce a novel physiological index that may be a useful marker of state-dependent processing speed of an individual.

Coupling of autonomic and central events during sleep benefits declarative memory consolidation.

While anatomical pathways between forebrain cognitive and brainstem autonomic nervous centers are well-defined, autonomic-central interactions during sleep and their contribution to waking performance are not understood. Here, we analyzed simultaneous central activity via electroencephalography (EEG) and autonomic heart beat-to-beat intervals (RR intervals) from electrocardiography (ECG) during wake and daytime sleep. We identified bursts of ECG activity that lasted 4-5 s and predominated in non-rapid-eye-movement sleep (NREM). Using event-based analysis of NREM sleep, we found an increase in delta (0.5-4 Hz) and sigma (12-15 Hz) power and an elevated density of slow oscillations (0.5-1 Hz) about 5 s prior to peak of the heart rate burst, as well as a surge in vagal activity, assessed by high-frequency (HF) component of RR intervals. Using regression framework, we show that these Autonomic/Central Events (ACE) positively predicted post-nap improvement in a declarative memory task after controlling for the effects of spindles and slow oscillations from sleep periods without ACE. No such relation was found between memory performance and a control nap. Additionally, NREM ACE negatively correlated with REM sleep and learning in a non-declarative memory task. These results provide the first evidence that coordinated autonomic and central events play a significant role in declarative memory consolidation.

Computational model of brain-stem circuit for state-dependent control of hypoglossal motoneurons.

In patients with obstructive sleep apnea (OSA), the pharyngeal muscles become relaxed during sleep, which leads to a partial or complete closure of upper airway. Experimental studies suggest that withdrawal of noradrenergic and serotonergic drives importantly contributes to depression of hypoglossal motoneurons and, therefore, may contribute to OSA pathophysiology; however, specific cellular and synaptic mechanisms remain unknown. In this new study, we developed a biophysical network model to test the hypothesis that, to explain experimental observations, the neuronal network for monoaminergic control of excitability of hypoglossal motoneurons needs to include excitatory and inhibitory perihypoglossal interneurons that mediate noradrenergic and serotonergic drives to hypoglossal motoneurons. In the model, the state-dependent activation of the hypoglossal motoneurons was in qualitative agreement with in vivo data during simulated rapid eye movement (REM) and non-REM sleep. The model was applied to test the mechanisms of action of noradrenergic and serotonergic drugs during REM sleep as observed in vivo. We conclude that the proposed minimal neuronal circuit is sufficient to explain in vivo data and supports the hypothesis that perihypoglossal interneurons may mediate state-dependent monoaminergic drive to hypoglossal motoneurons. The population of the hypothesized perihypoglossal interneurons may serve as novel targets for pharmacological treatment of OSA. NEW & NOTEWORTHY In vivo studies suggest that during rapid eye movement sleep, withdrawal of noradrenergic and serotonergic drives critically contributes to depression of hypoglossal motoneurons (HMs), which innervate the tongue muscles. By means of a biophysical model, which is consistent with a broad range of empirical data, we demonstrate that the neuronal network controlling the excitability of HMs needs to include excitatory and inhibitory interneurons that mediate noradrenergic and serotonergic drives to HMs.

Comparing the cardiac autonomic activity profile of daytime naps and nighttime sleep.

Heart rate variability (HRV) is a reliable technique to evaluate autonomic activity and shows marked changes across a night of sleep. Previous nighttime sleep findings report changes in HRV during non-rapid eye movement sleep (NREM), which have been associated with cardiovascular health benefits. Daytime sleep, however, has been linked with both positive and negative cardiovascular outcomes. Yet, no studies have directly compared HRV profiles during an ecologically-valid daytime nap in healthy, well-rested adults to that of nighttime sleep. Using a within-subjects design, 32 people took a daytime nap and slept overnight in the lab at least one week apart; both sleep sessions had polysomnography, including electrocardiography (ECG), recorded. We measured inter-beat intervals (RR), total power (TP), low frequency power (LF; .04-.15 Hz), and high frequency power (HF; .15-.40 Hz) components of HRV during NREM and rapid eye movement (REM) sleep. Compared to the nap, we found longer RR intervals and decreased heart rate during the night for both Stage 2 and SWS and increased TP, LF and HF power during nighttime Stage 2 sleep only; however, no differences in the LFHF ratio or normalized HF power were found between the nap and the night. Also, no differences in REM sleep between the nap and night were detected. Similar relationships emerged when comparing the nap to one cycle of nighttime sleep. These findings suggest that longer daytime naps, with both SWS and REM, may provide similar cardiovascular benefits as nocturnal sleep. In light of the on-going debate surrounding the health benefits and/or risks associated with napping, these results suggest that longer daytime naps in young, healthy adults may support cardiac down-regulation similar to nighttime sleep. In addition, napping paradigms may serve as tools to explore sleep-related changes in autonomic activity in both healthy and at-risk populations.

The effect of sex and menstrual phase on memory formation during a nap.

Memory formation can be influenced by sleep and sex hormones in both men and women, and by the menstrual cycle in women. Though many studies have shown that sleep benefits the consolidation of memories, it is not clear whether this effect differs between men and women in general or according to menstrual phase in women. The present study investigated the effect of sex and menstrual cycle on memory consolidation of face-name associations (FNA) following a daytime nap. Recognition memory was tested using a face-name paired associates task with a polysomnographic nap between morning and evening testing. Seventeen healthy women (age: 20.75 (1.98) years) were studied at two time points of their menstrual cycles, defined from self-report and separated by 2weeks (perimenses: -5days to +6days from the start of menses, and non-perimenses: outside of the perimenses phase), and compared with eighteen healthy men (age: 22.01 (2.91) years). Regardless of menstrual phase, women had better pre-nap performance than men. Further, menstrual phase affected post-nap memory consolidation, with women showing greater forgetting in their perimenses phase compared with their non-perimenses phase and men. Interestingly, post-nap performance correlated with electrophysiological events during sleep (slow oscillations, spindles, and temporal coupling between the two), however, these correlations differed according to menstrual phase and sex. Men's performance improvement was associated with the temporal coupling of spindles and slow oscillations (i.e., spindle/SO coincidence) as well as spindles. Women, however, showed an association with slow oscillations during non-perimenses, whereas when they were in their perimenses phase of their cycle, women appeared to show an association only with sleep spindle events for consolidation. These findings add to the growing literature demonstrating sex and menstrual phase effects on memory formation during sleep.

A comparison of abdominal muscle thickness changes after a lifting task in subjects with and without chronic low-back pain.

OBJECTIVE: Using ultrasound imaging, the abdominal muscles' response to the back extensor muscle fatigue was assessed in subjects with chronic low-back pain (CLBP). BACKGROUND: Lumbar muscle fatigue is a common occurrence among workers. Alteration in motor coordination is one consequence of muscular fatigue. According to previous studies, CLBP subjects use their back and abdominal muscles in different ways, but questions remain about abdominal muscle responses to back muscle fatigue in CLBP patients. METHOD: Thirteen CLBP patients and 15 healthy subjects participated in this study. The thickness of abdominal muscles-including transverse abdominis (TrA), internal oblique abdominis (IO), and external oblique abdominis (EO) muscles-was measured in standing position with and without axial loads before and after a lifting fatigue task. RESULTS: The results reveal a significant difference for the main effects of group on percentage of change in TrA thickness (F = 8.9, p = .004). Percentage of change in thickness of TrA was 10% greater in the CLBP group. Although IO thickness displayed greater percentage of change in the CLBP group, the difference between groups was not significant. CONCLUSION: Abdominal muscle behavior changes with back-muscle fatigue in both healthy and CLBP subjects, but responses were more exaggerated in CLBP patients. APPLICATION: Ultrasound imaging technique can provide critical information about the effect of fatigue on spinal muscle activation and consequently about the stability of the spine. As a more applicable and easy technique, ergonomists can use ultrasound imaging in musculoskeletal system assessment in worker populations in future studies.