K-Complexes: Interaction between the Central and Autonomic Nervous Systems during Sleep

Zambotti, Massimiliano de; Ar, Willoughby; Pl, Franzen; Db, Clark; Baker, Fiona C.; Im, Colrain

doi:10.5665/sleep.5770

Cited by 36 publications

(63 citation statements)

References 60 publications

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“…We then analyzed heart rate activity within the ±5 second window following the SO downstate. During Stage 2 sleep, this window was characterized by an acceleration in heart rate following by a deceleration (Figure 1), in agreement with previous studies (de Zambotti, et al, 2016). The detected SO events during stable Stage 2 bins, co-occurred with a peak in heart rate, which was 12.09±1.48 % above the average Stage 2 heart rate.…”

Section: Resultssupporting

confidence: 91%

Timing between cortical slow oscillations and heart rate bursts during sleep predicts perceptual speed, but not offline consolidation

Naji

Krishnan

McDevitt

et al. 2018

Preprint

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Central and autonomic nervous system activity are coupled during sleep. Cortical slow oscillations (SOs, <1Hz) 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 perceptual speed and learning on a texture discrimination task, by testing subjects before and after a nap. The coherence of SO-HR events during sleep strongly correlated with an individual’s perceptual 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 reliable 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.Significance StatementStudies show that autonomic and central nervous system activity is coupled. For example, increases in heart rate follow cortical slow oscillations during sleep. However, the functional significance of this coupling for cognition is not understood. In three experimental visits, we show that the timing between these sleep events (the peak-to-peak delay between the slow oscillation and the heart rate burst) is highly correlated with waking perceptual processing speed. This reliable individual difference measure may be a useful marker of generalized processing speed.

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Section: Resultssupporting

confidence: 91%

Timing between cortical slow oscillations and heart rate bursts during sleep predicts perceptual speed, but not offline consolidation

Naji

Krishnan

McDevitt

et al. 2018

Preprint

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“…It's been hypothesized that in the case of the K-complex, the recruited synchronized EEG response acts as a mechanism to decrease cortical arousal, suggesting that the heart-rate acceleration (tachycardia, or HR bursts) can be viewed as peripheral response of arousal from sleep. Taken together, the subsequent heart-rate deceleration that de Zambotti et al (2016) showed and the surge of HF that Naji et al (2019) and the current study found may reflect a feedback effect of arousal showing an inertial effect once the arousal stimulus is removed. Alternatively, arousal and post-arousal periods may modulate the autonomic system reflecting the activation-deactivation of neuronal oscillations intrinsically regulated by the cyclic arousability of the sleepy brain (Schnall et al, 1999;Sforza et al, 1999;Ferri et al, 2000).…”

Section: Heart-brain Interaction During Sleep: Findings and Potentialsupporting

confidence: 61%

“…In recent years, a number of studies have explored the association between central and autonomic activity during sleep, offering promising new perspectives to understand brain-body interplay in humans (Brandenberger et al 2001a;Thomas et al 2014;Ako et al 2003). For example, a recent study investigated the relationship between cardiac activity and K-complexes (KC; 0.5-1 Hz)-a positive-negative-positive waveform during Stage 2 sleep similar to slow oscillations-and demonstrated that KCs were associated with a biphasic cardiac response, with a marked heart rate acceleration followed by a gradual deceleration (de Zambotti et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Autonomic/Central Coupling Boosts Working Memory in Healthy Young Adults

Chen

Whitehurst²,

Naji³

et al. 2020

Preprint

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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 (Kuriyama et al. 2008a;Zinke, Noack, and Born 2018), with WM improvement correlated with slow wave activity (SWA; 0.5-1Hz) during slow wave sleep (SWS) (Sattari et al. 2019;Pugin et al. 2015;Ferrarelli et al. 2019). A different body of literature has suggested an important role for autonomic activity during wake for WM (Hansen et al. 2004;Mosley, Laborde, and Kavanagh 2018). A recent study from our group reported that the temporal coupling of autonomic and central events (ACEs) during sleep was associated with memory consolidation (Naji et al. 2019). We found that heart rate bursts (HR bursts) during non-rapid eye movement (NREM) sleep are accompanied by increases in SWA and sigma (12-15Hz) 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 may 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 (with electroencephalography (EEG) and electrocardiography (ECG)) or wake 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.

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“…Research has consistently shown that a period of non-rapid eye movement (NREM) sleep yields greater memory retention of declarative memories (e.g., explicit, episodic memories) than a comparable period of REM sleep or waking activity 1 . Several EEG features of NREM sleep have been linked with memory consolidation, with most studies focusing on spectral power in the slow wave activity (SWA, 0.5-4Hz) and sigma (12)(13)(14)(15) Hz) bands, or specific events including hippocampal sharp wave-ripples (150-250 Hz) 2 , cortical slow oscillations (SO, 0.5-1 Hz), and thalamic sleep spindles 3 . In fact, co-occurring SOs and sigma/spindles may be a key mechanism of memory consolidation during sleep 4 .…”

Section: Introductionmentioning

confidence: 99%

“…Prior work hints at a possible coordination between central features and autonomic activity. For example, auditory-evoked K-complexes were associated with increased heart rate 15 and have been shown to appear frequently 250 and 650 msec after the onset of the P wave in ECG 16 . Furthermore, the QRS complex of ECG has been shown to modulate sleep spindle phases 17 .…”

Section: Introductionmentioning

confidence: 99%

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

Naji

McDevitt

Bazhenov

et al. 2017

Preprint

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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 seconds and predominated in non-rapid-eye-movement sleep (NREM). Using event-based analysis of NREM sleep, we found an increase in delta (0.5-4Hz) and sigma (12-15Hz) power and an elevated density of slow oscillations (0.5-1Hz) about 5 secs 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.

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K-Complexes: Interaction between the Central and Autonomic Nervous Systems during Sleep

Cited by 36 publications

References 60 publications

Timing between cortical slow oscillations and heart rate bursts during sleep predicts perceptual speed, but not offline consolidation

Timing between cortical slow oscillations and heart rate bursts during sleep predicts perceptual speed, but not offline consolidation

Autonomic/Central Coupling Boosts Working Memory in Healthy Young Adults

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

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