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

Abstract

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 (0.5-4 Hz) and sigma (12-15 Hz) power and an elevated density of slow oscillations (0.5-1 Hz) 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.

Autonomic/Central Coupling Boosts Working Memory in Healthy Young Adults

“…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).…”

“…Though the functional significance of CNS-ANS couplings during sleep is only beginning to be explored, we hypothesize that ACE activity may play an important role in hippocampalprefrontal cognitive enhancement. Results from our group have shown ACE (SWA and spindles) contributions to long-term, episodic memory(Naji et al 2019), as well as WM gains (SWA, current study). In addition, recent studies implicate frontal SWA with improvement in WM, a cognitive ability strongly supported by the prefrontal cortex(Wager and Smith 2003).…”

BOLD signatures of sleep

“…Nonetheless, BOLD signal results from a complex interplay between neuronal and vascular events (Friston et al, 2000, Obrig et al, 2000, Logothetis et al, 2001, Shmueli et al, 2007, Bianciardi et al, 2009, Webb et al, 2013, Yuan et al, 2013, Rayshubskiy et al, 2014, Chang et al, 2016, Tong et al, 2016, where oscillations in the signal could be affected by vasomotion (~0.1 Hz intrinsic fluctuations in arteriole diameter) or by autonomous nervous system activity (cardiac or respiratory activity). Notably, dynamic coupling between cardiac activity and spindle or slow wave activity has been reported during human sleep (Lechinger et al, 2015, Lin et al, 2016, Menson et al, 2016, de Zambotti et al, 2018, which predicts the post-sleep improvements in cognitive performances (Naji et al, 2018), consistent with the visceral influences on brain and behavior observed during wake (Critchley andHarrison, 2013, Park et al, 2014). Moreover, vasomotion is entrained by neuronal oscillations of similar frequency (Mateo et al, 2017).…”

Procedural memory consolidation is associated with heart rate variability and sleep spindles

“…Although sleep studies generally implement heart rate measurements, few have analyzed its association with memory. Using daytime nap protocols, Whitehurst, Cellini, Mcdevitt, Duggan, and Mednick () found HF during rapid eye movement (REM) to be positively associated with performance improvement on a declarative remote associates test, whereas Naji, Krishnan, Mcdevitt, Bazhenov, and Mednick () found HF during N2 to be positively correlated with improvement on a declarative face–name association task. Investigations for full‐night sleep protocols as well as the procedural memory domain are as of yet lacking, yet longer sleep duration may provide a clearer insight into HRV during sleep and its relation to OMC.…”

“…Results indicate that daytime naps prevent the memory deterioration observed during an identical period of daytime wakefulness, whereas full‐night sleep may result in significant improvements in performance (van Schalkwijk et al., ). Following the recent studies on HRV and OMC during a daytime nap (Naji et al., ; Whitehurst et al., ), the present study re‐analyzed the procedural dataset of the full‐night study to investigate long‐term (7 days) memory performance changes and associations between SpA and HRV as potential mediators of OMC that are underrepresented in the current literature. Participants were trained on a procedural mirror‐tracing task for which short‐ (12 hr) and long‐term (7 days) performance changes were evaluated.…”