Cardiac autonomic modulation and sleepiness: Physiological consequences of sleep deprivation due to 40 h of prolonged wakefulness

Highlights

• Sleep deprivation by constant routine (CR) changes sleep during the recovery night.

• Autonomic nervous system (ANS) sympathovagal balance increases at the CR 2nd day.

• EEG spectral α band attenuation reveals enhanced drowsiness at the CR 2nd day.

• Subjective sleepiness and unintended sleep episodes increase during CR 2nd day.

• Sleep deprivation affects ANS during CR wakefulness and subsequent sleep.

Abstract

The autonomic nervous system (ANS) is modulated by sleep and wakefulness. Noninvasive assessment of cardiac ANS with heart rate variability (HRV) analysis is a window for monitoring malfunctioning of cardiovascular autonomic modulation due to sleep deprivation.

This study represents the first investigation of dynamic ANS effects and of electrophysiological and subjective sleepiness, in parallel, during 40 h of prolonged wakefulness under constant routine (CR) conditions. In eleven young male healthy subjects, ECG, EEG, EOG, and EMG chin recordings were performed during baseline sleep, during 40 h of sleep deprivation, and during recovery sleep. After sleep deprivation, slow-wave sleep and sleep efficiency increased, whereas HRV – global variability and HRV sympathovagal balance – was reduced (all p < 0.05). Sleep-stage-dependent analysis revealed reductions in the sympathovagal balance only for NREM sleep stages (all p < 0.05). Comparison of the daytime pattern of CR day one (CR baseline) with that of CR day two (CR sleep deprivation) disclosed an increase in subjective sleepiness, in the amount of unintended sleep, and in HRV sympathovagal balance, with accompaniment by increased EEG alpha attenuation (all p < 0.05). Circadian rhythm analysis revealed the strongest influence on heart rate, with less influence on HRV sympathovagal balance. Hour-by-hour analysis disclosed the difference between CR sleep deprivation and CR baseline for subjective sleepiness at almost every single hour and for unintended sleep particularly in the morning and afternoon (both p < 0.05). These findings indicate that 40 h of prolonged wakefulness lead in the following night to sleep-stage-dependent reduction in cardiac autonomic modulation. During daytime, an increased occurrence of behavioral and physiological signs of sleepiness was accompanied by diminished cardiac autonomic modulation. The observed changes are an indicator of autonomic stress due to sleep deprivation — which, if chronic, could potentially increase cardiovascular risk.

Introduction

The autonomic nervous system (ANS) plays a major role in the regulation of sleep and wakefulness. Measurement of heart rate variability (HRV) has shown its ability to reflect the state of the cardiac ANS as a noninvasive measure [1]. The transition from pre-sleep wakefulness to non-rapid eye movement (NREM) sleep leads to reduced sympathetic and to increased vagal predominance of the cardiac ANS, as indicated by a fall in heart rate and an increased HRV [2], [3]. Furthermore, the occurrence of rapid eye movement (REM) sleep gives rise to sympathetic activation, which is demonstrated by increased heart rate [4] and by decreased HRV components [4], [5] in comparison to NREM sleep — although values may remain above wakefulness levels [4]. In addition, circadian system influence on cardiac ANS, independent of sleep stage, is present: which results in decreased heart rate [4] and increased HRV [5] in the morning hours.

The interaction of the sleep–wake state and circadian timing with the cardiac ANS has attained increased importance: indeed, sleep loss, sleep disruption, and sleep restriction are today extensively present not only in conjunction with certain sleep disorders, but also with a number of conditions related to shift work.

A constant-routine (CR) setting enables the study of effects of acute sleep deprivation on the cardiac ANS in highly controlled manner: not only by avoiding external time cues but also by monitoring other factors that influence cardiac autonomic modulation and sleepiness such as food intake [6] and illuminance [7]. Viola et al. [5] studied participants under 40-hour CR conditions and determined that HRV was diminished during recovery sleep after CR-related sleep deprivation. Analysis of these results obtained during CR daytime revealed a decrease in HRV due to sleep deprivation — but with less intensity than during sleep. Zhong et al. [8] found, in persons with over 36 h of sleep deprivation, a progressive increase during daytime in sympathetic, and a decrease in parasympathetic cardiac autonomic modulation. This was demonstrated by reduced HRV values in the frequency domain for healthy participants while test persons performed a cognitive task repetitively. In contrast, Pagani et al. [9] could not find increased sympathetic drive expressed during daytime by diminished HRV values after one night of sleep deprivation. Another investigation under CR conditions revealed a correlation of HRV spectral values with psychomotor vigilance test performance during sleep deprivation [10].

To investigate the effect of acute sleep deprivation on HRV and on sleepiness at various times of day, and on HRV during post-recovery sleep, we performed a study under CR conditions. Our aim was to investigate to what extent a prolonged wakefulness period under strictly controlled conditions influences cardiac autonomic modulation, and in what manner this behavior is related during daytime to quantitative EEG parameters, to subjective ratings of sleepiness, and – during the subsequent recovery night – to the various stages of sleep. HRV and EEG were recorded continuously and analyzed for pre-CR baseline sleep, CR-related sleep deprivation, and post-CR recovery sleep.