Causality of cortical and cardiovascular activity during cyclic alternating pattern in non-rapid eye movement sleep

Abstract

The dynamic interplay between central and autonomic nervous system activities plays a pivotal role in orchestrating sleep. Macrostructural changes such as sleep-stage transitions or phasic, brief cortical events elicit fluctuations in neural outflow to the cardiovascular system, but the causal relationships between cortical and cardiovascular activities underpinning the microstructure of sleep are largely unknown. Here, we investigate cortical–cardiovascular interactions during the cyclic alternating pattern (CAP) of non-rapid eye movement sleep in a diverse set of overnight polysomnograms. We determine the Granger causality in both 507 CAP and 507 matched non-CAP sequences to assess the causal relationships between electroencephalography (EEG) frequency bands and respiratory and cardiovascular variables (heart period, respiratory period, pulse arrival time and pulse wave amplitude) during CAP. We observe a significantly stronger influence of delta activity on vascular variables during CAP sequences where slow, low-amplitude EEG activation phases (A1) dominate than during non-CAP sequences. We also show that rapid, high-amplitude EEG activation phases (A3) provoke a more pronounced change in autonomic activity than A1 and A2 phases. Our analysis provides the first evidence on the causal interplay between cortical and cardiovascular activities during CAP. Granger causality analysis may also be useful for probing the level of decoupling in sleep disorders. This article is part of the theme issue ‘Advanced computation in cardiovascular physiology: new challenges and opportunities’.

Brain and brain-heart Granger causality during wakefulness and sleep

“…An example is the study by Hartmann et al, where GC was used to study the brain-heart interactions during the cyclic alternating pattern of non-rapid eye movement sleep (Hartmann et al, 2021). According to the authors, their study provided the first evidence on the causal interplay between cortical and cardiovascular activities during cyclic alternating pattern.…”

“…Despite the popularity of GC in neuroscience applications, including in the study of physiological states similar to sleep, such as anesthesia ( Nicolaou et al, 2012 ; Pullon et al, 2020 ), there are only a handful of studies applying it in sleep. An example is the study by Hartmann et al, where GC was used to study the brain-heart interactions during the cyclic alternating pattern of non-rapid eye movement sleep ( Hartmann et al, 2021 ). According to the authors, their study provided the first evidence on the causal interplay between cortical and cardiovascular activities during cyclic alternating pattern .…”

Sleep apnea pathophysiology

“…SA and its associated causes are quite hazardous to one's health, most notably in patients with pre-existing cardiac and bronchopulmonary pathology. Three hundred to four hundred thousand of these patients die during sleep each year in the USA alone [2,[88][89][90][91]. We have already discussed SIDS and its impact on infants.…”

Advanced computation in cardiovascular physiology: new challenges and opportunities

“…The proposed framework relies on a maximal information coefficient analysis between nonlinear multiscale features derived from electroencephalographic spectra and from an inhomogeneous point-process model for heartbeat dynamics. Hartmann et al [15] study the dynamic interplay between the central and autonomic nervous system activity during sleep. Focusing on non-rapid eye movement sleep stages, they show the causal interplay between cortical and cardiovascular activity during cyclic alternating patterns.…”