Dynamic coupling between the central and autonomic nervous systems during sleep: A review

Abstract

Sleep is characterized by coordinated cortical and cardiac oscillations reflecting communication between the central (CNS) and autonomic (ANS) nervous systems. Here, we review fluctuations in ANS activity in association with CNS-defined sleep stages and cycles, and with phasic cortical events during sleep (e.g., arousals, K-complexes). Recent novel analytic methods reveal a dynamic organization of integrated physiological networks during sleep and indicate how multiple factors (e.g., sleep structure, age, sleep disorders) affect "CNS-ANS coupling". However, these data are mostly correlational and there is a lack of clarity of the underlying physiology, making it challenging to interpret causality and direction of coupling. Experimental manipulations (e.g., evoking K-complexes or arousals) provide information on the precise temporal sequence of cortical-cardiac activity, and are useful for investigating physiological pathways underlying CNS-ANS coupling. With the emergence of new analytical approaches and a renewed interest in ANS and CNS communication during sleep, future work may reveal novel insights into sleep and cardiovascular interactions during health and disease, in which coupling could be adversely impacted.

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).…”

Cardiac autonomic dynamics during sleep are lost in patients with TIA and stroke

“…In physiological conditions, cardiac autonomic control fluctuates during sleep stages, with a predominant vagal modulation during NREM sleep and a sympathetic overactivity during REM (Benarroch, ; Busek et al., ; Ferri et al., ; Rossi et al., ; Tobaldini, Nobili et al., ; de Zambotti et al., ). However, data on autonomic control during sleep after acute ischaemic stroke are lacking.…”

“…Central control of the autonomic nervous system implicates a widespread cortical and subcortical network, including the bilateral insular cortex, anterior cingulate gyrus, amygdala and hypothalamus (Beissner, Meissner, Bär, & Napadow, ; Benarroch, ; Hilz et al., ; Ozdemir & Hachinski, ; Rossi, Santarnecchi, Valenza, Ulivelli, & Rossi, ; Verberne & Owens, ; de Zambotti, Trinder, Silvani, Colrain, & Baker, ). The insula has a prominent role and stroke affecting the insula (especially on the right side) is associated with elevated cardiac troponin, electrocardiogram (ECG) changes (altered repolarization phase and prolonged QTc) and cardiac arrhythmias (Abboud, Berroir, Labreuche, Orjuela, & Amarenco, ; Christensen, ; Colivicchi, Bassi, Santini, & Caltagirone, ; De Raedt et al., ).…”

Autonomic regulation during sleep and wakefulness: a review with implications for defining the pathophysiology of neurological disorders

“…Collectively, these pathways activate the cortex and contribute to the low-voltage, high-frequency electroencephalogram (EEG) pattern occurring during wakefulness. Glutamatergic neurons in the parabrachial nucleus of the rostral pons are preferentially active during wakefulness [15, 16]; projections from the parabrachial nucleus to the NTS may represent a mechanism for adjusting BP between wakefulness and sleep. Increased parabrachial nucleus activity may inhibit the baroreflex [17–19], representing a mechanism for maintaining higher BP during wakefulness compared with sleep.…”