Research Article: The Role of the Suprachiasmatic Nucleus in Cardiac Autonomic Control during Sleep

Date Published: March 24, 2016

Publisher: Public Library of Science

Author(s): S. D. Joustra, R. H. Reijntjes, A. M. Pereira, G. J. Lammers, N. R. Biermasz, R. D. Thijs, Raffaele Ferri.

http://doi.org/10.1371/journal.pone.0152390

Abstract

The suprachiasmatic nucleus (SCN) may play an important role in central autonomic control, since its projections connect to (para)sympathetic relay stations in the brainstem and spinal cord. The cardiac autonomic modifications during nighttime may therefore not only result from direct effects of the sleep-related changes in the central autonomic network, but also from endogenous circadian factors as directed by the SCN. To explore the influence of the SCN on autonomic fluctuations during nighttime, we studied heart rate and its variability (HRV) in a clinical model of SCN damage.

Fifteen patients in follow-up after surgical treatment for nonfunctioning pituitary macroadenoma (NFMA) compressing the optic chiasm (8 females, 26–65 years old) and fifteen age-matched healthy controls (5 females, 30–63 years) underwent overnight ambulatory polysomnography. Eleven patients had hypopituitarism and received adequate replacement therapy. HRV was calculated for each 30-second epoch and corrected for sleep stage, arousals, and gender using mixed effect regression models.

Compared to controls, patients spent more time awake after sleep onset and in NREM1-sleep, and less in REM-sleep. Heart rate, low (LF) and high frequency (HF) power components and the LF/HF ratio across sleep stages were not significantly different between groups.

These findings suggest that the SCN does not play a dominant role in cardiac autonomic control during sleep.

Partial Text

Sleep exerts major effects on cardiac autonomic control. For example, compared to slow-wave sleep, rapid eye movement sleep is associated with increased heart rate (HR) and low-frequency power of HR variability (HRV), and decreased high-frequency power [1]. The suprachiasmatic nucleus (SCN) is the critical relay of the diurnal sleep-wake regulation [2]. It may also play an important role in central autonomic control, as tracing studies demonstrated that SCN neurons project to the paraventricular nucleus and connect with parasympathetic and sympathetic relay stations in the brainstem and spinal cord [3,4]. Accordingly, SCN lesions in rat reduced the HR decrease during resting periods [5]. Furthermore, humans showed diurnal rhythms of HR and HRV independent of sleep stage in a constant routine protocol [6]. Consequently, it may well be argued that cardiac autonomic control during nighttime not only results from direct effects of sleep-related changes in the central autonomic network, but also from endogenous circadian factors as directed by the SCN.

We studied the role of the SCN in sleep-related cardiac autonomic control in a cohort of NFMA patients and healthy age-matched controls and did not identify major autonomic alterations. Our results suggest that modulation of sleep-related cardiac autonomic control is predominantly linked to sleep processes with a subordinate role for the SCN. This is supported by experiments of shifting the sleep period, inducing a concomitant shift in the diurnal variation of HRV [18], in contrast to other circadian parameters such as the melatonin peak and core body temperature nadir that showed respectively no shift and a biphasic curve in similar experiments [19]. Furthermore, preservation of the effects of sleep on HR in patients with bilateral carotid tumour resection also suggests that these alterations are predominantly generated through central, non-baroreflex mediated pathways [16]. In rats a bidirectional relationship has been demonstrated between sleep processes and SCN activity [20]. Sleep processes might therefore influence cardiac control through altering SCN activity. In view of our findings it seems however likely that other central circuitries linking sleep and cardiac autonomic control, e.g. the hypothalamic nuclei [21, 22], outweigh this influence.

 

Source:

http://doi.org/10.1371/journal.pone.0152390