Elsevier

Neurophysiologie Clinique

Volume 50, Issue 5, October 2020, Pages 339-343
Neurophysiologie Clinique

Original article
Spindles insufficiency in sleepwalkers’ deep sleep

https://doi.org/10.1016/j.neucli.2020.08.003Get rights and content

Abstract

Objectives

Sleepwalkers have consistently shown N3 sleep discontinuity, especially after sleep deprivation. In healthy subjects, sleep spindles activity has been positively correlated to sleep stability. We aimed to compare spindles density during N3 sleep between sleepwalkers and healthy controls.

Methods

Two cohorts of 10 and 21 adult sleepwalkers respectively controlled with 10 and 18 healthy volunteers underwent one baseline and one recovery sleep recording after 38 h (cohort 1) and 25 h (cohort 2) of sleep deprivation. For the two recordings, we performed an automatic detection of spindles (11–16 Hz) from EEG signal during N3 sleep, restricted to the first sleep cycle and repeated for all cycles. For better interpretation of results, we extended the analysis to N2 sleep and we also measured the density of slow waves oscillation (SWO) (0.5–4 Hz) during the same periods.

Results

Compared to controls, sleepwalkers showed significantly lower spindle densities during N3 sleep considering the first sleep cycle (both cohorts) or all cycles (cohort 1). SWO densities did not differ (cohort 1) or were lower (cohort 2) for sleepwalkers. The effect of sleep deprivation did not interact with the effect of group on spindles and SWO densities.

Conclusion

This work suggests that the instability of N3 sleep inherent to sleepwalkers may be underpinned by a specific alteration of spindles activity.

Introduction

Sleepwalking is currently conceptualized as the clinical manifestation of partial arousals mostly emerging from stage 3 sleep (N3) [15]. Sleepwalkers’ N3 sleep is characterized by instability: more awakenings and higher awakening index during N3, lower slow-wave activity (SWA), as well as an increased cyclic alternating pattern (CAP) rate [5]. Moreover, sleep deprivation usually increases the frequency of sleepwalking episodes [12].

In mice, the manipulation of SK2 channels enhanced spindles activity and improved sleep stability under noisy conditions [14]. In humans, spindles density during both N2 and N3 stages is correlated to sleep stability against noise exposure [3]. An impaired upkeep of sufficient spindles activity during the deepening of non-rapid-eye-movement (NREM) sleep may thus underlie the reported N3 discontinuity in sleepwalkers.

The spindles activity during N3 sleep has already been investigated in a controlled cohort of eleven individuals suffering from a NREM parasomnia (five from sleepwalking and six from night terrors) [4]. The spindles density during N3 sleep was lower in parasomniacs but without a reliably statistical significance across the sleep cycles. Authors explained these results by the increase of slow waves, correlating spindles and slow waves inversely. However, only the percentage of time occupied by the delta band during N3 sleep tended to be slightly increased in parasomniacs, whereas EEG power density during NREM sleep did not differ significantly.

We hypothesized that sleepwalkers have a N3 sleep instability linked to a spindles insufficiency. We compared spindles density during N3 sleep between sleepwalkers and healthy volunteers. To rightly interpret the results, we also analyzed N2 sleep and compared slow wave oscillation (SWO) densities between sleepwalkers and controls.

Section snippets

Subjects

Sleepwalkers come from two cohorts that have been already studied by our group [6], [7]. The first cohort comprised 10 adult sleepwalkers (male = 3; median age = 23.5 years; min–max = 20–34 years) and 10 healthy volunteers (male = 3; median age = 25.5 years; min–max = 21–32 years). The second cohort comprised 21 adult sleepwalkers (male = 10; median age = 27 years; min–max = 18–44 years) and 18 healthy volunteers (male = 8, median age = 26 years; min–max = 20–45 years). All participants were recruited from 1998 to

Standard sleep measures

For cohort 1, basic PSG measures have been previously reported [7]. In brief, sleepwalkers exhibited a significant higher number of awakenings from N3 (baseline: 3.7 ± 0.6 vs 1.0 ± 0.6; recovery sleep: 5.0 ± 1.1 vs 0.7 ± 1.2, p < 0.001) and a significant increased awakening index from N3 (baseline: 2.8 h–1 ± 0.5 vs 0.8 h–1 ± 0.5, recovery sleep: 1.9 h–1 ± 0.4 vs 0.2 h–1 ± 0.5, p < 0.001) compared to controls. For cohort 2, basic PSG measures are reported in Table 1. Compared to controls, sleepwalkers showed a higher

Discussion

This work reveals that sleepwalkers exhibit a lower N3 spindles density than healthy controls. The same trend was replicated in the second cohort, reaching the statistical significance only for the first sleep cycle.

The working hypothesis was that sleep spindles might promote sleep stability by disengaging the cortex from sensorial inputs during NREM sleep, in particular from auditory stimuli [2], [14]. Especially since sleepwalkers exhibited an abnormal vulnerability to noise during N3 sleep

Acknowledging

This research was supported by the Canadian Institutes of Health Research (grant # MOP 49515) to AZ and by the Fonds de Recherche du Québec-Santé to AD. NC received graduate fellowship support from a partnership between Association des Chefs de Service Hospitaliers de Nancy and Groupe Pasteur Mutualité.

Disclosure of interest

AD received research grants from GSK, Novartis pharma, Jazz Pharma and Flamel Ireland Inc, as well as honoraria from speaking engagements from UCB and Paladin labs. The other authors have no conflict of interest.

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