Nico Romeijn

Sleep deprivation leads to a loss of functional connectivity in frontal brain regions

BackgroundThe restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connectivity characteristics in different brain regions, we performed a within-subject study of resting state brain activity using the graph theory framework adapted for the individual electrode level.In balanced order, we obtained high-density resting state electroencephalography (EEG) in 8 healthy participants, during a day following normal sleep and during a day following total sleep deprivation. We computed topographical maps of graph theoretical parameters describing local clustering and path length characteristics from functional connectivity matrices, based on synchronization likelihood, in five different frequency bands. A non-parametric permutation analysis with cluster correction for multiple comparisons was applied to assess significance of topographical changes in clustering coefficient and path length.ResultsSignificant changes in graph theoretical parameters were only found on the scalp overlying the prefrontal cortex, where the clustering coefficient (local integration) decreased in the alpha frequency band and the path length (global integration) increased in the theta frequency band. These changes occurred regardless, and independent of, changes in power due to the sleep deprivation procedure.ConclusionsThe findings indicate that sleep deprivation most strongly affects the functional connectivity of prefrontal cortical areas. The findings extend those of previous studies, which showed sleep deprivation to predominantly affect functions mediated by the prefrontal cortex, such as working memory. Together, these findings suggest that the restorative effect of sleep is especially relevant for the maintenance of functional connectivity of prefrontal brain regions.

Sleep, vigilance, and thermosensitivity

The regulation of sleep and wakefulness is well modeled with two underlying processes: a circadian and a homeostatic one. So far, the parameters and mechanisms of additional sleep-permissive and wake-promoting conditions have been largely overlooked. The present overview focuses on one of these conditions: the effect of skin temperature on the onset and maintenance of sleep, and alertness. Skin temperature is quite well suited to provide the brain with information on sleep-permissive and wake-promoting conditions because it changes with most if not all of them. Skin temperature changes with environmental heat and cold, but also with posture, environmental light, danger, nutritional status, pain, and stress. Its effect on the brain may thus moderate the efficacy by which the clock and homeostat manage to initiate or maintain sleep or wakefulness. The review provides a brief overview of the neuroanatomical pathways and physiological mechanisms by which skin temperature can affect the regulation of sleep and vigilance. In addition, current pitfalls and possibilities of practical applications for sleep enhancement are discussed, including the recent finding of impaired thermal comfort perception in insomniacs.

Manipulation of skin temperature improves nocturnal sleep in narcolepsy

Objective: Besides excessive daytime sleepiness, disturbed nocturnal sleep is a major complaint of patients with narcolepsy. Previously, alterations in skin temperature regulation in narcoleptic patients have been shown to be related to increased sleepiness. This study tests the hypothesis that direct control of nocturnal skin temperature might be applied to improve the disturbed sleep of narcoleptic patients. Methods: Participants were eight patients (five males) diagnosed as having narcolepsy with cataplexy according to the ICSD-2 criteria, mean (SD) age 28.6 (6.4) years, range 18–35 years. During two nights, sleep was recorded polysomnographically while proximal and distal skin temperature were manipulated using a comfortable thermosuit that induced skin temperature to cycle slowly with an amplitude of only 0.4°C within the comfortable range normally observed during sleep. Logistic regression was used to evaluate the effect of skin temperature manipulation on the probability of occurrence of different sleep stages and nocturnal wakefulness. Results: Proximal skin warming significantly suppressed wakefulness and enhanced slow wave sleep (SWS). In contrast, distal skin warming enhanced wakefulness and stage 1 sleep at the cost of SWS and REM sleep. The optimal combination of proximal skin warming and distal skin cooling led to a 160% increase in SWS, a 50% increase in REM sleep and a 68% decrease in wakefulness, compared with the least beneficial combination of proximal skin cooling and distal skin warming. Interpretation: Subtle skin temperature manipulations under controlled conditions significantly improved the typical nocturnal sleep problems in narcolepsy.

Correlated Fluctuations of Daytime Skin Temperature and Vigilance

Skin temperature shows spontaneous ultradian fluctuations during everyday-life wakefulness. Previous work showed that mild manipulations of skin temperature affect human sleep and vigilance, presumably by influencing neuronal systems involved in both thermal sensing and arousal regulation. We therefore examined whether fluctuations in skin temperature are associated with those in vigilance level under conditions similar to everyday-life situations requiring sustained attention. Eight healthy participants (30.1 ± 8.1 years, M ± SD) participated in a 2-day protocol, during which vigilance and skin temperature were assessed 4 times per day in a silent, dimly lit, temperature-controlled room. Vigilance was assessed by measuring reaction speed and lapses on a novel sustained vigilance task specifically designed to increase lapse rate and range of reaction times. Skin temperature was sampled at 30-second intervals from 3 locations: distal, intermediate, and proximal temperatures were obtained from the middle finger (Tfinger ), the wrist (Twrist), and the infraclavicular area (Tchest), respectively. Furthermore, 3 distal to proximal gradients were calculated. Mixed-effect regression analyses were used to evaluate the association of the fluctuations in temperatures and gradients and those in response speed and lapse probability. Especially the spontaneous fluctuations in proximal temperature were negatively associated with fluctuations in response speed and positively with lapse rate. If individual Tchest temperature ranges were classified into 10 deciles, they accounted for 23% of the variance in response speed and 11% of the variance in lapse rate. The findings indicate coupling between the spontaneous fluctuations in skin temperature and vigilance during the day and are compatible with the hypothesis of overlap in brain networks involved in the regulation of temperature and vigilance. From an applied point of view, especially proximal skin temperature assessment may be of use in vigilance monitoring.

Does sleep restore the topology of functional brain networks

Previous studies have shown that healthy anatomical as well as functional brain networks have small‐world properties and become less optimal with brain disease. During sleep, the functional brain network becomes more small‐world‐like. Here we test the hypothesis that the functional brain network during wakefulness becomes less optimal after sleep deprivation (SD). Electroencephalography (EEG) was recorded five times a day after a night of SD and after a night of normal sleep in eight young healthy subjects, both during eyes‐closed and eyes‐open resting state. Overall synchronization was determined with the synchronization likelihood (SL) and the phase lag index (PLI). From these coupling strength matrices the normalized clustering coefficient C (a measurement of local clustering) and path length L (a measurement of global integration) were computed. Both measures were normalized by dividing them by their corresponding C‐s and L‐s values of random control networks. SD reduced alpha band C/C‐s and L/L‐s and theta band C/C‐s during eyes‐closed resting state. In contrast, SD increased gamma‐band C/C‐s and L/L‐s during eyes‐open resting state. Functional relevance of these changes in network properties was suggested by their association with sleep deprivation‐induced performance deficits on a sustained attention simple reaction time task. The findings indicate that SD results in a more random network of alpha‐coupling and a more ordered network of gamma‐coupling. The present study shows that SD induces frequency‐specific changes in the functional network topology of the brain, supporting the idea that sleep plays a role in the maintenance of an optimal functional network. Hum Brain Mapp, 2013.

Cold Hands, Warm Feet: Sleep Deprivation Disrupts Thermoregulation and Its Association with Vigilance

STUDY OBJECTIVES Vigilance is affected by induced and spontaneous skin temperature fluctuations. Whereas sleep deprivation strongly affects vigilance, no previous study examined in detail its effect on human skin temperature fluctuations and their association with vigilance. DESIGN In a repeated-measures constant routine design, skin temperatures were assessed continuously from 14 locations while performance was assessed using a reaction time task, including eyes-open video monitoring, performed five times a day for 2 days, after a normal sleep or sleep deprivation night. SETTING Participants were seated in a dimly lit, temperature-controlled laboratory. PATIENTS OR PARTICIPANTS Eight healthy young adults (five males, age 22.0 ± 1.8 yr (mean ± standard deviation)). INTERVENTION One night of sleep deprivation. MEASUREMENTS AND RESULTS Mixed-effect regression models were used to evaluate the effect of sleep deprivation on skin temperature gradients of the upper (ear-mastoid), middle (hand-arm), and lower (foot-leg) body, and on the association between fluctuations in performance and in temperature gradients. Sleep deprivation induced a marked dissociation of thermoregulatory skin temperature gradients, indicative of attenuated heat loss from the hands co-occurring with enhanced heat loss from the feet. Sleep deprivation moreover attenuated the association between fluctuations in performance and temperature gradients; the association was best preserved for the upper body gradient. CONCLUSIONS Sleep deprivation disrupts coordination of fluctuations in thermoregulatory skin temperature gradients. The dissociation of middle and lower body temperature gradients may therefore be evaluated as a marker for sleep debt, and the upper body gradient as a possible aid in vigilance assessment when sleep debt is unknown. Importantly, our findings suggest that sleep deprivation affects the coordination between skin blood flow fluctuations and the baroreceptor-mediated cardiovascular regulation that prevents venous pooling of blood in the lower limbs when there is the orthostatic challenge of an upright posture.

Compression of the optic chiasm is associated with permanent shorter sleep duration in patients with pituitary insufficiency

Objective  Patients with pituitary insufficiency often experience some degree of impaired sleep. Sleep–wake rhythm is regulated to a large extent by the suprachiasmatic nucleus (SCN). Because the SCN is located just superior to the optic chiasm, we hypothesized that a history of compression of the optic chiasm (CC) due to a tumour with suprasellar extension is associated with altered sleep patterns in patients with pituitary insufficiency.

Coupling of infraslow fluctuations in autonomic and central vigilance markers: Skin temperature, EEG beta power and ERP P300 latency

Even under thermoneutral conditions, skin temperature fluctuates spontaneously, most prominently at distal parts of the body. These fluctuations were shown to be associated with fluctuations in vigilance: mild manipulation of skin temperature during nocturnal sleep affects sleep depth and the power spectral density of the electroencephalogram (EEG), and fluctuations in skin temperature during daytime wakefulness are related to sleep propensity and task performance. The association of daytime skin temperature fluctuations with EEG markers of vigilance has not previously been investigated. Therefore, the present study aimed to evaluate the association between daytime fluctuations in skin temperature with those in two quantitative EEG measures: the power spectral density of background EEG, and the event related potential (ERP) elicited by visual stimuli. High-density EEG and skin temperature were obtained in eight healthy adults five times a day while they performed a visual sustained-attention task. Assessments were made after a night of normal sleep and after the challenge of a night of total sleep deprivation. Fluctuations in the distal-to-proximal skin temperature gradient measured from the earlobe and mastoid were associated with fluctuations in parieto-occipital high beta band (20-40 Hz) power of the pre-stimulus background EEG, but only after sleep deprivation. The temperature fluctuations were moreover associated with fluctuations in the latency of the P300 elicited by the stimulus. The findings demonstrate close association between fluctuations in an autonomic correlate of the vigilance state (i.e. the distal-to-proximal skin temperature gradient), and fluctuations in central nervous system correlates of the vigilance state (i.e. background EEG and ERP). The findings are of theoretical and practical relevance for the assessment and manipulation of vigilance.

Medical History of Optic Chiasm Compression in Patients With Pituitary Insufficiency Affects Skin Temperature and Its Relation to Sleep

The hypothalamus is crucially involved in the circadian timing of the sleep-wake rhythm, yet also accommodates the most important thermoregulatory neuronal network. We have shown before that adults with pituitary insufficiency and history of chiasm compression due to a tumor with suprasellar extension fall asleep later and sleep shorter than those without such history and presumed hypothalamic involvement. To solidify the hypothesized link between vigilance and thermoregulation by the hypothalamus, we aimed to test the hypothesis that the presumed hypothalamic impairment in these patients also affects skin temperature and its association with sleep onset. In a case-control study of 50 patients (54.7 ± 14.5 yrs of age, 30 males) with pituitary insufficiency, 33 of whom had a history of chiasm compression, ambulatory distal and proximal skin temperatures were assessed continuously for 24 h. Sleep parameters were assessed via questionnaire. Group differences in mean skin temperature, calculated over the wake and sleep periods separately, and group differences in the strength of association between pre-sleep skin temperature and sleep onset latency were compared. Results showed that patients with a medical history of chiasm compression had lower proximal skin temperature during the day (34.1°C ± .7°C vs. 34.6°C ± .7°C, p = .045). Additionally, the typical association between sleep onset latency and pre-sleep distal-to-proximal skin temperature gradient was absent in these patients (r = −.01, p = .96), whereas it was unimpaired in those without chiasm compression (r = −.61, p = .02). Thus, patients with history of chiasm compression show impaired skin temperature regulation in association with disturbed sleep. The findings support the hypothesis that a medical history of chiasm compression affects hypothalamic regulation of both vigilance and temperature, possibly by chronically affecting relevant nuclei, including the ventrolateral preoptic area and anterior hypothalamic preoptic area. (Corresponding Author: n.romeijn@nin.knaw.nl)

Alpha Power Predicts Persistence of Bistable Perception

Perception is strongly affected by the intrinsic state of the brain, which controls the propensity to either maintain a particular perceptual interpretation or switch to another. To understand the mechanisms underlying the spontaneous drive of the brain to explore alternative interpretations of unchanging stimuli, we repeatedly recorded high-density EEG after normal sleep and after sleep deprivation while participants observed a Necker cube image and reported the durations of the alternating representations of their bistable perception. We found that local alpha power around the parieto-occipital sulcus within the first second after the emergence of a perceptual representation predicted the fate of its duration. An experimentally induced increase in alpha power by means of sleep deprivation increased the average duration of individual representations. Taken together, these findings show that high alpha power promotes the stability of a perceptual representation and suppresses switching to the alternative. The observations support the hypothesis that synchronization of alpha oscillations across a wide neuronal network promotes the maintenance and stabilization of its current perceptual representation. Elevated alpha power could also be key to the poorly understood cognitive deficits, that typically accompany sleep deprivation, such as the loss of mental flexibility and lapses of responsiveness.