Cerebral blood flow changes after a day of wake, sleep, and sleep deprivation

Abstract

Elucidating the neurobiological effects of sleep and wake is an important goal of the neurosciences. Whether and how human cerebral blood flow (CBF) changes during the sleep-wake cycle remain to be clarified. Based on the synaptic homeostasis hypothesis of sleep and wake, we hypothesized that a day of wake and a night of sleep deprivation would be associated with gray matter resting CBF (rCBF) increases and that sleep would be associated with rCBF decreases. Thirty-eight healthy adult males (age 22.1±2.5 years) underwent arterial spin labeling perfusion magnetic resonance imaging at three time points: in the morning after a regular night's sleep, the evening of the same day, and the next morning, either after total sleep deprivation (n=19) or a night of sleep (n=19). All analyses were adjusted for hematocrit and head motion. rCBF increased from morning to evening and decreased after a night of sleep. These effects were most prominent in bilateral hippocampus, amygdala, thalamus, and in the occipital and sensorimotor cortices. Group x time interaction analyses for evening versus next morning revealed significant interaction in bilateral lateral and medial occipital cortices and in bilateral insula, driven by rCBF increases in the sleep deprived individuals and decreases in the sleepers, respectively. Furthermore, group x time interaction analyses for first morning versus next morning showed significant effects in medial and lateral occipital cortices, in anterior cingulate gyrus, and in the insula, in both hemispheres. These effects were mainly driven by CBF increases from TP1 to TP3 in the sleep deprived individuals. There were no associations between the rCBF changes and sleep characteristics, vigilant attention, or subjective sleepiness that remained significant after adjustments for multiple analyses. Altogether,

Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity

“…Interestingly, the largest of these studies (Elvsåshagen et al, 2019) reported regional CBF increases related to duration of wakefulness in the same regions where we observed the strongest time of day-associated reductions in resting state BOLD signal fluctuation and RSFC (e.g. somatomotor and visual cortex).…”

“…Based on the premise that synaptic strengthening has a significant metabolic cost (Harris et al, 2012), the synaptic homeostasis hypothesis (Tononi and Cirelli, 2003) predicts an increase in cerebral oxygen and glucose consumption, and as a result, increased cerebral blood flow (CBF) with cumulative wakefulness (Tononi and Cirelli, 2006). Indeed, several studies have reported elevated CBF in the evening relative to morning (Braun, 1997;Kuboyama et al, 1997;Elvsåshagen et al, 2019; but see Shannon et al, 2013;Hodkinson et al, 2014).…”

“…Examples include diurnal variation in synaptic protein levels and synaptic strength (Vyazovskiy et al, 2008;Gilestro et al,2009;Liu et al, 2010), the amplitude and slope of cortical or motor evoked responses (Vyazovskiy et al, 2008;Huber et al, 2013;Kuhn et al, 2016), theta power (Finelli et al, 2000;Hung et al, 2013) as well as changes in cerebral blood flow (Braun, 1997;Hodkinson et al, 2014;Elvsåshagen et al, 2019), task-related BOLD activation (Schmidt et al, 2009;Muto et al, 2016;Byrne et al, 2017), resting state BOLD signal amplitude (Jiang et al, 2016;Cordani et al, 2018) and resting state functional connectivity (Blautzik et al, 2013;Shannon et al, 2013;Hodkinson et al, 2014).…”

ExploreASL: an image processing pipeline for multi-center ASL perfusion MRI studies

“…We illustrate the ExploreASL image processing results and reproducibility for three populations with similar 2D-EPI PCASL protocols: perinatally-infected HIV children, healthy adults, and elderly with mild cognitive complaints, from the NOVICE (Blokhuis et al 2017), the Sleep (Elvsåshagen et al 2018), and the European Prevention of Alzheimer’s Dementia (EPAD) studies (Ritchie et al 2016), respectively (Supplementary Table 3). All three studies adhered to the Declaration of Helsinki and were approved by the local ethics committees (Academic Medical Center (AMC) in Amsterdam, Norwegian South East Regional Ethics Committee, and VU Medical Center Amsterdam and University of Edinburgh, respectively).…”

“…ExploreASL allows to adjust for individual arterial blood T1 by either providing its value directly (Li et al 2017) or by providing the hematocrit value and computing the blood T1 (Hales et al 2016). As hematocrit and blood T1 measurements can be noisy - especially when obtained at different laboratories - a pragmatic approach is to apply the average blood T1 correction on a population rather than on an individual level (Elvsåshagen et al 2018). Additionally, hematocrit and blood T1 can be modeled based on age and sex (Hales et al 2014), but this requires validation.…”