Rapid fast-delta decay following prolonged wakefulness marks a phase of wake-inertia in NREM sleep

Abstract

Sleep-wake driven changes in non-rapid-eye-movement sleep (NREM) sleep (NREMS) EEG delta (δ-)power are widely used as proxy for a sleep homeostatic process. Here, we noted frequency increases in δ-waves in sleep-deprived mice, prompting us to re-evaluate how slow-wave characteristics relate to prior sleep-wake history. We identified two classes of δ-waves; one responding to sleep deprivation with high initial power and fast, discontinuous decay during recovery sleep (δ2) and another unrelated to time-spent-awake with slow, linear decay (δ1). Reanalysis of previously published datasets demonstrates that δ-band heterogeneity after sleep deprivation is also present in human subjects. Similar to sleep deprivation, silencing of centromedial thalamus neurons boosted subsequent δ2-waves, specifically. δ2-dynamics paralleled that of temperature, muscle tone, heart rate, and neuronal ON-/OFF-state lengths, all reverting to characteristic NREMS levels within the first recovery hour. Thus, prolonged waking seems to necessitate a physiological recalibration before typical NREMS can be reinstated.

Sub-minute prediction of brain temperature based on sleep–wake state in the mouse

“…SD was achieved by gentle handling ( Mang and Franken, 2012 ). In addition to the main experiment above, a subset of five animals (1 WT and 4 KO mice) was subjected to a 2- and 4-hr SD following the same protocol as for the 6-hr SD experiment but without recovery 2 ( Hubbard et al, 2020 ). One session was excluded due to a technical problem resulting in abrupt discontinuity of the temperature data.…”

Parsing Neurodynamic Information Streams to Estimate the Frequency, Magnitude and Duration of Team Uncertainty

“…Delta waves are widely used as proxy for a sleep homeostatic process and have primarily been reported in the context of sleep-wake driven changes (Hubbard et al, 2020 ), but more recently they have gained attention as a modulator of executive action of motor function (Harmony, 2013 ).…”

Challenging sleep homeostasis

“…More recently, the entire relationship between NREM SWA and Process S has been questioned. The portion of SWA responsive to sleep loss resolves itself within 60 min and may be influenced by physiological variables unrelated to Process S. This challenges previous mathematical models describing changes in NREM SWA proportionate to prior wake time ( Hubbard et al, 2020 ). All other electrophysiological measures of Process S (e.g., neuronal firing rates ( Vyazovskiy et al, 2009 )) must also now be reconsidered, as they are interpreted in terms of changes in NREM SWA.…”

“…It represents yet another switch in sleep/wake mechanisms that when a certain threshold of waking is exceeded, it engages other switches that trigger sleep onset. This would explain why mammalian sleep propensity appears to discharge within 60 min ( Hubbard et al, 2020 ). This might also be entirely explained in mundane ways as increasing refractory periods in waking circuits (based on known principles of synaptic transmission) that release sleep-inducing circuits from inhibition.…”

“…Therefore, an important challenge is to test direct links between this measure of sleep propensity and proposed sleep functions. Recent findings showing that sleep propensity dissipates within 60 min are more difficult to explain ( Hubbard et al, 2020 ), but it would be premature to disregard hundreds of studies based on a single report. It is important that these findings be replicated and subjected to further tests using subjects with variable time courses of Process S ( Franken et al, 2001 ) as well as mutants that show increases and decreases in the compensatory response to SD ( Shaw and Franken, 2003 ).…”