Desynchrony and synchronisation underpinning sleep-wake cycles

TL;DR

This study uses a biophysical model to explore how the interaction of circadian, homeostatic, and light oscillators influences sleep-wake cycles, revealing mechanisms of synchronization and desynchronization affecting health.

Contribution

It introduces a biophysical model that elucidates how different oscillators synchronize or desynchronize, highlighting the roles of light, circadian, and homeostatic processes in sleep regulation.

Findings

Synchronization promotes sleep and brain clearance.

Desynchronization can result from altered homeostatic clearance rates.

External inputs can cause complete loss of sleep.

Abstract

A biophysical model of arousal dynamics is used to study mechanisms of synchronisation and loss of synchrony among the three key oscillators controlling sleep-wake cycles: the circadian, homeostatic, and light oscillators. Synchronisation of these rhythms promotes sleep and brain clearance and is critical for human health. Conversely, their desynchrony is linked to impaired performance and disease. We find that the default state of the model corresponds to the endogenous homeostatic period that is far from ~24 h of the circadian and light-dark cycles. Combined action of light and circadian oscillator on the homeostatic rhythm is required to achieve the typical sleep-wake pattern of healthy people. Change of homeostatic clearance is found to induce two types of desynchronisation: (i) fast clearance rates desynchronise the homeostatic oscillator from the circadian, while the circadian rhythm remains entrained to light, and (ii) slow clearance maintains synchronisation between the homeostatic and circadian oscillators, but the period is different from that of the light-dark cycle. Between these regimes, all three rhythms are synchronised under the studied conditions. The system is highly sensitive to external inputs to the neuronal populations of the sleep-wake switch, which can lead to complete loss of sleep. The model shows that loss of synchronisation can be caused by changes in the homeostatic clearance rate or external input to the neuronal populations of the sleep-wake switch. This has implications for understanding individual variability in sleep-wake patterns and in mechanisms of sleep and circadian disorders.