Homeostatic dysregulation of slow wave activity during sleep in idiopathic hypersomnia

Sleep homeostasis describes the accumulation of sleep pressure during wakefulness and its dissipation during sleep. Electroencephalographic delta power (SWA, [0.5-4 Hz]) is a known marker of sleep pressure. Dysregulation of this process has been proposed in idiopathic hypersomnia (IH), a debilitating disorder characterized by severe daytime sleepiness and excessive sleep duration. We investigated SWA regulation in IH with (IH-LST) and without (IH-nLST) long-sleep time and healthy participants in a controlled ad libitum sleep protocol.

We recorded SWA in 208 IH participants and 25 controls during a 32-hour continuous polysomnography without circadian cues. We characterized sleep architecture and SWA as functions of sleep and prior wake duration, to capture dissipation and accumulation of sleep pressure. We then applied an established model of sleep pressure fitted individually. Model parameters were compared across groups, and simulations were performed to predict and compare sleep pressure during extended sleep and wakefulness.

In all IH participants (88% IH-LST, 12% IH-nLST), SWA persisted during extended sleep, while wakefulness led to greater SWA rebounds only in IH-LST; indicating dysregulation of accumulation and dissipation. In the mathematical approach, sleep pressure failed to dissipate after nine hours of sleep in all IH participants, and accumulated faster during the first four hours of wakefulness in the IH-LST subgroup. These effects were mediated by a stronger accumulation during both early wakefulness and late REM sleep.

Our findings highlight a dysregulation of sleep homeostasis in idiopathic hypersomnia and support the reintroduction of the distinction between the phenotypes with and without long sleep time.