Sleepers Selectively Suppress Informative Inputs During Rapid Eye Movements

Abstract

Sleep leads to a disconnection from the external world. Even when sleepers regain consciousness during Rapid Eye Movement (REM) sleep, little, if any, external information is incorporated into dream content. While gating mechanisms might be at play to avoid interference on dreaming activity, a total disconnection would prevent the sleeper from promptly responding to informative events (e.g., threat signals). In fact, a whole range of neural responses to external events are preserved, at least partially, during REM sleep. Thus, it remains unsettled whether external inputs are either integrated or conversely gated during REM sleep. Here, we sought to disentangle this issue by studying the impact of eye movements (EMs) on the processing of informative signals. EMs constitute a reliable predictor of reporting a dream upon awakening and induce a higher arousal threshold to external stimuli. We hypothesized that although sleepers might continue responding to external events, periods of EMs would be associated with the gating of informative signals in order to reduce interference with dreaming activity. By reconstructing perceived speech in a multi-talker, cocktail-party environment from electrophysiological responses, we show that informative speech is selectively amplified over meaningless speech during REM sleep. However, we show that at the precise timing of EMs, informative speech is, on the contrary, selectively suppressed. Importantly, this suppression did not affect the processing of non-informative signals, revealing a selective mechanism of gating for informative contents rather than a general decline in sensory encoding. These results reveal flexible mechanisms of amplification/suppression of external inputs during REM sleep, and demonstrate the impact of EMs on the selective gating of informative stimuli.