Neural Markers of Responsiveness to the Environment in Human Sleep

Abstract

Sleep is characterized by a loss of behavioral responsiveness. However, recent research has shown that the sleeping brain is not completely disconnected from its environment. How neural activity constrains the ability to process sensory information while asleep is yet unclear. Here, we instructed human volunteers to classify words with lateralized hand responses while falling asleep. Using an electroencephalographic (EEG) marker of motor preparation, we show how responsiveness is modulated across sleep. These modulations are tracked using classic event-related potential analyses complemented by Lempel-Ziv complexity (LZc), a measure shown to track arousal in sleep and anesthesia. Neural activity related to the semantic content of stimuli was conserved in light non-rapid eye movement (NREM) sleep. However, these processes were suppressed in deep NREM sleep and, importantly, also in REM sleep, despite the recovery of wake-like neural activity in the latter. In NREM sleep, sensory activations were counterbalanced by evoked down states, which, when present, blocked further processing of external information. In addition, responsiveness markers correlated positively with baseline complexity, which could be related to modulation in sleep depth. In REM sleep, however, this relationship was reversed. We therefore propose that, in REM sleep, endogenously generated processes compete with the processing of external input. Sleep can thus be seen as a self-regulated process in which external information can be processed in lighter stages but suppressed in deeper stages. Last, our results suggest drastically different gating mechanisms in NREM and REM sleep.

Targeted memory reactivation during sleep elicits neural signals related to learning content

“…Memory reactivation was facilitated when the cue was followed by a spindle, as evidenced both by later memory performance and by EEG analyses. Moreover, this paradigm -using lateralized differences as a means of tracking reactivation of specific episodic associations -could be useful for uncovering nuanced relationships between reactivation and memory (Lewis-Peacock and Norman, 2014) and investigating how reactivation differs across physiological states (Andrillon et al, 2016;Jiang et al, 2017;Schönauer et al, 2017;Belal et al, 2018) and human populations (Mander et al, 2013;Westerberg et al, 2015).…”

“…Several prior findings suggest that lateralized neural signals can be tracked with EEG. After training participants to perform lateralized judgments on words during wake (e.g., "press left if word, press right if nonword"), corresponding lateralized responses were elicited by those stimuli during sleep (Kouider et al, 2014;Andrillon et al, 2016). This finding shows that participants can apply a well-learned task set (acquired during wake) to stimuli presented during sleep, but does not show retrieval of specific episodic memories.…”

Increased spontaneous EEG signal diversity during stroboscopically-induced altered states of consciousness

“…The reduction in the diversity of subjective experiences during these 'diminished' states may plausibly be reflected in the diversity of neural signals in these states. Indeed, measures of spontaneous EEG signal diversity, such as Lempel-Ziv complexity, are reduced in states with diminished or absent conscious experience, such as during sleep or under anaesthesia, relative to the normal waking state [5][6][7] . In a more direct test of the relation between experiential diversity and neuronal signal diversity, Schartner et al, 8 reported a brain-wide robust increase in signal diversity during altered states of consciousness (ASC) induced by the classic psychedelics LSD, ketamine and psilocybin.…”

EEG signal diversity during propofol sedation: an increase in sedated but responsive, a decrease in sedated and unresponsive subjects

“…Promising results of the PCI studies encouraged researchers to investigate similar properties in the spontaneous brain activity recorded during different states of consciousness. Similarly to PCI, diversity of spontaneous EEG signals is high during wakefulness and drops during propofol anesthesia or NREM sleep (Schartner et al, 2015(Schartner et al, , 2017Andrillon et al, 2016).…”