Behavioral and brain responses to verbal stimuli reveal transient periods of cognitive integration of external world in all sleep stages

Abstract

Sleep has long been considered as a state of disconnection from the environment, with absent reactivity to external stimuli. Here, we questioned this sleep disconnection dogma by directly investigating behavioral responsiveness in 49 napping subjects (27 with narcolepsy and 22 healthy volunteers) engaged in a lexical decision task. Participants were instructed to frown or smile depending on the stimulus type (words vs pseudo-words). We found accurate behavioral responses, visible via contractions of the corrugator or zygomatic muscles, in all sleep stages in both groups (except slow-wave sleep for healthy volunteers). Stimuli presented during states with high (vs. low) values of neural markers indexing rich cognitive states more often yielded responses. Our findings suggest that transient windows of reactivity to external stimuli exist in all sleep stages, even in healthy individuals. Such windows of reactivity could be used to probe sleep-related mental and cognitive processes in real-time across all sleep stages.

Thalamocortical Spindles occur during Rapid Eye Movement Sleep in Mouse Somatosensory Pathway

“…While the same mechanism is likely to take place during REM spindle bouts, ongoing tonic firing activity in half of VPM neurons (Figure 3) may set the thalamocortical network at an “activatable state” level, rapidly allowing sensory transmission to resume during phasic episodes of RWM (Figure S4). Indeed, a recent study provided evidence in human of transient windows of sensory connection with the outside world during which external information can be processed in REM 65 . Increased cholinergic activity in S1 may further act to suppress delta cortical activity during RWM 66 , as reported during whisking in wakefulness 67 .…”

Mind the blank: behavioral, experiential, and physiological signatures of absent-mindedness

“…We computed three classes of neural markers: 1) spectral markers (normalized power spectral densities (PSD) in the delta, theta, alpha, beta and gamma bands); 2) complexity markers 21,27 (Kolmogorov Complexity (KC), Approximative Entropy (AE), Sample Entropy (SE) and Permutation Entropy (PE), this last marker being computed in different frequency bands); and 3) connectivity markers (weighted symbolic mutual information 20 (wSMI) in the delta, theta, alpha, beta and gamma bands and the Phase Locking Value (PLV)). These markers (and other similar measures) have been previously shown to be able to track cognitive and consciousness state modifications in a large range of conditions, including disorders of consciousness (DoC) 20,21,28 , sleep [29][30][31] , hypnosis 32 and meditation 33 .…”

“…By combining these markers, it is possible to distinguish conscious participants, patients in a minimal consciousness state and patients with unresponsive wakefulness syndrome [20][21][22] . These measures can also differentiate sleep stages 29,31,41 and track cognitive and consciousness modifications related to psychedelics or meditation 33 . In our study, we computed these different measures to try to describe the neural correlates of the different mind states (ON, MW and MB).…”

Episodic long-term memory formation during slow-wave sleep

“…Neural complexity is indicative of both the brain's capacity to process sensory information (Waschke et al, 2017(Waschke et al, , 2019 and the extent of ongoing cognitive activity (Höhn et al, 2023;Parbat & Chakraborty, 2021). Furthermore, levels of neural complexity closely correspond to the depth of sleep (Casali et al, 2013;Höhn et al, 2023;Ma et al, 2018;Türker et al, 2023) Here, we explored whether word presentations would have distinct impacts on post-stimulus neural complexity when stimulation was targeted to the Trough, where sleep-learning occurred, vs. to the Peak, where no sleep-learning occurred. To this aim, we calculated the Higuchi Fractal Dimension (HFD) of the EEG signal in the time domain at each channel separately for a pre-(-2 to -0.5 s) and a post-stimulus (0.5 to 2s) time window.…”

“…Although the thalamic gating hypothesis had claimed a blockade of sensory information at the thalamic level (McCormick & Bal, 1994), we now know that sleepers still monitor the environment for their safety and survival (Ai et al, 2018;Andrillon et al, , 2017Arzi et al, 2012;Blume et al, 2017;Koroma et al, 2022;Ruch et al, 2014;Ruch & Henke, 2020;Züst et al, 2019). The sleeping brain decides whether an external event can be disregarded, requires immediate awakening or should be stored for later consideration in the waking state (Ameen et al, 2022;Blume et al, 2018;Formby, 1967;Holeckova et al, 2006;Moyne et al, 2022;Oswald et al, 1960;Türker et al, 2023).…”