Sleep is generally defined as a period during which the body and mind are at rest, as if disconnected from the world. © Nicolas Decat
When we sleep we are not completely cut off from our environment: we are still able to hear and understand words. These observations, resulting from the close collaboration between researchers from Inserm, CNRS, Sorbonne Université and AP-HP at the Brain Institute and the Department of Sleep Disorders at Pitié-Salpêtrière Hospital in Paris, call into question the very definition of sleep and the clinical criteria that distinguish between its different stages. They are detailed in a new study published in Nature Neuroscience.
Sleep is generally defined as a period during which the body and mind are resting, as if disconnected from the world. However, a new study led by Delphine Oudiette, Inserm researcher, Isabelle Arnulf (Sorbonne Université, AP-HP) and Lionel Naccache (Sorbonne Université, AP-HP) at the Brain Institute, shows that the boundary between wakefulness and sleep is much more porous than it would appear.
The scientists have shown that sleepers with no particular disorders are able to capture verbal information transmitted by a human voice and respond to it by contracting facial muscles. What is more, this astonishing ability manifests itself intermittently during almost all stages of sleep — as if windows to the outside world were temporarily opened.
These new data on sleep behavior suggest that it may eventually be possible to develop standardized protocols for communication with sleepers in order to better understand how mental activity changes during sleep.
On the horizon: a new access route to the cognitive processes that underpin normal and pathological sleep.
A Thousand and One Variations in Consciousness
“Even if it seems familiar to us because we do it every night, sleep is a very complex phenomenon. Our research has taught us that wakefulness and sleep are not stable states: both resemble a kaleidoscope of conscious moments… and moments that do not appear to be so,” explains Prof. Lionel Naccache, neurologist at Pitié-Salpêtrière Hospital AP-HP and neuroscience researcher.
It is essential to improve our understanding of the brain mechanisms that underlie these intermediate states between wakefulness and sleep.
“When out of sync, they can be associated with disorders such as sleepwalking, sleep paralysis, hallucinations, the feeling of not sleeping at night or, on the contrary, sleeping with the eyes open“, explains Prof. Isabelle Arnulf, head of the Sleep Disorders Department at Pitié-Salpêtrière Hospital AP-HP.
However, in order to distinguish between wakefulness and the different stages of sleep, we have so far used simple and inaccurate physiological indicators, such as specific brain waves made visible through electroencephalography. Such indicators do not capture in detail what is going on inside the heads of sleepers, especially as they are sometimes in contradiction with what the sleepers tell us themselves.
“We need more refined physiological measurements that are aligned with the sleeper’s feelings and ability to respond to the outside world; this is to better define their level of vigilance“, adds Delphine Oudiette, Inserm researcher in cognitive neuroscience.
A Game Between Unconsciousness and Lucidity
The research team therefore explored this avenue and recruited 22 people without sleep disorders and 27 narcoleptic patients — i.e. victims of irrepressible sleep episodes.
People with narcolepsy have the particularity of having many lucid dreams, namely in which they are aware of being asleep and can sometimes shape the scenario. In addition, they easily and quickly reach REM sleep (the stage where the lucid dream emerges) during the day, making them good candidates for studying consciousness during sleep under experimental conditions.
“One of our previous studies had shown that two-way communication, between the scientist and the dreamer and vice versa, is possible during lucid REM sleep, explains Oudiette. For our latest study, we wanted to know if these findings could be extrapolated to other sleep stages and to individuals who do not have lucid dreams. “
The study participants were asked to take a nap. The researchers had them do a “lexical decision” test in which a human voice uttered a series of words, both real and made up. The participants had to respond by smiling or frowning, in order to place the words in one of the two categories. Throughout the experiment, the participants were monitored using polysomnography—a comprehensive examination to record their brain and heart activity, eye movements, and muscle tone. Finally, upon waking, they had to report whether or not they had a lucid dream during their nap, and whether they remembered interacting with someone.
“Most of the participants, whether narcoleptic or not, managed to respond correctly to the verbal stimuli while sleeping. These events were admittedly more frequent during episodes of lucid dreams, characterized by a high level of consciousness; however, we observed them occasionally in both groups, during all sleep phases”, specifies Arnulf.
By combining these physiological and behavioral data with the subjective reports of the participants, the researchers also show that it is possible to predict the opening of these windows of connection with the environment, i.e. the times when the sleepers were able to respond to stimuli. These were heralded by an acceleration of brain activity, and by physiological indicators usually associated with rich cognitive activity.
“In people who had a lucid dream during their nap, the ability to dialog with the investigator and talk about this experience on waking was also characterized by a specific electrophysiological signature, adds Naccache. Our data suggest that lucid dreamers have privileged access to their inner world, and that this increased awareness also extends to the outside world. “
Further research will be needed to determine whether the increase in these windows is correlated with sleep quality, and whether they could be used to improve certain sleep disorders or promote learning.
“More advanced neuroimaging techniques, such as magnetoencephalography and intracranial recording of brain activity, will help us to better understand the brain mechanisms that orchestrate sleep behaviors“, concludes Oudiette.
Finally, these new data could help to revise the definition of sleep, a state that is ultimately very active, perhaps more conscious than we thought, and open to the world and others.
This study was funded by the French National Research Agency and the French Society for Sleep Research and Medicine (SFRMS).
 Including PhD students Başak Türker, Esteban Munoz Musat and Emma Chabani, whose participation was essential to the conduct of this study.
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