Humans Remain Behaviorally Responsive to External Auditory Stimuli During Deep Sleep

Author: Vignesh Subramanian, Class of 2024

It has long been assumed that sleep is a stable state of unconsciousness in which an individual cannot perceive and respond to most external stimuli. However, recent studies have indicated that humans can process information, discriminate between basic sensations, and carry out limited executive functions, such as answering yes–no questions, while still asleep. Some oneirological studies have focused on determining whether two-way communication is possible with lucid dreamers, individuals who are aware they are dreaming while asleep. Such studies have noted that in certain phases of sleep – such as rapid eye movement (REM) sleep, the deepest phase of sleep, in which most dreams occur and when brain activity closely resembles that of wakefulness – lucid dreamers often demonstrate behavioral responsiveness to stimuli while asleep in the form of eye and facial muscle movements. 

Researchers at the Paris Brain Institute sought to examine whether humans with less fitful, vivid dreams are similarly behaviorally responsive to their environments while asleep. The researchers recruited 49 participants – 27 with narcolepsy, which is associated with having a high frequency of lucid dreams, and 22 healthy, non-lucid dreamers – and instructed them to distinguish between spoken words and non-words while napping by either smiling (if they heard a real word) or frowning (if they heard a pseudo-word). The participants were then directed to begin naps; their sleep/wake stages were verified with polysomnograms, which utilize a combination of electroencephalography, electrooculography, and electromyography, the latter being the measurement of muscle activity in response to nervous stimulation. Facial electromyography of participants’ zygomatic and corrugator muscles, which are associated with smiling and frowning, respectively, was also recorded to track participants’ responses. 

The researchers found that both narcoleptic and healthy participants were significantly more behaviorally responsive when words and non-words were spoken, including in both the N2 and REM stages of sleep, than in the “off” or silent periods of the lexical decision task. Overall, all of the participants, both with and without a sleep disorder, accurately distinguished between real and pseudo-words for at least 70% of the auditory prompts. Response rates were highest during REM sleep for all participants, providing some of the first evidence of behavioral responsiveness by humans experiencing bona fide, non-lucid REM sleep. These results collectively indicate that humans undergo transient periods of sensory connection and higher cognitive states while deeply asleep, further unraveling the mystery of the interplay between consciousness and sleep.

Figure 1: Rapid eye movement (REM) sleep is the stage of the deepest sleep in the sleep cycle, although brain activity in this stage closely resembles that of wakefulness.

[1] Türker, B., Musat, E. M., Chabani, E., Fonteix-Galet, A., Maranci, J-B., Wattiez, N., Pouget, P., Sitt, J., Naccache, L., Arnulf, I., & Oudiette, D. (2023). Behavioral and brain responses to verbal stimuli reveal transient periods of cognitive integration of the external world during sleep. Nature Neuroscience, 26(11), 1981-1993. doi: 10.1038/s41593-023-01449-7 

[2] Image retrieved from: https://unsplash.com/photos/woman-sleeping-on-bed-under-blankets-rUc9hVE-L-E 

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