How much does your brain pay attention while you’re asleep?

Posted by Susan Lubejko on July 9, 2020 in Neuroscience, Sleep | 2 Comments

*Tick, tick, tick* I glance over into the dusty corner of the dimly lit room, and to my horror, I see what looks like some sort of explosive device fitted with a clock, inevitably ticking down to my demise. *Tick, tick, tick* I freeze in fear, unsure of how to resolve this situation. The ticking of the clock on the device seems to be getting louder, unable to be drowned out by the rush of blood in my ears. *TICK, TICK, TICK* The clock is about to reach zero… when my eyes fly open and I sit up in bed, realizing this scary scenario was all a nightmare. Looking around my room, I determine that the ticking sound was actually a page of a magazine flapping rhythmically in the air coming from my ceiling fan. 

This phenomenon of outside stimuli (like sounds or lights) making their way into dreams is not uncommon. Scientific studies going back to the 1960s formally tested the ability for outside stimuli to appear in dreams by reading names of individuals known to the study participants during periods of sleep in which they were likely dreaming [1]. The results were pretty hit or miss, but some participants remembered having dreams related to the names read, although not exactly in the way you might expect (think: the study participant was read the name “Morgan” and had a dream in which they were suddenly an expert at playing the pipe organ). Though this phenomenon certainly can happen, it often seems like sleepers’ brains are totally disconnected from the outside world during sleep. And yet other times, outside noises, like a tree branch brushing up against your window, immediately wake you up. So, how much outside information is your brain really processing during sleep? How much does this processing rely on what the stimulus is and when it is happening during sleep? And what parts of the brain take this information and wake us up when necessary?

Does the brain process incoming information during sleep?

Before getting into the details of information processing during sleep, what does normal sleep look like, and how is it studied? Sleep can be divided into two broad categories: REM (rapid eye movement) and NREM (non-REM) sleep. The brain cycles through the stages of NREM sleep and REM sleep multiple times each night, and these cycles are defined by characteristic changes in brain electrical activity that can be recorded by electrodes placed on the scalp, in a process known as electroencephalography or EEG. For a full understanding of sleep, the associated cycles, and brain activity, check out these NeuWriteSD articles.

For the purposes of information processing, we will focus on REM sleep. REM sleep is characterized by the rapid darting around of the eyes behind the eyelids and is the sleep stage most associated with dreaming. In an effort to keep you from acting out your dreams, large muscle groups in the body become paralyzed during REM sleep. For these reasons, it might make sense for your brain’s ability to process external stimuli to be decreased during REM sleep because you wouldn’t be able to physically react anyway. However, it is clear from brain activity recordings that sound information processing is surprisingly intact in REM sleep, including the brain’s response to hearing the individual’s own name [2], especially when spoken by a familiar voice [3]. 

In taking a closer look at this phenomenon, sleep scientists have recently further broken down REM sleep into two parts. The first phase has relatively little of the characteristic eye movements and lower arousal thresholds – it is relatively easy to wake a person in this phase. The second phase of REM features abundant and extremely rapid eye movements (EMs) and very high arousal thresholds, meaning it is decidedly difficult to wake from this phase of REM sleep [4]. In this context, then, how does the brain process incoming information during these phases of REM sleep, when complete blockade of signals would best serve sleep and dreaming?

What kinds of information are still processed during sleep?

In a 2020 study from sleep researchers in France [5], subjects were trained while awake to listen to two different recordings through headphones. The first recording was an “informative” story, meaning that the story was spoken in understandable English and thus had information content. The second recording, inspired by the Lewis Carroll poem “The Jabberwocky”, included normal sentence structure but with nonsense words and thus had no meaningful, informative content for the listener. While still awake, the subjects listened to both stories at the same time, one in each ear, and were told to focus their attention on the story with informative content (aka the story with real words). Next, the subjects were instructed to take a nap while the researchers recorded their brain activity by EEG and continued to play the two stories in each ear. By analyzing the shape and location of brain activity, the researchers were then able to determine how much of the incoming auditory information the subjects’ brains were processing during different phases of sleep. 

Interestingly, during the periods of REM sleep in which there were no EMs (when the subjects could still wake up), their brains continued to process both the informative and Jabberwocky stories, meaning that their brains were still paying attention to their surroundings for any meaningful content that could signal a need to wake up. However, when the subjects displayed a lot of EMs and were most likely in the phase of REM sleep with the most dreaming and inability to wake, their brains actually selectively stopped processing the informative story in favor of the nonsense Jabberwocky speech. It may be that during periods of sleep most associated with dreaming and paralysis, the brain attempts to isolate itself from outside content that has meaning to the sleeper, and therefore would be more likely to disrupt them. 

But there are surely situations in which a particularly important outside noise cannot be ignored for our safety. So, what brain systems are involved in waking up to noises in our environment?

How does the brain wake us up if we need to?

As we’ve discussed, there are variations in normal sleep phases regarding how easy it would be for a sound to wake someone. Ultimately, it would have been unsafe for our ancestors sleeping outside and at risk of attack by predators to fully suppress arousal from certain sounds for the entirety of night. What parts of our brain control our ability to be aroused from sleep in response to potentially threatening outside stimuli?

A recent study from researchers in Israel [6] sought to understand both the brain chemicals and brain regions involved in “sound-evoked awakenings” (SEAs) in sleeping rats that were played tones of different intensities throughout the duration of their sleep cycles. This research found a major role for the brain chemical norepinephrine in whether the tone could wake the sleeping rat. Levels of norepinephrine are known to be high during waking periods and low during sleep, and are therefore often given major credit in arousal and natural transitions between sleeping and waking. When the rats were treated with drugs to decrease the amount of norepinephrine in their bodies, the researchers found that the tones were less likely to wake the rats.

To determine where in the brain this all-important norepinephrine could be coming from, the researchers looked to the locus coeruleus (LC), the source of a majority of the neurons in the brain that release norepinephrine. The LC has thus unsurprisingly been credited with major roles in arousal and wakefulness. Activity in the neurons of the LC is high during waking periods, but is thought to be very low during REM and NREM sleep. By recording the activity of neurons in the LC in their sleeping rats, the researchers found that sound trials that led to awakening correlated with more activity in the LC neurons in the moments leading up to the tone, as compared to very low LC activity preceding trials in which the rat remained asleep. The researchers also found that artificially activating neurons in the LC increased the chances that the tones would wake the rats in any sleep phase [6]. Each of these findings supports a role for norepinephrine released by the LC in determining the likelihood that an outside stimulus will wake a sleeping rat. Extending this idea to humans, similar mechanisms may be at play when you are suddenly awoken by that annoying tree branch, and could help explain the variability in the likelihood of waking up due to a noise in different circumstances. Additionally, these mechanisms could perhaps be at play differently in different people to explain why some people are much more prone to waking up due to outside lights or noises. 

Striking the right balance

Getting the right amount and quality of sleep is known to be extremely important for all kinds of brain and body functions. Sound, uninterrupted sleep allows us to cycle through the important sleep stages and wake feeling well-rested. However, the need to be able to rapidly wake upon experiencing certain outside threats is also important, especially for our ancestors that had less protection during their sleep. This balance is thought to be disturbed in many different types of psychiatric disorders, including in patients with posttraumatic stress disorder (PTSD). Patients with PTSD exhibit severe sleep disruption that correlates with increased norepinephrine circulating in the body during sleep [7], perhaps indicating that this threat detection by the LC and noradrenaline that leads to arousal from sleep is in overdrive. 

So, the next time you wake up from a curious dream that was clearly influenced by the movie you fell asleep during, or abruptly wake due to the benign noise of a tree branch tapping on your window, you can thank your brain for selectively keeping track of what is going on around you while you enjoy your snooze.

References 

1. Berger RJ (1963) Experimental modification of dream content by meaningful verbal stimuli. British Journal of Psychiatry, 109:722-740
2. Perrin F, Garcia-Larrea L, Mauguiere F, Bastuji H (1999) A differential brain response to the subject’s own name persists during sleep. Clinical Neurophysiology, 110:2153-2164
3. Blume C, del Giudice R, Wislowska M, Heib DPJ, Schabus M (2018) Standing sentinel during human sleep: continued evaluation of environmental stimuli in the absence of consciousness. NeuroImage, 178:638-648
4. Ermis U, Krakow K, Voss U (2010) Arousal thresholds during human tonic and phasic REM sleep. Journal of Sleep Research, 19:400-406
5. Koroma M, Lacaux C, Andrillon T, Legendre G, Leger D, Kouider S (2020) Sleepers selectively suppress informative inputs during rapid eye movements. Current Biology, 30:1-7
6. Hayat H, Regev N, Matosevich N, Sales A, Paredes-Rodriguez E, Krom AJ, Bergman L, Li Y, Lavigne M, Kremer EJ, Yizhar O, Pickering AE, Nir Y (2020) Locus coeruleus norepinephrine activity mediates sensory-evoked awakenings from sleep. Science Advances, 6:eaaz4232
7. Mellman TA, Kumar A, Kulick-Bell R, Kumar M, Nolan B (1995) Noctural/daytime urine noradrenergic measures and sleep in combat-related PTSD. Biological Psychiatry, 38:174-179