25 Jan 2019

Rocking isn’t just for babies anymore—it can soothe slumbering adults, too. Two papers in the January 24 Current Biology online suggest that a gentle, rhythmic sway throughout the night promotes sleep and memory. In the first study, scientists led by Laurence Bayer, University of Geneva, report that rocking lengthens and deepens sleep in people, enhancing brain oscillations and improving declarative memory. The second report by the same group of scientists, this time anchored by Paul Franken, University of Lausanne, Switzerland, explores the mechanism using mice. The authors found that rocking increased time spent in non-rapid eye movement (NREM) sleep, likely by stimulating the vestibular system.

Scientists led by David Holtzman, Washington University School of Medicine in St. Louis, recently reported that NREM sleep takes a nosedive when pathological Aβ and tau are present in the brain (Jan 2019 news). 

“I found both of these papers fascinating,” said Holtzman, who was not involved in the studies. “Given the beneficial effect of slow-wave sleep on memory, that we all have less slow-wave sleep with normal aging, and the likely beneficial effects of slow-wave sleep on decreasing proteins linked to AD pathogenesis, it would be really interesting to see the effect of rocking on NREM sleep and similar parameters the authors measured in middle-aged and elderly people.”

Bayer and colleagues previously showed that rocking young adults side to side at 0.25 Hz during a 45-minute nap helped them fall asleep faster and spend more time in NREM sleep. Rocking also enhanced sleep spindles, which are short bursts of neuronal oscillations visible by EEG that occur in NREM stage 2 sleep (Bayer et al., 2011). Each calm back-and-forth motion was slow, spanning four seconds. Would rocking have further benefits if done overnight?

To find out, first author Aurore Perrault brought 18 young adults into the lab to sleep on three separate occasions. One overnight stay was a habituation trial, to get used to sleeping in the lab. The next two were spent in a bed that was either stationary or connected to a rocking motor. The authors alternated which condition participants experienced first. During the sleepovers, the volunteers were hooked up to EEG monitors to record brain-wave activity. In the evening before they fell asleep and in the morning after, the researchers tested the volunteers’ reaction times and declarative memories. For the latter, participants had to recall 46 word pairs they had learned during the day.

Rocking measurably improved sleep quality, though not in quite the same way as previously seen in a short nap. The volunteers moved faster from NREM stage 1 to stage 2 sleep, then spent more time in the deepest stage 3 sleep. They also experienced 60 percent fewer EEG arousals in this deep-sleep stage. Arousals are sudden shifts in EEG frequency that last at least three seconds. They are often followed by a return to deep sleep, but can also lead a person to wake up.

The EEG waveforms characteristic of NREM sleep also changed when the person was being rocked. Sleep spindles of 11 to 16 Hz and slow oscillations of less than 1.5 Hz, visible on EEGs, represent coordinated neuronal firings that are important for overnight memory consolidation (Dec 2017 news). In rocked sleep, NREM stage 3 sleep was marked by up to 40 percent more sleep spindles, and 20 percent more slow oscillations. These waveforms seemed to be synchronized to the rocking phase, clustering at specific points during the four-second back-and-forth motion (see image above).

In the morning, participants remembered more word pairs than they had before they went to sleep. Those who had slept in the stationary bed remembered about two more pairs, while those in the rocking bed gained around five.

The results suggest that rocking improves sleep and memory consolidation, wrote the authors. “These results encourage our future research into the effect of rocking on a population with a sleep disorder, particularly patients with insomnia,” Bayer wrote to Alzforum. “If rocking can help this population sleep better, it will be a nice alternative or a natural complement to drugs.”

“These studies provide interesting thoughts on novel methods to improve sleep in a non-pharmacological manner,” agreed Jurgen Claassen, Radboud University Nijmegen Medical Center, the Netherlands. While the findings are not directly applicable to neurodegenerative diseases, they hint at a possible method of prevention, given that sleep has been demonstrated to help clear amyloid-forming proteins, improve memory, and bolster neurons (Jan 2018 news; Dec 2017 conference news). Sleep also benefits heart health. “Long-term improvement of sleep may turn out to be a factor that can reduce future risk of dementia, by reducing cardiovascular risk and thereby the effects of cardiovascular disease on dementia, and potentially by beneficial effects on amyloid and tau accumulation,” Claassen wrote.

But how would rocking improve sleep? Scientists had long hypothesized that it stimulated the vestibular system, the inner-ear mechanism that senses motion and the position of the head relative to gravity to maintain balance and posture (Korner et al., 1982; Woodward et al., 1990). However, no one had yet tested that idea. To do that, Franken and colleagues designed a companion study in mice. First author Konstantinos Kompotis first confirmed that rocking improved sleep in mice as well as humans. They hooked up C57BL/6J mice to an EEG monitor and placed them in individual cages on a rocking platform. The platform moved laterally in both directions at an adjustable speed (see diagram below). During a 12-hour lights-on period, which is when mice slumber, those that rocked at a speed of 1.0 Hz spent 40 more minutes in NREM sleep and woke less often than those that were stationary. They also fell asleep in half the time—just 10 minutes on average, as opposed 20 when they were still.

To see if vestibular stimulation was involved, Kompotis turned to the tilted mouse, in which a homozygous mutation in the tlt gene prevents functional otoliths forming in the inner ear. Normally, head motion causes these tiny crystals (otoconia) of mostly calcium to titillate the fine cilia in the ear that sense movement. Without otoliths, the brain cannot sense linear acceleration. Indeed, tlt-negative mice did not respond to rocking, sleeping only as well as stationary littermates without the mutation.

Kompotis suspects that the rhythmic back-and-forth sensed by otoliths travels to the vestibular nuclei in the brain stem, from where it transmits to other brainstem structures linked to sleep regulation, such as the pedunculopontine tegmentum nucleus. The PPT, in turn, projects to the thalamus and hippocampus, which are responsible for generating sleep-related oscillations.

“This is one of the few papers that has used rocking stimulation to modify sleep architecture,” Thanh Dang-Vu, Concordia University, Montreal, told Alzforum. “That the authors have convergent findings between human and animal studies makes a strong case that this phenomenon is conserved across species and has important biological underpinnings.” The next step will be to replicate the findings in a larger sample and extend them to other populations, for instance older individuals and those with sleep disorders, he said.—Gwyneth Dickey Zakaib

Comments

1. • David Holtzman
     Washington University
   • Posted: 25 Jan 2019

   I found both of these papers fascinating. It is convincing that rocking in the young adult humans assessed increased NREM sleep, particularly stage 3, which is where the most slow-wave activity occurs. It also increased slow-wave oscillations and fast spindles, which coincided with improved memory. Given the beneficial effect of slow-wave sleep on memory, the fact that we all have less and less slow-wave sleep with normal aging, and the likely beneficial effects of slow-wave sleep on decreasing proteins linked to AD pathogenesis, it would be really interesting to see the effect of rocking on NREM sleep and similar parameters measured here in middle-aged and elderly people. If it has effects there, this is something practical that should potentially be further explored more broadly as a potential treatment. The paper in mice nicely shows the effect of rocking/moving on sleep is via the vestibular system. Very cool.

   View all comments by David Holtzman

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References

News Citations

1. Tau, More than Aβ, Affects Sleep Early in Alzheimer’s 12 Jan 2019
2. Disturbed Sleep Exerts Toll on Memory and Neurodegeneration 21 Dec 2017
3. Skimping on Sleep Makes For More Aβ in the Brain 15 Jan 2018

Paper Citations

1. Bayer L, Constantinescu I, Perrig S, Vienne J, Vidal PP, Mühlethaler M, Schwartz S. Rocking synchronizes brain waves during a short nap. Curr Biol. 2011 Jun 21;21(12):R461-2. PubMed.
2. Korner AF, Ruppel EM, Rho JM. Effects of water beds on the sleep and motility of theophylline-treated preterm infants. Pediatrics. 1982 Dec;70(6):864-9. PubMed.
3. Woodward S, Tauber ES, Spielmann AJ, Thorpy MJ. Effects of otolithic vestibular stimulation on sleep. Sleep. 1990 Dec;13(6):533-7. PubMed.

Further Reading

Papers

1. Besnard S, Tighilet B, Chabbert C, Hitier M, Toulouse J, Le Gall A, Machado ML, Smith PF. The balance of sleep: Role of the vestibular sensory system. Sleep Med Rev. 2018 Dec;42:220-228. Epub 2018 Sep 8 PubMed.
2. Cellini N, Mednick SC. Stimulating the sleeping brain: Current approaches to modulating memory-related sleep physiology. J Neurosci Methods. 2018 Nov 16; PubMed.

News

1. Does Amyloid Accumulate After a Single Sleepless Night? 18 Apr 2018
2. Does Daytime Drowsiness Foreshadow Aβ Accumulation? 16 Mar 2018
3. Faulty Brain Clocks Precede Alzheimer’s, May Drive Pathology 14 Feb 2018
4. Skimping on Sleep Makes For More Aβ in the Brain 15 Jan 2018