Sleep, like food and drink, is a basic requirement. Keith Hengen, an assistant professor of biology at Washington University in St. Louis, says that without it, you will die.
But what exactly does sleep accomplish? For years, most academics could say that sleep reduces sleepiness, which is hardly a satisfactory explanation for a core human requirement.
However, by combining notions from physics and biology, Hengen and his colleagues have developed a theory that could explain both the significance of sleep and the complexity of the brain. In a new study, they analyzed the brain activity of sleeping rats to argue that the brain has to reset its operating system on a regular basis to achieve “criticality,” a state that enhances thinking and processing.
“The brain is like a biological computer. Memory and experience during waking change the code bit by bit, slowly pulling the larger system away from an ideal state. The central purpose of sleep is to restore an optimal computational state,”
Hengen said.
Credit: Nature Neuroscience (2024). DOI: 10.1038/s41593-023-01536-9
Random and Regular
Ralf Wessel, a professor of physics, Yifan Xu, a graduate student in biology studying neuroscience, and Aidan Schneider, a graduate student in the Computational & Systems Biology program, all from Arts & Sciences, are co-authors on the paper.
Wessel stated that physicists have been thinking about criticality for more than 30 years, but they never imagined their research would have an impact on sleep. In physics, criticality refers to a complicated system that lies at the boundary between order and chaos.
“At one extreme, everything is completely regular. At the other extreme, everything is random,”
Wessel said.
Criticality maximizes information encoding and processing, making it an appealing candidate for a universal concept of neurobiology. Hengen and Wessel argued in a 2019 study that the brain actively attempts to maintain criticality.
Systems-level Solution
The team’s latest article provides the first direct evidence that sleep restores the brain’s computing power. It is a major break from the long-held belief that sleep must replenish enigmatic and unknown substances depleted during waking hours.
After their 2019 paper, Hengen and Wessel theorized that learning, thinking, and being awake must push the brain away from criticality and that sleep is perfectly positioned to reset the system.
We realized this would be a really cool and intuitive explanation for the core purpose of sleep. Sleep is a systems-level solution to a systems-level problem,”
Hengen said.
Neural Avalanches
To put their theory about the role of criticality in sleep to the test, the researchers monitored the spiking of many neurons in the brains of young rats as they went about their normal sleeping and waking routines.
“You can follow these little cascades of activity through the neural network,”
Hengen said.
He said these cascades, also called neural avalanches, reflect how information flows through the brain.
“At criticality, avalanches of all sizes and durations can occur. Away from criticality, the system becomes biased toward only small avalanches or only large avalanches. This is analogous to writing a book and only being able to use short or long words.”
Resetting Brain Criticality
Avalanches of various proportions occurred in the rats who had just awoken from restorative sleep, as predicted. During the course of awakening, the cascades began to shrink to ever-smaller proportions.
The researchers discovered that by tracking the distribution of avalanches, they could anticipate when rats were about to sleep or wake up. Sleep was not far away when cascade sizes were lowered to a certain point.
The results suggest that every waking moment pushes relevant brain circuits away from criticality, and sleep helps the brain reset,
Hengen said.
Self-organized Complexity
When physicists first developed the concept of criticality in the late 1980s, they were looking at piles of sand on a checkerboard-like grid, a scenario that appeared to be far removed from brains.
But those sand piles provided an important insight, Wessel said. If thousands of grains are dropped on the grid following simple rules, the piles quickly reach a critical state where interesting things start happening. Large and small Avalanches can start without warning, and piles in one square start spilling into the others.
“The whole system organizes itself into something extremely complex,”
he said.
Wessel compared the neuronal avalanches that occur in the brain to sand avalanches on a grid. Cascades are the hallmark of a system that has achieved its maximum complex state in each situation.
According to Hengen, every neuron is like an individual grain of sand following very basic rules. Neurons are essentially on/off switches that decide whether or not to fire based on straightforward inputs.
If billions of neurons can reach criticality — the balance point between too much order and too much chaos — they can collaborate to create something complex and wondrous.
“Criticality maximizes a bunch of features that sound very desirable for a brain,”
Hengen said.
Abstract
Sleep is assumed to subserve homeostatic processes in the brain; however, the set point around which sleep tunes circuit computations is unknown. Slow-wave activity (SWA) is commonly used to reflect the homeostatic aspect of sleep; although it can indicate sleep pressure, it does not explain why animals need sleep. This study aimed to assess whether criticality may be the computational set point of sleep. By recording cortical neuron activity continuously for 10–14 d in freely behaving rats, we show that normal waking experience progressively disrupts criticality and that sleep functions to restore critical dynamics. Criticality is perturbed in a context-dependent manner, and waking experience is causal in driving these effects. The degree of deviation from criticality predicts future sleep/wake behavior more accurately than SWA, behavioral history or other neural measures. Our results demonstrate that perturbation and recovery of criticality is a network homeostatic mechanism consistent with the core, restorative function of sleep.
Reference:
- Xu, Y., Schneider, A., Wessel, R. et al. Sleep restores an optimal computational regime in cortical networks. Nat Neurosci (2024). Doi: 10.1038/s41593-023-01536-9