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Sleep as a fundamental property of neuronal assemblies

Nature Reviews Neuroscience volume 9, pages 910919 (2008) | Download Citation

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Abstract

Sleep is vital to cognitive performance, productivity, health and well-being. Earlier theories of sleep presumed that it occurred at the level of the whole organism and that it was governed by central control mechanisms. However, evidence now indicates that sleep might be regulated at a more local level in the brain: it seems to be a fundamental property of neuronal networks and is dependent on prior activity in each network. Such local-network sleep might be initiated by metabolically driven changes in the production of sleep-regulatory substances. We discuss a mathematical model which illustrates that the sleep-like states of individual cortical columns can be synchronized through humoral and electrical connections, and that whole-organism sleep occurs as an emergent property of local-network interactions.

Key points

  • Sleep is a fundamental property of neuronal assemblies such as cortical columns.

  • Sleep is regulated in a neuronal-assembly use-dependent manner.

  • The mechanisms that underlie neuronal-assembly sleep include enhanced activity of sleep-regulatory substances, induced by neuronal use-enhanced metabolism.

  • A mathematical model of loosely connected neuronal assemblies shows that they synchronize their sleep-like and awake-like states.

  • Sleep probably evolved from a metabolically quiescent rest state.

  • Sleep seems to function to stabilize instinctual and learned memories.

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Acknowledgements

This work was supported by the W.M. Keck Foundation, the US National Institutes of Health (grant numbers NS 25378, NS 31453 and MH 71830), the US Army Research Development and Material Command, the National Science Foundation, and the National Aeronautics and Space Administration.

Author information

Affiliations

  1. Department of VCAPP, College of Veterinary Medicine, Washington State University, PO BOX 646520, Pullman, Washington 99164-6520, USA.

    • James M. Krueger
  2. Sleep and Performance Research Center and Programs in Neuroscience, Washington State University, Pullman and Spokane, Washington 99164-6520, USA.

    • James M. Krueger
    • , David M. Rector
    • , Hans P. A. Van Dongen
    • , Gregory Belenky
    •  & Jaak Panksepp
  3. Electrical Engineering, Washington State University, Pullman and Spokane, Washington 99164-6520, USA.

    • Sandip Roy

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Corresponding author

Correspondence to James M. Krueger.

Glossary

Cortical columns

Collections of highly interconnected neurons that often focus on particular tasks. Columns are layered structures, and the individual layers are concerned with different functions, such as the receipt of afferent input and producing an output. There is more intercellular connectivity within columns than between columns. This makes each column a functional unit. In humans, each column contains 1,000–10,000 cells and there are 100,000 cortical columns.

Parasomnias

States in which behavioural or physical phenomena that are characteristic of waking occur while parts of the body seem to be asleep. Sleep walking is a well-known example of a parasomnia.

Non-rapid-eye-movement sleep

(NREMS). A type of sleep characterized by high-amplitude (up to 500 μV) electroencephalographic slow waves (delta waves). In humans it is often divided into four stages, the first two of which are characterized less by delta waves than by a transition from fast to slower electroencephalographic activity. In intermediate stages of NREMS, thalamic cells produce 8–12 Hz bursts known as spindles, which also characterize lighter stages of NREMS.

Delta-wave power

The calculated power (in μV2) of delta waves, obtained from fast fourier transformations of the EEG. Delta waves are from 0.5–3.5 Hz. Delta-wave power is higher during sleep after sleep deprivation and is considered an indicator of NREMS intensity. Delta waves are generated by the synchronous and cyclical switching of cortical cells between a hyperpolarized and a depolarized state. Although this rhythm is present in isolated cortical slices, similar rhythms occur in the thalamus and might drive the cortical cells into alternating hyperpolarized and depolarized states.

Rapid-eye-movement sleep

A state characterized by a relatively fast waveform EEG and a flat electromyogram in postural muscles. This state is also well known for the vivid dreams that can be remembered.

Evoked response potentials

The field potentials measured from electrodes on the surface of the cerebral cortex or scalp that occur in response to sensory afferent stimulation. Synchronous synaptic activation of many cells in a cortical column generates an electrical potential gradient that can be detected by the electrodes. By using multiple electrodes and/or discrete sensory stimuli, these potentials can be localized to individual cortical columns.

Clock mechanisms of the suprachiasmatic nuclei

In mammals the suprachiasmatic nuclei of the hypothalamus house the cellular and molecular mechanisms that are responsible for circadian rhythms. If the suprachiasmatic nuclei are lesioned, circadian rhythms that are normally entrained by light are lost. In the absence of light–dark cues, normal animals exhibit rhythms that approximate 24 hours through the actions of the free-running molecular oscillators in the suprachiasmatic cells.

Sleep-active neurons

Neurons with activity that increases during sleep or just before sleep onset.

Wake-active neurons

Neurons with activity that increases during wakefulness or just before wakefulness onset.

Hebbian plasticity

The type of rapid (on the scale of minutes to hours) changes in neuronal connectivity that are associated with use of the network of which the neurons are a part. The term is derived from the work of Donald Hebb, a Canadian psychologist who first posited, in 1949, that neurons that fire together tend to wire together.

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https://doi.org/10.1038/nrn2521

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