Chaotic Dynamics Mediate Brain State Transitions, Driven by Changes in Extracellular Ion Concentrations

Cell Syst. 2017 Dec 27;5(6):591-603.e4. doi: 10.1016/j.cels.2017.11.011. Epub 2017 Dec 13.

Abstract

Previous studies have suggested that changes in extracellular ion concentrations initiate the transition from an activity state that characterizes sleep in cortical neurons to states that characterize wakefulness. However, because neuronal activity and extracellular ion concentrations are interdependent, isolating their unique roles during sleep-wake transitions is not possible in vivo. Here, we extend the Averaged-Neuron model and demonstrate that, although changes in extracellular ion concentrations occur concurrently, decreasing the conductance of calcium-dependent potassium channels initiates the transition from sleep to wakefulness. We find that sleep is governed by stable, self-sustained oscillations in neuronal firing patterns, whereas the quiet awake state and active awake state are both governed by irregular oscillations and chaotic dynamics; transitions between these separable awake states are prompted by ionic changes. Although waking is indicative of a shift from stable to chaotic neuronal firing patterns, we illustrate that the properties of chaotic dynamics ensure that the transition between states is smooth and robust to noise.

Keywords: chaos; ions; modeling; sleep; state transition; wakefulness.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / physiology*
  • Electrophysiological Phenomena
  • Extracellular Space
  • Humans
  • Ions / metabolism
  • Models, Neurological*
  • Neurons / physiology*
  • Potassium Channels / metabolism*
  • Sleep*
  • Wakefulness*

Substances

  • Ions
  • Potassium Channels