SUMMARY The most prominent EEG events in sleep are slow waves, reflecting a slow (<1 Hz) oscillation between up and down states in cortical neurons. It is unknown whether slow oscillations are synchronous across the majority or the minority of brain regions—are they a global or local phenomenon? To examine this, we recorded simultaneously scalp EEG, intracerebral EEG, and unit firing in multiple brain regions of neurosurgical patients. We find that most sleep slow waves and the underlying active and inactive neuronal states occur locally. Thus, especially in late sleep, some regions can be active while others are silent. We also find that slow waves can propagate, usually from medial prefrontal cortex to the medial temporal lobe and hippocampus. Sleep spindles, the other hallmark of NREM sleep EEG, are likewise predominantly local. Thus, intracerebral communication during sleep is constrained because slow and spindle oscillations often occur out-of-phase in different brain regions.

SUMMARY The need to sleep grows with the duration of wakefulness and dissipates with time spent asleep, a process called sleep homeostasis. What are the consequences of staying awake on brain cells, and why is sleep needed? Surprisingly, we do not know whether the firing of cortical neurons is affected by how long an animal has been awake or asleep. Here we found that after sustained wakefulness cortical neurons fire at higher frequencies in all behavioral states. During early NREM sleep after sustained wakefulness, periods of population activity (ON) are short, frequent, and associated with synchronous firing, while periods of neuronal silence are long and frequent. After sustained sleep, firing rates and synchrony decrease, while the duration of ON periods increases. Changes in firing patterns in NREM sleep correlate with changes in slow-wave-activity, a marker of sleep homeostasis. Thus, the systematic increase of firing during wakefulness is counterbalanced by staying asleep.

No abstract

When the brain is awake, neurons in the cerebral cortex fire irregularly and the electroencephalogram (EEG) displays low amplitude, high frequency fluctuations. After falling asleep, neurons start oscillating between ON periods, when they fire as during wake, and OFF periods, when they stop firing altogether, and the EEG displays high amplitude slow waves. But what happens to neuronal firing after a long period of wake? We show here in freely behaving rats that, after prolonged wake, cortical neurons can go briefly “OFF line” as they do in sleep, accompanied by slower waves in the local EEG. Strikingly, neurons often go OFF line in one cortical area and not in another. During these periods of “local sleep”, whose incidence increases with wake duration, rats appear awake, active, and display a wake EEG. However, they are progressively impaired in a sugar pellet reaching task. Thus, though both the EEG and behavior indicate wakefulness, local populations of neurons in the cortex may be falling asleep, with negative consequences on performance.

In the human EEG, the decline of SWA during sleep is accompanied by changes in slow-wave parameters that were predicted by a computer model simulating a homeostatic reduction of cortical synaptic strength.