Natural Waking and Sleep States: A View From Inside Neocortical Neurons

TLDR

The study aimed to determine how natural waking and sleep states influence neocortical neuron electrophysiology, contrasting with prior anesthetized or slice preparations. The authors recorded intracellular activity in awake cats, quantifying firing patterns, membrane potential fluctuations, firing rates, and input resistance across wakefulness, REM, and slow‑wave sleep. Fast‑spiking neurons dominated during wakefulness, while intrinsically bursting neurons were rarer than in anesthetized preparations; firing rates during depolarizing phases of slow‑wave sleep matched those of wake and REM, and maximum rates exceeded regular‑spiking neurons in both states, with input resistance rising during quiet wakefulness due to neuromodulator release, implying that neocortical neurons process internally generated signals even in slow‑wave sleep.

Abstract

In this first intracellular study of neocortical activities during waking and sleep states, we hypothesized that synaptic activities during natural states of vigilance have a decisive impact on the observed electrophysiological properties of neurons that were previously studied under anesthesia or in brain slices. We investigated the incidence of different firing patterns in neocortical neurons of awake cats, the relation between membrane potential fluctuations and firing rates, and the input resistance during all states of vigilance. In awake animals, the neurons displaying fast-spiking firing patterns were more numerous, whereas the incidence of neurons with intrinsically bursting patterns was much lower than in our previous experiments conducted on the intact-cortex or isolated cortical slabs of anesthetized cats. Although cortical neurons displayed prolonged hyperpolarizing phases during slow-wave sleep, the firing rates during the depolarizing phases of the slow sleep oscillation was as high during these epochs as during waking and rapid-eye-movement sleep. Maximum firing rates, exceeding those of regular-spiking neurons, were reached by conventional fast-spiking neurons during both waking and sleep states, and by fast-rhythmic-bursting neurons during waking. The input resistance was more stable and it increased during quiet wakefulness, compared with sleep states. As waking is associated with high synaptic activity, we explain this result by a higher release of activating neuromodulators, which produce an increase in the input resistance of cortical neurons. In view of the high firing rates in the functionally disconnected state of slow-wave sleep, we suggest that neocortical neurons are engaged in processing internally generated signals.