Differential state-dependence of low and high firing neurons in the hippocampus
Recent evidence suggests that low and high firing neurons display different plasticity and dynamics. Here, we assess how neuronal firing changes across brain states in both the hippocampus and frontal cortices of rats. To do so, we rank-ordered rat hippocampal CA1 and frontal cortical units by their firing rates and implemented corrections to account for regression-to-the-mean. We observed remarkably consistent effects across these regions. In both regions firing rates increased during rapid eye movement (REM) sleep, but with relatively larger increases in high-firing versus low-firing cells accompanied by increased interneuron spiking, indicative of competitive interactions. In contrast, upon non-REM (NREM) sleep, inhibitory firing decreased, and low-firing rate neurons showed larger increases in firing compared to high-firing neurons. These state changes resulted in narrowing of firing rate distributions during each NREM episode with subsequent dispersion of distributions during REM. Following these undulations in variance over the course of sleep, the net effect of sleep was a decrease in firing-rates across all cells, which had a stronger relative effect on lower-firing neurons. Our results suggest greater plasticity in low-firing neurons and indicate that NREM sleep plays a uniquely normalizing role in sleep, while REM sleep disperses firing rates through competitive interactions.\n\nSignificance StatementMiyawaki and colleagues analyze firing patterns separately in the hippocampus and the neocortex within and across sleep. They find that in both regions REM sleep activity is dominated by high-firing neurons and increased inhibition, resulting in a wider distribution of firing rates. On the other hand, NREM sleep produces lower inhibition, and results in a more homogenous distribution of firing rates. These findings provide insights into the effects and functions of different sleep stages on cortical neurons.