Regulation of Hippocampal Firing by Network Oscillations during Sleep

It has been hypothesized that waking leads to higher-firing neurons, with increased energy expenditure, and that sleep serves to return activity to baseline levels. Oscillatory activity patterns during different stages of sleep may play specific roles in this process, but consensus has been missing. To evaluate these phenomena in the hippocampus, we recorded from region CA1 neurons in rats across the 24-hr cycle, and we found that their firing increased upon waking and decreased 11% per hour across sleep. Waking and sleeping also affected lower- and higher-firing neurons differently. Interestingly, the incidences of sleep spindles and sharp-wave ripples (SWRs), typically associated with cortical plasticity, were predictive of ensuing firing changes and were more robustly predictive than other oscillatory events. Spindles and SWRs were initiated during non-REM sleep, yet the changes were incorporated in the network over the following REM sleep epoch. These findings indicate an important role for spindles and SWRs and provide novel evidence of a symbiotic relationship between non-REM and REM stages of sleep in the homeostatic regulation of neuronal activity.