Infraslow coordination of slow wave activity through altered neuronal synchrony

Abstract

Slow wave activity (SWA; the EEG power between 0.5 and 4 Hz during non-rapid eye movement sleep [NREM]) is the best electrophysiological marker of sleep need; SWA dissipates across the night and increases following sleep deprivation. In addition to these well-documented homeostatic SWA trends, SWA exhibits extensive variability across shorter timescales (seconds to minutes) and between local cortical regions. The physiological underpinnings of SWA variability, however, remain poorly characterized. In male Sprague-Dawley rats, we observed that SWA exhibits pronounced infraslow fluctuations (∼40- to 120-s periods) that are coordinated across disparate cortical locations. Peaks in SWA across infraslow cycles were associated with increased slope, amplitude, and duration of individual slow waves and a reduction in the total number of waves and proportion of multipeak waves. Using a freely available data set comprised of extracellular unit recordings during consolidated NREM episodes in male Long-Evans rats, we further show that infraslow SWA does not appear to arise as a consequence of firing rate modulation of putative excitatory or inhibitory neurons. Instead, infraslow SWA was associated with alterations in neuronal synchrony surrounding "On"/"Off" periods and changes in the number and duration of "Off" periods. Collectively, these data provide a mechanism by which SWA can be coordinated across disparate cortical locations and thereby connect local and global expression of this patterned neuronal activity. In doing so, infraslow SWA may contribute to the regulation of cortical circuits during sleep and thereby play a critical role in sleep function.