Entrained cortical delta-spindle activity, not periodic synchrony, prevents arousal by NREM thalamic bursts

Thalamic neurons discharge tonically during wakefulness and rapid-eye-movement (REM) sleep, but switch to burst firing during non-REM (NREM) sleep. It has been hypothesized that NREM thalamic bursts do not serve as a cortical "wake-up" signal due to their periodic and synchronized nature. Here, we analyze the simultaneously recorded polysomnographic signals, field potentials, and spiking activity of neurons in the ventral anterior and centromedian thalamic nuclei of two female non-human primates during naturally occurring vigilance states. These nuclei receive GABAergic output from the basal ganglia, with discharge rate decreasing during NREM sleep. Despite this reduction in inhibitory input, NREM bursting increases significantly as reported for glutamate-driven thalamic nuclei.  The NREM bursts are neither periodic nor tightly synchronized. However, delta and sleep-spindle EEG activity and thalamic field potentials time-locked to burst onset during NREM sleep markedly differ from those observed during wakefulness and REM sleep. These results suggest that the basal ganglia modulate, rather than drive, their thalamic targets. Additionally, unique state-dependent thalamocortical dynamics, rather than the periodicity or tight synchrony of the thalamic bursts, are sufficient to account for why NREM thalamic bursts do not awaken the cortex.