Why bursts in thalamic nuclei receiving basal ganglia output fail to wake the cortex during sleep?

Thalamic neurons discharge tonically during wakefulness and rapid-eye-movement (REM) sleep, but burst 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. To explore this hypothesis, we studied polysomnographic signals, field potentials, and spiking activity of multiple 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. Nevertheless, NREM bursting increased significantly as reported for glutamate-driven thalamic nuclei. NREM bursts were neither periodic nor tightly synchronized. However, EEG activity and thalamic field potentials time-locked to burst onset during NREM sleep markedly differed from those observed during wakefulness and REM sleep. These results suggest that NREM thalamic bursts do not awaken the cortex, due to unique state-dependent thalamocortical dynamics.