Entrainment to sleep spindles reflects dissociable patterns of connectivity between cortex and basal ganglia

Abstract

Communication between the basal ganglia (BG) and cortex is crucial for behavior as it allows learning through external reinforcement. Non-REM sleep benefits learning in the corticostriatal system through the sleep spindle-associated reactivation of previously active neuronal ensembles and the subsequent modification of synaptic weights. However, how sleep spindles coordinate cross-region spiking, and whether spindle-driven reactivation occurs in other BG structures, remains unknown. We recorded field potentials (FP) and spiking activity in cortex and BG during sleep in two non-human primates immediately following a task that involved the learning of new cue-reward contingencies. FP sleep spindles were widespread in the BG, and they were similar to cortical spindles in morphology, spectral content and response to learning prior to sleep. Further, BG FP spindles were concordant with EEG spindles and associated with increased cortico-BG correlation. However, spindles across the BG differed markedly in their entrainment of local spiking. The spiking activity of striatal projection neurons exhibited consistent phase locking to striatal FP spindles and EEG spindles, producing phase windows of peaked cross-region spindling. In contrast, in the subthalamic nucleus (STN), which like the striatum receives substantial thalamocortical input, and in BG nuclei downstream to the striatum and STN, neuronal firing was not entrained to either local or EEG sleep spindles. These results dissociate striatal projection neurons from the rest of the BG, and suggest corticostriatal synapses as the main hub for offline communication between cortex and BG.

Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease

“…In healthy primates, basal ganglia neurons have been shown to exhibit slow oscillations in firing similar to those observed in cortical neurons (Mizrahi-Kliger et al, 2018). Recording of local field potentials (LFPs) in the basal ganglia demonstrate dramatically reduced slow oscillations compared with thalamocortical networks (Mizrahi-Kliger et al, 2018). In the 1-methyl-4-phenyl-1,2,3,6tetrahydropyridine (MPTP) primate model of parkinsonism, increased power in the alpha and low beta range (10-17 Hz) during NREM was seen in GPe, GPi, and STN (Mizrahi-Kliger et al, 2020).…”

“…Although a definite pathophysiological mechanism remains elusive, a growing body of evidence implicates the basal ganglia as an important node in a brainwide network critical for the maintenance of sleep (Liu and Dan, 2019). In healthy primates, basal ganglia neurons have been shown to exhibit slow oscillations in firing similar to those observed in cortical neurons (Mizrahi-Kliger et al, 2018). Recording of local field potentials (LFPs) in the basal ganglia demonstrate dramatically reduced slow oscillations compared with thalamocortical networks (Mizrahi-Kliger et al, 2018).…”