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Significance Slow-wave sleep is widely associated with synchronized slow oscillations recorded in the cortical mantle and elsewhere in the brain. In this study, we focused on the basal ganglia, a group of interconnected subcortical nuclei implicated in habit learning and in common neurological disorders (e.g., Parkinson’s disease). We show that unlike cortical circuits, where slow oscillation is locally synchronized, slow oscillations of firing rates within each basal ganglia nucleus are not phase-locked between adjacent neurons, and are decoupled from the local field potential. Our results establish that neuronal slow oscillations and synchrony do not always co-occur, and highlight decorrelation as a key feature of basal ganglia circuitry that persists even in the most synchronized physiological conditions.

Desynchronization of slow oscillations in the basal ganglia during natural sleep