Sequential Neural Activity in Primary Motor Cortex during Sleep

Sequential firing of neurons during sleep is thought to play a role in the consolidation of learning. However, direct evidence for such sequence replay is limited to only a few brain areas and sleep states mainly in rodents. Using a custom-designed wearable neural data logger and chronically implanted electrodes, we made long-term recordings of neural activity in the primary motor cortex of two female nonhuman primates during free behavior and natural sleep. We used the local field potential (LFP) spectrogram to characterize sleep cycles, and examined firing rates, correlations, and sequential firing of neurons at different frequency bands through the cycle. Slow-wave sleep (SWS) was characterized by low neural firing rates and high synchrony, reflecting slow oscillations between cortical down and up states. However, the order in which neurons entered up states was similar to the sequence of neural activity observed at low frequencies during waking behavior. In addition, we found evidence of brief bursts of theta oscillation, associated with non-SWS states, during which neurons fired in strikingly regular sequential order phase-locked to the LFP. Theta sequences were preserved between waking and sleep, but appeared not to resemble the order of neural activity observed at lower frequencies. The sequential firing of neurons during slow oscillations and theta bursts may contribute to the consolidation of procedural memories during sleep. SIGNIFICANCE STATEMENT Replay of sequential neural activity during sleep is believed to support consolidation of daytime learning. Despite a wealth of studies investigating sequential replay in association with episodic and spatial memory, it is unknown whether similar sequences occur in motor areas during sleep. Within long-term neural recordings from monkey motor cortex, we found two distinct patterns of sequential activity during different phases of the natural sleep cycle. Slow-wave sleep was associated with delta-band sequences that resembled low-frequency activity during movement, while occasional brief bursts of theta oscillation were associated with a different order of sequential firing. Our results are the first report of sequential sleep replay in the motor cortex, which may play an important role in consolidation of procedural learning.