ETD

• Closed-Loop Neurotechnology
• Macaque
• Neuronal Assemblies
• NREM
• REM
• Sleep Replays
• The Motor Cortex

Neuronal assemblies, groups of co-active neurons representing sensory, motor, or cognitive states, are well-studied in other cortical areas, but their temporal structure and function in the motor cortex are poorly understood. In this study, we investigated cell assemblies of the ventral premotor and primary motor cortex of two macaques engaged in a grasping task, free movements, and during the subsequent sleep phases. During wakefulness, assemblies coordinated neural activity in diverse, context-dependent timescales. During sleep, recruitment patterns were phase-specific: REM assemblies coordinated activity with fast precision (about 22 ms), whereas NREM assemblies operated at slower timescales (of about 170 ms). Assemblies identified during wakefulness robustly reactivated in sleep with marked time compression, approximately sixfold in NREM and fiftyfold in REM. Replay content was recency-biased: assemblies active during free movement dominated when spontaneous behaviour preceded sleep. Cell-type analysis revealed selective unit recruitment of sleep assemblies; notably, mirror-like neurons were more frequently recruited by REM and NREM assemblies. Finally, analysis of the activation patterns of assembly's units revealed state-dependent directionality of activation. Ventral premotor neurons led primary motor neurons during task acting whereas the directionality reversed during REM sleep. These results show that motor commands in non-human primates are encoded through dynamically organized neuronal assemblies with rich temporal diversity. During sleep, these assemblies undergo time-compressed and directionally reconfigured replay, preferentially reactivating the most recent waking experience.