Motor cortex activity during sleep and wake movements sharpens across development but continues to lag the red nucleus

The development of motor control in primary motor cortex (M1) requires both movements and neural activity. In rats, cortical motor control first appears around postnatal day (P) 25, prior to which movements are generated by subcortical motor nuclei such as the red nucleus (RN). While these subcortically generated movements are thought to provide the activity that guides the development of M1, the specific movements associated with M1 activity and their somatotopic and temporal precision remain unknown. Here, we performed acute electrophysiological recordings of neural activity in the forelimb region of M1 of P12-24 rats as they cycled between sleep and wake and compared M1 and RN activity in P24 rats. At every age, M1 neurons exhibited somatopically precise activity during REM sleep twitches, along with strong activity during wake movements. From P12 to P24, the proportion of neurons exhibiting twitch-related activity decreased, twitch-related activity became more temporally refined, and a larger fraction of spikes occurred before movement onset. At P24, M1 showed less premovement activity than RN. Further, in contrast to the non-selective activity seen in M1, some RN neurons showed movement-selective activity patterns during wake, firing only during particular wake movements. These findings reveal that movement-related activity in M1 is somatotopically precise by P12 and temporally precise by P24. But M1 still lacks the strong premovement activity and selectivity characteristic of RN, suggesting that at P24, subcortical outputs remain the main drivers of M1's movement-related activity.