Subcortically generated movements activate motor cortex during sleep and wake in rats through postnatal day 24

During early postnatal development, cortical motor control emerges from complex interactions between cortical and subcortical circuits. In primary motor cortex (M1), we know that this process depends on neural activity, but large gaps remain in our understanding of how M1 neural activity is patterned prior to the development of cortical motor control. To track the development of movement-related activity in M1 across sleep and wake, we performed acute, extracellular recordings of single-unit activity in the forelimb region of M1 of unanesthetized, head-fixed rats from postnatal day 12 (P12) to P24. At all ages, a subset of M1 neurons responded robustly and somatotopically to spontaneous limb twitches that occur during REM sleep. M1 neurons also showed robust responses to wake movements at these ages. From P12 to P24, the proportion of M1 neurons that showed twitch-related activity decreased, twitch-related activity became more temporally refined, and there was an increase in the proportion of activity that preceded movement onset. To compare M1’s developmentally nascent activity at P24 with that of an established motor structure, we performed simultaneous recordings in M1 and the red nucleus (RN). RN activity reliably preceded both twitches and wake movements, particularly compared to M1, reinforcing the conclusion that as late as P24 RN still predominantly drives limb movements. These results highlight M1’s protracted development and the continued importance of subcortically generated movements in driving activity that shapes M1’s circuitry, suggesting that movement-related activity during sleep and wake promotes the development of M1’s motor functions.