Subcortically generated movements activate motor cortex during sleep and wake in rats through postnatal day 24
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During early postnatal life, cortical motor control emerges from complex interactions between cortical and subcortical circuits. Although activity-dependent processes are essential for primary motor cortex (M1) to develop motor functions, the precise activity patterns that precede this transition remain unclear. To track the development of movement-related activity in M1, we recorded single-unit activity in the forelimb region of M1 in unanesthetized, head-fixed rats across sleep and wake at postnatal days (P) 12, 16, 20, and 24. At every age, a subset of M1 neurons showed somatotopically precise responses to spontaneous limb twitches that occur during REM sleep, along with strong responses to wake movements. From P12 to P24, the proportion of M1 neurons that showed twitch-related activity decreased, twitch-related activity became more temporally refined, and a larger fraction of spikes occurred before movement onset. To compare M1’s developmentally nascent activity with that of an established motor structure, we performed simultaneous recordings in M1 and the red nucleus (RN) at P24. Compared to M1, more RN activity preceded twitches and wake movements. Further, RN activity was more diverse, with neurons firing during specific wake movements, whereas wake-movement-related activity in M1 was largely non-selective. These results suggest that through P24, movement-related activity in M1 reflects predicted and actual sensory feedback across both sleep and wake, whereas movement-related activity in RN drives limb movements across both sleep and wake. Altogether, these data highlight the continued importance of subcortically generated movements in shaping M1’s functional organization.
Significance Statement
In adults, primary motor cortex (M1) is widely recognized for its role in initiating voluntary movements and guiding motor learning. However, during early development, our findings show that M1 processes activity related to self-generated limb movements but does not drive the production of those movements. Using simultaneous recordings from M1 and the red nucleus (RN) of developing rats, we show that although M1 shows movement-related activity during wake and sleep, RN remains the principal driver of behavior through at least postnatal day 24. These results refine our understanding of early movement-related activity and highlight the possibility that both sleep-related twitches and wake movements shape sensorimotor development by driving neural activity in M1 and RN.
