Sensory coding of limb kinematics in developing primary motor cortex

Abstract

Primary motor cortex (M1) undergoes protracted development in rodents, functioning initially as a sensory structure. As we reported previously in neonatal rats (Dooley and Blumberg, 2018), self-generated forelimb movements—especially the twitch movements that occur during active sleep—trigger sensory feedback (reafference) that strongly activates M1. Here, we expand our investigation by using a video-based approach to quantify the kinematic features of forelimb movements with sufficient precision to reveal receptive-field properties of individual M1 units. At postnatal day (P) 8, nearly all M1 units were strongly modulated by movement amplitude, but only during active sleep. By P12, the majority of M1 units no longer exhibited amplitude-dependence, regardless of sleepwake state. At both ages, movement direction produced changes in M1 activity, but to a much lesser extent than did movement amplitude. Finally, we observed that population spiking activity in M1 becomes more continuous and decorrelated between P8 and P12. Altogether, these findings reveal that M1 undergoes a sudden transition in its receptive field properties and population-level activity during the second postnatal week. This transition marks the onset of the next stage in M1 development before the emergence of its later-emerging capacity to influence motor outflow.