Early skill learning is expressed through selection and tuning of cortically represented muscle synergies

Skill learning may be based on integrating and adapting movement building blocks organized in the CNS. We examined at what level integration and adaptation occur during early skill learning, the level of individual muscles, muscle synergies or combinations of synergies through time, and whether these operations are expressed through the primary motor cortex (M1). Forelimb muscle and M1 cell activity were recorded over the first day of training on a reach-to-grasp task in rodents. Independent components analysis was used to assess how well muscle activation patterns could be described as time-varying combinations of synergies. In 3 of 11 animals, prereach M1 activity predicted the activation of different combinations of independent components (ICs) to perform the task. With training, animals increasingly adopted postures and prereach patterns of M1 activity that supported activation of the more successful combination. With training, animals also adjusted the activation magnitude (6 of 11 animals) and weights (11 of 11) of specific ICs that constituted the selected combination. Weights represent how IC activation patterns were distributed to forelimb muscles; this distribution pattern was adapted with training. M1 cells (37 of 100) had task-related firing rates that were significantly correlated with IC activation patterns. Changes in M1 firing rates were associated with corresponding changes in either the activation magnitude or weights of the correlated IC. Our data suggest that early skill learning is expressed through selection and tuning of M1 firing rates, which specify time-varying patterns of synergistic muscle contractions in the limb.