Sequence action representations contextualize during early skill learning

Activities of daily living rely on our ability to acquire new motor skills composed of precise action sequences. Here, we asked in humans if the millisecond-level neural representation of an action performed at different contextual sequence locations within a skill differentiates or remains stable during early motor learning. We first optimized machine learning decoders predictive of sequence-embedded finger movements from magnetoencephalographic (MEG) activity. Using this approach, we found that the neural representation of the same action performed in different contextual sequence locations progressively differentiated-primarily during rest intervals of early learning (offline)-correlating with skill gains. In contrast, representational differentiation during practice (online) did not reflect learning. The regions contributing to this representational differentiation evolved with learning, shifting from the contralateral pre- and post-central cortex during early learning (trials 1-11) to increased involvement of the superior and middle frontal cortex once skill performance plateaued (trials 12-36). Thus, the neural substrates supporting finger movements and their representational differentiation during early skill learning differ from those supporting stable performance during the subsequent skill plateau period. Representational contextualization extended to Day 2, exhibiting specificity for the practiced skill sequence. Altogether, our findings indicate that sequence action representations in the human brain contextually differentiate during early skill learning, an issue relevant to brain-computer interface applications in neurorehabilitation.