Cortical Patterns Shift from Sequence Feature Separation during Planning to Integration during Motor Execution.

Abstract

Performing sequences of movements from memory and adapting them to changing task demands is a hallmark of skilled human behavior, from handwriting to playing a musical instrument. Prior studies showed a fine-grained tuning of cortical primary motor, premotor, and parietal regions to motor sequences: from the low-level specification of individual movements to high-level sequence features, such as sequence order and timing. However, it is not known how tuning in these regions unfolds dynamically across planning and execution. To address this, we trained 24 healthy right-handed human participants (14 females, 10 males) to produce four five-element finger press sequences with a particular finger order and timing structure in a delayed sequence production paradigm entirely from memory. Local cortical fMRI patterns during preparation and production phases were extracted from separate No-Go and Go trials, respectively, to tease out activity related to these perimovement phases. During sequence planning, premotor and parietal areas increased tuning to movement order or timing, regardless of their combinations. In contrast, patterns reflecting the unique integration of sequence features emerged in these regions during execution only, alongside timing-specific tuning in the ventral premotor, supplementary motor, and superior parietal areas. This was in line with the participants' behavioral transfer of trained timing, but not of order to new sequence feature combinations. Our findings suggest a general informational state shift from high-level feature separation to low-level feature integration within cortical regions for movement execution. Recompiling sequence features trial-by-trial during planning may enable flexible last-minute adjustment before movement initiation.SIGNIFICANCE STATEMENT Musicians and athletes can modify the timing and order of movements in a sequence trial-by-trial, allowing for a vast repertoire of flexible behaviors. How does the brain put together these high-level sequence features into an integrated whole? We found that, trial-by-trial, the control of sequence features undergoes a state shift from separation during planning to integration during execution across a network of motor-related cortical areas. These findings have implications for understanding the hierarchical control of skilled movement sequences, as well as how information in brain areas unfolds across planning and execution.