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

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.

Competitive state of movements during planning predicts sequence performance.

Humans can learn and produce skilled movement sequences from memory, yet the nature of sequence planning is not well understood. Previous computational and neurophysiological work suggests that movements in a sequence are planned as parallel graded activations and selected for output through competition. However, the relevance of this planning pattern to sequence production fluency and accuracy, as opposed to the temporal structure of sequences, is unclear. To resolve this question, we assessed the relative availability of constituent movements behaviorally during the preparation of motor sequences from memory. In three separate multisession experiments, healthy participants were trained to retrieve and produce four-element finger press sequences with particular timing according to an abstract sequence cue. We evaluated reaction time (RT) and error rate as markers of movement availability to constituent movement probes. Our results demonstrate that longer preparation time produces more pronounced differences in availability between adjacent sequence elements, whereas no effect was found for sequence speed or temporal grouping. Further, participants with larger position-dependent differences in movement availability tended to initiate correct sequences faster and with a higher temporal accuracy. Our results suggest that competitive preactivation is established gradually during sequence planning and predicts sequence skill, rather than the temporal structure of the motor sequence.NEW & NOTEWORTHY Sequence planning is an integral part of motor sequence control. Here, we demonstrate that the competitive state of sequential movements during sequence planning can be read out behaviorally through movement probes. We show that position-dependent differences in movement availability during planning reflect sequence preparedness and skill but not the timing of the planned sequence. Behavioral access to the preparatory state of movements may serve as a marker of sequence planning capacity.